From Cone Contrast to Colour Perception

PERIPHERAL HUMAN COLOUR VISION; FROM CONE CONTRASTTO COLOUR PERCEPTION

A THESIS SUBMITTEDTO THE UNIVERSITYOF MANCHESTER FORTHEDEGREEOF DOCTOROF PHILOSOPHY (PHD) INTHE FACULTY OF LIFE SCIENCES

2010

ATHANASIOS PANORGIAS CONTENTS

Abstract 11

Declaration 13

Acknowledgements 16

Alternative Format Thesis 19

Rationale and aims 21

1 General introduction 23

1.1 Overview of the visual process...... 23 1.2 Physiology of the visual process...... 24 1.2.1 First stage: Photoreceptors...... 24 1.2.2 Post-receptoral neural organisation of the retina...... 28 1.2.3 Second stage: Cone opponency...... 30 1.2.4 Retino-thalamic pathways and cortex...... 33 1.3 Transformation from retina-LGN to cortex. Third stage: Colour opponency. 36 1.4 Individual variations in colour vision...... 37

2 CONTENTS

1.5 Colour perception in peripheral retina...... 39 1.6 References...... 42

2 Materials and general methods 50

2.1 Colour space...... 50 2.2 Cone fundamentals and L-, M-, S-cone activation units...... 53 2.3 Cardinal directions, chromatic axes and purity...... 55 2.4 Cone opponent model...... 58 2.5 Cone contrast...... 59 2.6 Experimental equipment and calibration procedure...... 61 2.7 Experimental procedures and colour vision tests...... 63 2.7.1 Colour vision tests...... 63 2.7.2 Asymmetric matching paradigm...... 65 2.7.3 Naming experiment...... 69 2.8 Ethics...... 70 2.9 References...... 71

3 Nasal-temporal differences in cone opponency in the near peripheral retina 73

3.1 Abstract...... 73 3.2 Introduction...... 74 3.3 Methods...... 76 3.4 Results...... 79 3.5 Discussion...... 83 3.6 References...... 87

4 Naming versus matching and the stability of unique hues 91

4.1 Abstract...... 91

3 CONTENTS

4.2 Introduction...... 92 4.3 Methods...... 95 4.3.1 Stimuli...... 95 4.3.2 Colour space...... 95 4.3.3 Observers...... 96 4.3.4 Procedures...... 97 4.4 Results...... 98 4.5 Discussion...... 102 4.6 References...... 106

5 Cone contrast in peripheral retina 109

5.1 Abstract...... 109 5.2 Introduction...... 110 5.2.1 Contrasted colours and colour constancy...... 111 5.2.2 Colour perception in the periphery...... 112 5.3 Methods...... 114 5.3.1 Colour matching...... 115 5.3.2 Colour naming...... 116 5.3.3 Cone contrast...... 116 5.4 Results...... 117 5.5 Discussion...... 122 5.5.1 Peripheral L-, M- and S-cone contrast...... 123 5.5.2 Peripheral RMS cone contrast...... 124 5.5.3 The oddity of green...... 126 5.5.4 Cone versus colour opponency...... 126 5.6 References...... 128

4 CONTENTS

6 Phases of daylight and the stability of colour perception in peripheral human retina 131

6.1 Abstract...... 131 6.2 Introduction...... 132 6.3 Methods...... 137 6.3.1 Matching experiment...... 138 6.3.2 Naming experiment...... 139 6.4 Results...... 139 6.5 Discussion...... 145 6.5.1 Invariant blue and yellow...... 146 6.5.2 Unique blue and yellow...... 146 6.5.3 Inter-observer variability...... 149 6.5.4 Conclusions...... 151 6.6 References...... 153

7 Sex-related differences in peripheral human colour vision; a colour matching study 158

7.1 Abstract...... 158 7.2 Introduction...... 159 7.3 Methods...... 164 7.4 Results...... 166 7.4.1 Hue rotation difference...... 168 7.4.2 Saturation difference...... 169 7.4.3 Chromatic channel difference...... 172 7.4.4 Female observers with wide anomaloscope matching range.... 173 7.5 Discussion...... 176

5 CONTENTS

7.6 References...... 181

8 Conclusions and future experiments 185

8.1 Conclusions...... 185 8.2 Future experiments...... 187

A CIE1976 Lu’v’ colour space 189

B Ellipses 192

B.1 References...... 195

C Non parametric statistical test for circular data 196

C.1 References...... 198

D Reprint: Nasal-temporal differences in cone opponency in the near peripheral retina. 199

E Reprint: Naming versus matching and the stability of unique hues 200

Final word count: 36633

6 LIST OF FIGURES

1.1 Cone spectral sensitivities...... 26 1.2 Cone density...... 27 1.3 The primate retinal neural circuitry...... 29 1.4 Ganglion cell receptive ﬁelds...... 32 1.5 Areas of the visual brain...... 35 1.6 Unique hues and cardinal cone opponent axes...... 37

2.1 Colour matching functions...... 51 2.2 The CIE1931 xy colour space...... 53 2.3 Smith and Pokorny (1975) cone fundamentals...... 54 2.4 CIE1931 xy colour space, cardinal axes and purity...... 56 2.5 Correspondence between chromatic axes and wavelengths...... 57 2.6 Visual channel activation...... 59 2.7 Cone contrast...... 60 2.8 Monitor calibration - xy coordinates...... 62 2.9 Monitor calibration - luminance...... 62 2.10 Stimulus conﬁguration...... 66 2.11 Colour matching results in CIE1931xy...... 67 2.12 Hue rotation and saturation match...... 68

7 LIST OF FIGURES

2.13 Naming results...... 69

3.1 Stimuli chromaticities in CIE1931 xy colour space...... 78 3.2 Nasal and temporal colour matches...... 80 3.3 Cone opponency in the nasal and temporal visual ﬁeld...... 82

4.1 The CIE1931 xy colour space and the stimuli chromaticities...... 96 4.2 Unique hue settings at 1◦ and 10◦ eccentricity...... 99 4.3 Naming and colour matching results at 18◦ eccentricity...... 100

5.1 Asymmetric peripheral colour matching; stimuli conﬁguration...... 115 5.2 Colour matching and naming results...... 118 5.3 Peripheral L-, M- and S-cone contrast...... 119 5.4 Probe versus test L-, M- and S-cone contrast for invariant and unique hues 121 5.5 Probe versus test RMS cone contrast...... 122

6.1 The CIE1931 xy colour space, stimuli chromaticities and daylight locus. 138 6.2 Colour naming functions...... 140 6.3 Colour matching results on CIE1931 xy plot...... 141 6.4 Hue rotation and saturation match...... 142 6.5 Variability ellipses...... 144 6.6 Variability around the colour space...... 145 6.7 Unique hues and daylight locus on cone space...... 148

7.1 Male and female colour matches on CIE1931xy colour space...... 167 7.2 Male and female hue rotation...... 169 7.3 Male and female saturation match...... 170 7.4 Male and female L-M channel activation...... 172 7.5 Male and female S-(L+M) channel activation...... 174

8 LIST OF FIGURES

7.6 Male and female Nagel anomaloscope data...... 175

A.1 Colour matching results on CIE1976 u’v’ plot...... 190

9 LIST OF TABLES

4.1 Unique and invariant hues at 18◦ eccentricity for two observers...... 101

6.1 Unique hues at 18◦ eccentricity for three observers...... 140

7.1 CIE1931 xy probe chromaticity coordinates...... 166

10 ABSTRACT

It is well known that the colour preferences of ganglion and LGN cells do not match the four perceptually simple colours red, green blue and yellow. It is also known that although colour perception is distorted in the peripheral visual field, there are four hues that appear stable with eccentricity. These are defined as peripherally invariant hues. Both of these observations must in some way reflect the physiological substrate of neurons at different stages of the primary visual pathway. The experiments described here are aimed at understanding the link between the physiology and the perception of colour by studying the characteristics of peripheral colour vision The following questions have been addressed: i) to what extent does colour matching rely on the retinal physiological substrate? ii) what is the reason for the discrepancy between invariant and unique green and how is cone contrast linked to this paradox? iii) how are the ‘special’ hues (invariant and unique) related to human evolution? iv) how does peripheral colour vision vary between males and females? An asymmetric colour matching paradigm and a colour naming task have been employed. In the colour matching task, 24 chromatic axes of variable purity are used. Ob- servers match the chromaticity of a 3◦ peripheral spot with that of a 1◦ parafoveal spot. The results are expressed in terms of hue rotation, saturation match and cone contrast. In the colour naming experiment the observers name 40 chromatic axes as either red, blue,

11 ABSTRACT green or yellow and colour naming functions are derived. The central maxima of these functions are defined as the unique hues. The results suggest that colour matching and cone opponency reflect the characteristics of the retinal neural network as they exhibit nasal-temporal asymmetries, similar to known physiological asymmetries. Although three of the peripherally invariant hues match the unique counterparts, invariant and unique green are markedly different for all observers. In an important control experiment unique hues are shown to be stable with eccentricity and purity. This confirms that these attributes are not confounding factors for the observed discrepancy between invariant and unique green. Unlike for the other ‘special’ hues the RMS cone contrast of invariant green differs markedly between parafoveal and peripheral targets. It is likely that the cone contrast remains unchanged only if the stimuli excite the same number of cones. Two invariant and two unique hues (blue and yellow) fall on the daylight locus suggesting that discrimination in these regions of the colour space is strongly influenced by terrestrial illumination. Moreover, the inter-individual variability is found to be minimised around the daylight locus showing that the blue-yellow system is more stable across colour normal populations than the red-green system. A statistically significant difference is demonstrated between the peripheral colour vision of males and females. This may be attributed to the M-cone polymorphism which in addition to X-chromosome inactivation, results in more than three cone types in the female retina.

12 DECLARATION

I, Athanasios Panorgias, declare that no portion of this work referred to in the thesis has been submitted in support of an application for another degree or qualiﬁcation of this or any other university or other institute of learning.

13 COPYRIGHT STATEMENT

i. The author of this thesis (including any appendices and/or schedules to this thesis) owns certain copyright or related rights in it (the ‘Copyright’)1and s/he has given The University of Manchester certain rights to use such Copyright, including for administrative purposes.

ii. Copies of this thesis, either in full or in extracts and whether in hard or electronic copy, may be made only in accordance with the Copyright, Designs and Patents Act 1988 (as amended) and regulations issued under it or, where appropriate, in accordance with licensing agreements which the University has from time to time. This page must form part of any such copies made.

iii. The ownership of certain Copyright, patents, designs, trade marks and other intellectual property (the ‘Intellectual Property’) and any reproductions of copyright works in the thesis, for example graphs and tables (‘Reproductions’), which may be described in this thesis, may not be owned by the author and may be owned by third parties. Such Intellectual Property and Reproductions cannot and must not be made available for use without the prior written permission of the owner(s) of the relevant Intellectual Property and/or Reproductions.

1This excludes material already printed in academic journals, for which the copyright belongs to said journal and publisher.

14 COPYRIGHT STATEMENT iv. Further information on the conditions under which disclosure, publication and com- mercialisation of this thesis, the Copyright and any Intellectual Property and/or Re- productions described in it may take place is available in the University IP Policy (see http://www.campus.manchester.ac.uk/medialibrary/policies/intellectual- property.pdf), in any relevant Thesis restriction declarations deposited in the University Library, The University Library’s regulations (see http://www.manchester.ac.uk/library/aboutus/regulations) and in The University’s policy on presentation of Theses.

15 ACKNOWLEDGEMENTS

It is ordinary for every PhD student to thank his supervisor and it tends to be more of an obligatory statement and less of a sincere acknowledgment. I grasp here the opportunity to sincerely thank my Supervisor Dr Ian J. Murray for almost everything; for giving me the opportunity to come to the U.K. and work with him, for being really patient with me and willing to offer me unconditionally his guidance on any question and problem I have encountered during over the last three years. Last but not least I would like to thank him for being a friend while me being far from my home country, family and close friends. It is not at all certain what the future holds for anyone, but I can guarantee that we will be in touch. Thank you Ian! I would like to thank Professor Janus J. Kulikowski for his persistence, for his ideas and for the endless discussions we had late in the afternoons. Discussions not always relevant to this project but also about history, politics and science. I can already see his inﬂuence on my way of thinking. A big thank you goes to Dr Neil R.A. Parry. Without his software I would have spent the three years programming myself the experiments. Being very critical and passionate about the details he helped me to improve methodology, presentations, posters and this work in general. Working with him is always joyful even when he sometimes asks me to ‘log off’!

16 ACKNOWLEDGEMENTS

Without the ﬁnancial contribution of the ‘Kulikowski Visual Neuroscience Fund’ I would not be able to study abroad and do this PhD. I want, therefore, to express my sincere gratitude to the ‘Guarantors’ of this Fund. I would also like to thank Dr Declan J. McKeefry for his help on the manuscripts, Dr Humza J. Tahir and Jeremiah M. Kelly for being really patient observers and all the Vision Centre staff for helping me organise my experiments. Last but not least, I want to thank my Family for supporting me, on whatever my decisions/plans were and my friends, in Greece and Manchester for making my life easier and more pleasant.

17 to my Parents.

18 ALTERNATIVE FORMAT THESIS

It was decided to write this thesis using the alternative format because, at the time of writing it, two papers were already reviewed and published in a peer-reviewed journal. The alternative format thought to be very convenient as these two published papers can be implemented as two chapters of the thesis. Chapter 1 is a general introduction including the physiology of colour vision and work relevant to peripheral colour vision. Chapter 2 describes the general methods in detail, including calibration, mathematical equations and a detailed explanation/description of the graphs used across the thesis. Chapters 3 to 7 are the experimental chapters, written as papers. Chapter 3 and 4 are already reviewed and published in a peer-reviewed journal. Chapter 8 is a summary of the findings and the conclusions of the whole thesis. Future experiments are discussed. Three appendices (A, B and C) follow where colour space transformations and mathematics are discussed. Appendices D and E are the first pages of the published papers described in Chapter 3 and 4 and the copyright licence agreements. Because of the alternative format, each experimental chapter/paper has six sections, following the style of a published paper in a peer-reviewed journal. The first section is its abstract, the second is the relevant introduction to the particular chapter/paper, the third section the methods, the fourth the results, the fifth the discussion on the findings and the sixth are the references.

19 ALTERNATIVE FORMAT THESIS

An asymmetric matching paradigm is used across all chapters/papers with slight or no modiﬁcations and it is described in all method sections. This repetition of the experimental paradigm may be tedious for the reader but it is inevitable. The reader could easily omit reading the methods of Chapter 6 and 7 as they were described in the previous chapters. Chapters 3, 4 and 5 use the same methods but with few modiﬁcations. At the end of each experimental chapter/paper a statement on the contribution of each author on the particular chapter/paper is provided.

20 RATIONALE AND AIMS

Central vision is specialised for colour and high spatial resolution. In the periphery the organisation of the retinal neurons is dramatically different. Cone density reduces with eccentricity and there are associated changes in cone-bipolar-ganglion cell connectivity. Many studies show that cone opponency is somehow lost in the peripheral visual ﬁeld and that colour vision deteriorates with eccentricity. However, despite the substantial changes in neural connectivity, some aspects of colour vision are retained at least within the central 40◦, while some hues remain remarkable stable with eccentricity. The main thrust of this work is to conduct experiments which would highlight the impact of the known physiological changes in peripheral retina on colour processing and colour perception. For example there are well known nasal-temporal differences in the distribution of cones and ganglion cells in the mammalian retina. Can then be expected a corresponding nasal-temporal difference in peripheral cone opponency? A second issue is the observed correspondence between invariant, with eccentricity hues, and unique hues and in what extent the analysis in terms of cone contrast offer any interpretation of the shifts in peripheral colour vision. Many studies have suggested that the expression of human colour vision may be in- ﬂuenced by the phases of daylight. Therefore, relations may be expected in stability and

21 RATIONALE AND AIMS variability of colour vision according to the terrestrial illumination. Finally, there has been much controversy regarding gender related differences in human colour vision. It is speculated that the reduced number of cones in the peripheral retina may exaggerate any male-female differences. Accordingly, the aims of the work described here can be summarised as follows:

i) to determine whether there are differences in peripheral colour vision between nasal and temporal visual ﬁeld,

ii) to test whether eccentricity and purity are confounding factors for the correspondence between invariant and unique hues,

iii) to use cone contrast analysis for peripheral colour matching and to investigate to what extent cone contrast changes with eccentricity,

iv) to establish whether human colour vision is inﬂuenced by the phases of daylight,

v) to investigate possible male-female colour vision differences by testing peripheral colour vision.

22 CHAPTER ONE

GENERAL INTRODUCTION

-And what Socrates is the food of the soul? -Surely, I said, knowledge is the food of the soul. Πλατων´

HE general introduction is a brief description of the physiology of colour vision T along with the description of its three stages. Also, work on colour perception and peripheral colour perception will be described. This introductory chapter will provide only a short overview of the various issues regarding colour vision as each following experimental chapter includes a more detailed introduction.

1.1 Overview of the visual process

Although it is widely believed that we see with our eyes, this impression is erroneous. The organ which is responsible for our vision is the brain and the eyes can be regarded as an extension of it. Eyes are the organs which collect visual information and perform primary processing. Subsequent analysis is carried out in specialised areas of the brain. There is a well documented sub-cortical pathway between the eye and structures such as the superior colliculi and the details of these are not discussed here. Sensory information follows a very speciﬁc pathway through the brain which is called the primary visual pathway.

23 1.2. PHYSIOLOGY OF THE VISUAL PROCESS

In the early stages, human vision consists of many distinct mechanisms, artiﬁcially described as spatial, temporal, chromatic, scotopic, photopic and so on. The output of these processes, call it perception, is synthesised in the higher cortical areas to form the visual world. Light is absorbed by the pigment of the photoreceptors and is converted to tiny electrical signals which are transmitted to the ganglion cells via the bipolar, amacrine and horizontal cells. Afterwards, the signals from the ganglion cells exit the eye through the optic nerve head as axons of the ganglion cells, which terminate in the Lateral Genic- ulate Nucleus (LGN). From the LGN, the optic radiations ascend via the white matter and terminate in the Primary Visual Cortex (V1) and then the signals are further processed in higher visual centres such as V2, V3, V4, V5(MT).

Wavelength discrimination

Colour vision is concerned with the ability of the visual system to distinguish different wavelengths of light. About two centuries ago Young (1802) noted that human colour vision depends on three mechanisms whose excitation is responsible for colour perception. Hering (1964) ﬁrst referred to colour opponency, writing that human colour vision depends on mechanisms which combine, in opposition, electrical signals generated by the photoreceptors. Many years after these observations, there is still a gap between the perceptual subtleties and the neurophysiology underlying mechanisms of colour vision.

1.2 Physiology of the visual process

1.2.1 First stage: Photoreceptors

The ﬁrst stage of colour processing occurs at the photoreceptor layer which is the second retinal layer, after the retinal pigment epithelium. There are 4 types of photore-

24 1.2. PHYSIOLOGY OF THE VISUAL PROCESS ceptors; rods and 3 cone types. Cones are responsible for the perception of colour and for vision under photopic and mesopic conditions, while the rods are responsible for mesopic and scotopic vision. Although their biological characteristics differ in many ways, both cones and rods have an outer segment, inner segment and a synaptic terminal. The outer segment is attached at the retinal pigment epithelium and contains the photosensitive pigments. The next part of the photoreceptor is the inner segment which contains mitochon- dria and is responsible for metabolism. These two parts are connected by the connecting cilium. In the inner segment there is the nucleus of the cell and an axon which terminates at the synaptic terminal of the photoreceptor (Oyster, 1999). The four photoreceptors contain different photosensitive pigments, each composed of retinal and an opsin. The spectral sensitivity of these pigments depends on the sequence of amino acids within the opsin. The three different cone opsins have a different sequence of amino acids and small changes in the chain, shift their spectral sensitivity (Nathans, Thomas, & Hogness, 1986; Oyster, 1999). Phototransduction takes place at the outer segment of the photoreceptors where the photopigments are located. The light raises the energy level of the retinal which consequently changes its structure breaking one of its double bonds. While the structure of retinal is changing, the photopigment is said to be bleached which means that the photoreceptor can not react with light until it is regenerated into an activated form. The cone photopigments regenerate faster than rhodopsin, the rod photopigment, and under conditions of constant illumination there is equilibrium between the bleached and the activated photopigments (Oyster, 1999). The three cones are named L-, M- and S-cones and show maximum sensitivity in long, medium and short wavelengths, respectively. The L- cones are most sensitive at about 560nm, the M- at around 530nm and the S- at circa 430nm (see Figure 1.1). The rods peak sensitivity is at 500nm. The L- and M-cones are highly polymorphic. That means

25 1.2. PHYSIOLOGY OF THE VISUAL PROCESS

Figure 1.1: The Smith and Pokorny (1975) cone spectral sensitivities. Each curve actually describes the probability of each cone to absorb a photon of a particular wavelength. that there are more than two L- and M-cone types with slightly different peak spectral sensitivities from the L- and M-cones described previously (Neitz & Jacobs, 1986; Neitz, Neitz, & Jacobs, 1993). In the foveola there are no rods and cones are at their highest density. As the eccentricity increases the cone density decreases and the rod density increases. The cone density is maximum at foveola (see Figure 1.2) and the rod density at 20◦ from the centre of the macula lutea (Curcio, Sloan, Kalina, & Hendrickson, 1990). The cone mosaic at the fovea differs between individuals but this variation does not inﬂuence normal trichromatic colour vision (Hofer, Carroll, Neitz, Neitz, & Williams, 2005; Neitz, Carroll, Yamauchi, Neitz, & Williams, 2002). If one of the cone opsins is absent then colour vision is described as dichromatic. If there is a shift in the M-cone spectral sensitivity then deuteranomaly arises and if there is shift at the L-cone spectral sensitivity then protanomaly occurs. In the central 20arcmin of the foveola there are no S cones and this results in the phenomenon of foveal tritanopia (Williams, MacLeod, & Hayhoe, 1981).

26 1.2. PHYSIOLOGY OF THE VISUAL PROCESS

Figure 1.2: Cone density as a function of eccentricity. The x axis plots the eccentricity from the foveola in mm and the y axis represents the cone density in 1000cones/mm2. As the eccentricity increases the cone density decreases. Note the large variation in foveal cone density among individuals. Figure adopted from Curcio et al. (1990).

L- and M-cone variability in primate retina

Many efforts have been made to measure the number of the photoreceptors and to relate them to the functionality of colour vision. It was easier to measure the spectral characteristics of S-cones than measuring the L- and M-cones’ spectra sensitivity, and generally the results of anatomical and psychophysical studies are in agreement (Brainard et al., 2000; Otake & Cicerone, 2000; Curcio et al., 1991). The main reason for S-cones being unambiguously identiﬁed is that their spectral sensitivity is distinctly different from the spectral sensitivities of the L- and M-cones. There are large variations in the numbers of L- and M-cones in the primate retina. These variations concern not only the distribution pattern but also the relative numbers of the L- and M-cones (also known as the L/M ratio). Much effort has been expended on measuring this ratio because it represents one of the mysteries of colour vision. The role of the L/M ratio in chromatic visual performance

27 1.2. PHYSIOLOGY OF THE VISUAL PROCESS is not well established because it varies widely among individuals with normal colour vision. This fact forces scientists to assume that for colour normals, whilst the relative numbers of L- and M-cones may vary, an underlying mechanism must compensate for the variation so that normal colour vision is achieved. Many groups have measured the L/M ratio using different techniques. The photopic luminosity function, the spectral sensitivities functions and the psychometric functions are some psychophysical experiments for calculation of the L/M ratio (Smith & Pokorny, 1975; Kremers et al., 2000; Cicerone & Nerger, 1989). Electrophysiological recordings from the retina (ERGs) (Kremers, Usui, Scholl, & Sharpe, 1999; Jacobs, Neitz, & Krogh, 1996), using speciﬁc stimuli for the isolation of each cone, is another way of comput- ing the relative L- and M- cones number. Also, techniques such as retinal densitometry (Rushton & Baker, 1964), microspectrophotometry (Dartnall, Bowmaker, & Mollon, 1983), mRNA analysis (Hagstrom, Neitz, & Neitz, 1998; Hagstrom, Neitz, & Neitz, 2000) and the advanced method of adaptive optics (Roorda & Williams, 1999) are other experimental procedures for the determination of L/M ratio.

1.2.2 Post-receptoral neural organisation of the retina

The signals produced by the photoreceptors are transmitted at the next retinal layer where the horizontal, bipolar and amacrine cells lie (see Figure 1.3). There are two types of horizontal cells, H1 and H2, which appear to have cone selectivity. The H1 horizontal cells are connected primarily with the L and M cones while the H2 horizontal cells receive inputs from all cone types but they seem to prefer the S cones. The fact that horizontal cells convey information from the three cones, it considers that these cells are not sensitive to wavelength and so do not play a role in colour vision (Dacey, 1996, 1999). Horizontal cells are connected directly with cones but not with bipolar, amacrine or gan-

28 1.2. PHYSIOLOGY OF THE VISUAL PROCESS glion cells which means that these cells mediate a lateral pathway. This lateral pathway sends feedback to photoreceptors and so the direct connections with single cones include signals from neighbouring photoreceptors (Dacey, 1999, 1996).

Figure 1.3: The primate retinal neural circuitry. Photoreceptors are connected directly with bipolar, ganglion and horizontal cells creating a complex circuitry that provides evidence for cone opponency and speciﬁc neural pathways. Figure adopted from Lee (2004).

There are three types of cone bipolar cells and one type of rod bipolar cell, and the distinction is made by their retinal position and the cone or rod selectivity they exhibit. The cone bipolar cells are divided into midget bipolar cells, diffuse bipolar cells and blue bipolar cells (Kouyama & Marshak, 1992). There are no direct synapses between rod bipolar cells and ganglion cells, but they only connect with two types of amacrine cells (Kolb & Famiglietti, 1974). In contrast, cone bipolar cells are connected directly with ganglion cells and amacrine cells. There are about 25 types of amacrine cells which are connected with cone and rod bipolar cells and ganglion cells. Amacrine cells are divided into those having small, medium and large receptive ﬁeld. Small-ﬁeld amacrine

29 1.2. PHYSIOLOGY OF THE VISUAL PROCESS cells are about 100µm or less, large-field are about or more 500µm and medium-field amacrine cells are between the other two types. No evidence that amacrine cells serve cone opponency is found as there is no evidence that the amacrine cells connect selectively with cone bipolar cells or directly with specific cones (Dacey, 1999). The final cell layer in the retina is the ganglion cell layer where the information conveyed by the horizontal, bipolar and amacrine cells converges. Although there are many ganglion cell types, the primary visual pathway is regarded as being composed of midget ganglion cells (P cells), parasol ganglion cells (M cells) and small-bistratified ganglion cells (see below). The ganglion cell axons form the nerve fiber layer. The axons converge at the optic nerve head to become the optic nerve.

1.2.3 Second stage: Cone opponency

Neural retinal organisation provides the basis of a complex network linking horizontal, bipolar, amacrine and ganglion cells. The complex connection between these cells, is responsible for cone opponency which is the second coding stage. The bipolar and ganglion cells show a strong selectivity for photoreceptors, while there is no clear and strong evidence for contribution to colour opponency by horizontal and amacrine cells (Dacey & Packer, 2003).

Cone bipolar cells

The cone bipolar cells, as described previously, are divided into midget, diffuse and blue-cone bipolar cells. The midget bipolar cells lie in the central retina and are connected with a single L- or M-cone (Dacey, 1999). They are divided into ON and OFF midget bipolar cells, depending on their reaction to light. When cones depolarize, as a reaction to darkness, OFF midget bipolar cells also depolarize. When a cone depolarizes as a reaction

30 1.2. PHYSIOLOGY OF THE VISUAL PROCESS to light the ON midget bipolar cells hyperpolarize. These cone-selective bipolar cells terminate in one single midget ganglion cell and there is strong evidence that have centre- surround receptive fields (Boycott & Wassle, 1991). Their receptive fields, which are either red-ON, red-OFF, green-ON or green-OFF, provide a private connection between L- or M-cones and midget ganglion cells and so there is evidence that the midget bipolar cells serve the red-green opponent pathway. Blue-cone bipolar cells are connected with more than one S-cone, unlike midget bipolar cells which are connected with a single L- or M-cone. Their receptive fields are shown to be mostly blue-ON but there are suggestions that there are blue-cone bipolar cells which have a blue-OFF receptive field. The blue-cone bipolar cells transmit their inputs into small-bistratified ganglion cells and so serve the blue-yellow opponent pathway (Kouyama & Marshak, 1992; Dacey, 1993). Contrary to midget bipolar cells, diffuse bipolar cells are always connected with more L- and M-cones, even in the central retina, and transmit their inputs to parasol ganglion cells. Their receptive fields are found to receive the same inputs to their centre and surround and so it is believed that the diffuse bipolar cells contribute to the achromatic pathway or luminance pathway (Dacey, 1999).

Ganglion cells

There are three types of ganglion cells, the P cells, the M cells and the small-bistratiﬁed ganglion cells which project to different laminae in LGN. Three different pathways are formed for transferring the information from the retina to the LGN. The P cells form the red-green pathway which projects to the P laminae in the LGN (parvocellular pathway). P cells in the central retina receive inputs from midget bipolar cells and consequently from a single L- or M-cone. There are red-ON, green-ON, red-OFF and green-OFF P cell receptive ﬁelds which form the basis for a red-green opponent pathway (see Figure 1.4). In

31 1.2. PHYSIOLOGY OF THE VISUAL PROCESS peripheral retina, P cells increase in size and so their receptive ﬁelds increase too, which means that they receive inputs from a large number of midget bipolar cells (Dacey, 1999).

Figure 1.4: The retinal ganglion receptive fields. The red-ON, red-OFF, green-ON, green-OFF and blue-ON centre receptive fields are established either physiologically or psychophysically. The pathway and underlying mechanisms of the blue-OFF receptive field are still note clear.

P cells in the fovea and parafovea are cone-selective and they show cone opponency, but at the peripheral retina this opponent mechanism is lost as the inputs, both at the centre and the surround receptive field, are derived from both L- and M- cones. However, there are studies (Martin, Lee, White, Solomon, & Ruttiger, 2001) that suggest that even in peripheral retina, P cells are connected selectively with midget bipolar cells which receive input from either L- or M-cones. The pathway for the excitatory centre of the receptive field is well understood but the neural pathway for the inhibitory surround of the receptive field is not very clear (Dacey & Packer, 2003). The small-bistratified ganglion cells receive input from blue-cone bipolar cells and H2 horizontal cells. Small-bistratified ganglion cells form the blue-yellow pathway which project to the koniocellular laminae of the LGN (koniocellular pathway). Their receptive fields show a blue-ON centre and the surround is connected with diffuse bipolar cells, re- ceiving inhibitory inputs from both L- and M-cones. The blue-OFF receptive field of the blue-yellow pathway has not yet been identified, even though there are some rare phys-

32 1.2. PHYSIOLOGY OF THE VISUAL PROCESS iological reports for its existence (Dacey & Packer, 2003). The receptive fields of small bistratified ganglion cells are drawn symbolically in Figure 1.4 as there is no evidence for contribution in spatial resolution (Dacey & Packer, 2003). M cells form the magnocellular pathway and receive inputs from both L- and M-cones. Their receptive fields seem to receive the same amount of information from both cone types and for that reason it is believed that the magnocellular pathway carries information about luminance contrast. Their receptive fields are larger than those of midget ganglion cells (Field & Chichilnisky, 2007).

1.2.4 Retino-thalamic pathways and cortex

Retinal ganglion cell axons form three different pathways, parvocellular, magnocellular and koniocellular, for the transmission of the visual information to other processing stages. These names are derived from the LGN laminae to which their pathways project. The parvocellular pathway, which carries the signals from P cells, terminate at the parvocellular layer. The signals from M cells, which form the magnocellular pathway, terminate at the magnocellular layers of the LGN. The koniocellular layers, which were relatively recently identified (Casagrande, 1994), receive inputs from small-bistratified ganglion cells. LGN cells show similar receptive fields to retinal ganglion cells which means that parvocellular and koniocellular cells show cone opponent receptive fields, while magnocellular cells process information about luminance contrast. The three distinct pathways transmit the visual signals further to V1. The parvocellular pathway terminates at layer 4Cβ, the magnocellular at 4Cα and the koniocellular at layers 2, 3 and 1 (Gegenfurtner & Kiper, 2003). Some V1 cells have large receptive fields which means that in a specific receptive field they receive inputs from more than one midget ganglion cell. This observation might suggest that colour opponency is lost in V1, but

33 1.2. PHYSIOLOGY OF THE VISUAL PROCESS this is not the case (Gegenfurtner & Kiper, 2003; Solomon & Lennie, 2007). Studies found that V1 cells show chromatic sensitivity but there are no clear calculations about the percentage of these cells among the whole population. Recent studies mention that 10% of V1 cells show colour properties, while other works suggest about 50% (Solomon & Lennie, 2007; Gegenfurtner & Kiper, 2003). Johnson, Hawken, and Shapley (2001) examined the colour and the spatial properties of V1 cells. They found that in V1 there are cells which respond only to luminance stimuli, cells which are stimulated by luminance and colour stimuli, and ﬁnally cells which respond only to stimuli composed of colour properties. They suggested that the majority of cells in V1 layers are the colour-luminance cells and that most of these are double opponent. Double opponent cells means that these cells are responsive to both colour and luminance. Colour cells and luminance cells showed low-pass spatial characteristics while most of the colour-luminance cells showed spatial tuning. The existence of colour cells in V1 must subserve colour vision in some way, but these are not sufﬁcient for the experience of colour and V1 cells project to other cortical areas (Johnson et al., 2001) which are thought to culminate in true colour perception (Zeki & Marini, 1998). Colour sensitive cells are also found in V2, V3, V4 and other cortical structures, which leads to the conclusion that colour processing occurs in more than one cortical area (Solomon & Lennie, 2007). Many studies, using modern imaging techniques such as fMRI, found a strong response of V1 cells from colour stimuli, concluding that a major part of colour processing occurs there (Engel, Zhang, & Wandell, 1997). Subsequently V1 signals are transmitted to V2 and in macaque monkeys the process continues in V4 (see Figure 1.5). There is no homologous region in humans, but studies have shown that a colour centre exists which varies between individuals and is found in general terms on the lateral aspect of the collateral sulcus on the fusiform gyrus (McKeefry & Zeki, 1997). These cells respond to stimuli with other physical properties, like orientation and mo-

34 1.2. PHYSIOLOGY OF THE VISUAL PROCESS

Figure 1.5: Areas of the visual brain. Figure adopted from Zeki (2003). tion (Gegenfurtner, Kiper, & Fenstemaker, 1996; Gegenfurtner, Kiper, & Levitt, 1997; Leventhal, Thompson, Liu, Zhou, & Ault, 1995). More detail fMRI studies of V4 in macaque monkeys showed very strong responses to chromatic stimuli and single-unit recordings found that the majority of V4 cells are colour sensitive (Gegenfurtner & Kiper, 2003). This evidence led to the conclusion that V4 should be the centre for colour processing while another study showed that there is no great difference in performance of colour tasks between monkeys with V4 lesions and normal monkeys (Heywood, Gadotti, & Cowey, 1992). Also, experimentally induced damage in macaque monkey V4 affects not only colour vision but also causes deﬁcits in texture-shape discrimination, object recognition (Heywood & Cowey, 1987; Merigan, 1996, 2000) and also recognition of titled shapes (Walsh, Butler, Carden, & Kulikowski, 1992). Furthermore, Wild in 1985 found that lesions in rhesus monkey V4 are responsible for loss of colour constancy but not wavelength discrimination (Wild, Butler, Carden, & Kulikowski, 1985) nor hue cat- egorisation (Walsh, Kulikowski, Butler, & Carden, 1992), which suggests that there is another cortical centre for the completion of the two last tasks. So, there is no conclusive

35 1.3. TRANSFORMATION FROM RETINA-LGN TO CORTEX. THIRD STAGE: COLOUR OPPONENCY. evidence for a colour processing centre, but the overall process of colour vision can be regarded as the sum of many different cortical responses (Gegenfurtner & Kiper, 2003; Gegenfurtner, 2001).

1.3 Transformation from retina-LGN to cortex. Third

stage: Colour opponency.

Ingling and Huong-Peng Tsou (1977) suggested that the responses of the three cone- opponent channels are combined orthogonally and transmit their responses further in the visual pathway. Krauskopf, Williams, and Heeley (1982) found that there are indeed cardinal directions in colour space which isolate the responses of the three cone-opponent channels. Later, Derrington, Krauskopf, and Lennie (1984) showed electrophysiologically that these cardinal directions selectively stimulate cells in the LGN and so it was proposed that the cone-opponent stage reaches at least up to the LGN. These cardinal directions, though, fail to describe veridical colours; like pure red, blue, green and yellow. These veridical colours, which are composed by only one hue, are called unique hues. Unique red is neither yellowish nor bluish, unique blue is neither reddish nor greenish, unique green is neither bluish nor yellowish and unique yellow is neither greenish nor reddish and ‘show no perceptual similarity to any other hue’ (Wyszecki & Stiles, 1982). So far, there is no clear evidence on where unique hues are encoded even though it is suggested it may be encoded as early as in the primary visual cortex (Parkes, Mars- man, Oxley, Goulermas, & Wuerger, 2009) or as high as in the inferior temporal cortex (Stoughton & Conway, 2008; Mollon, 2009; Neitz & Neitz, 2008; Conway & Stoughton, 2009). The chromatic axes of the unique hues do not coincide with the cardinal axes of the cone-opponent stage (see Figure 1.6). This fact led to the proposal of the third stage

36 1.4. INDIVIDUAL VARIATIONS IN COLOUR VISION of the perception of colour; the colour opponency. The signals from the cone opponent stage are combined and/or rotated in higher brain centres so as to give veridical colour perception.

Figure 1.6: Unique hues and cardinal cone opponent axes. The +S and -S axes correspond to the blue-yellow cone opponent direction and the M-L and L-M axes correspond to the red-green cone opponent direction as described by Krauskopf et al. (1982). Each one peak of the colour scaling functions corresponds to one unique hue. Note the difference between the cardinal cone opponent axes and the unique hues. That discrepancy makes necessary the colour opponent stage that rotates/transforms the cone opponent chromatic axes into veridical colours. The graphs are from De Valois, De Valois, Switkes, and Mahon (1997).

1.4 Individual variations in colour vision

As mentioned earlier, the relative numbers of L- and M-cones vary widely among the colour normal population and many workers have tried to compare and establish whether L/M ratio variations have functional effects on colour vision (Brainard et al.,

37 1.4. INDIVIDUAL VARIATIONS IN COLOUR VISION

2000; Kremers et al., 2000; Miyahara, Pokorny, Smith, Baron, & Baron, 1998). Roorda and Williams (1999) found for two individuals that the L/M ratio is 1.15 and 3.79. Even though these two subjects had a different L/M ratio, they identified unique yellow (which relies only on L- and M-cone activation) almost at the same wavelength (20nm difference), a fact which lead to the conclusion that, at least, for yellow discrimination an underlying mechanism must weight the difference in L- and M- cones so that the perception remains stable (Brainard et al., 2000). Neitz et al. (2002) suggested a solution. They altered the everyday colour experience of their observers by using colour filters for a prolonged period of time. Unique yellow judgments changed because of the change in visual experience and that change persisted for several weeks after they removed the filters. They demonstrated that colour vision mechanisms show a plasticity which allows variations in L- and M- cone population to be compensated by an underlying mechanism (Neitz et al., 2002). Contrary to this study, Cicerone (1987) suggested that the unique yellow wavelength discrimination depends strongly on the relative numbers of the L- and M- cones. One problem which must be taken into account in colour vision experiments is the large individual variations, which are classified as normal. Such variations are evident in the position of the two cardinal axes, in the position of the unique hues and in the Rayleigh matches using an anomaloscope. These variations should be considered during the analysis of the experimental data. The origins of these individual variations are due mostly to the physiology of the individual eye characteristics such as the macular pigment, the lens density, the pigmentation density of the photoreceptors, the shift in λmax for the L- and M- photopigments and the L/M ratio (Webster & MacLeod, 1988). Smith and Pokorny (1995) report that biological variations (as mentioned above) are responsible for the rotation of the cardinal axes. Webster, Miyahara, Malkoc, and Raker (2000a), in accordance with the previous study, using colour adaptation experiments, re-

38 1.5. COLOUR PERCEPTION IN PERIPHERAL RETINA ported a shift in both cardinal axes. They found that the L-M axis is rotated negatively for a mean of 2.6◦ while the S-(L+M) axis shows a positive rotation of 9.6◦. These rotations were found to be correlated with macular pigment and lens density (especially the rotation of S-(L+M) axis) and cone photopigment λmax shifts and densities. Also, Webster, Miyahara, Malkoc, and Raker (2000b) showed that there are large individual variations in the judgment of unique hues but these variations are uncorrelated with physiological differences between individuals, and thus an underlying unknown mechanism may be responsible for the unique hues. Jordan and Mollon (1995) found that unique green is correlated with the lightness of the iris, which is an index of the eye pigmentation and also they supposed that the locus of unique green is not ﬁxed by the cone photopigments but that it is inﬂuenced by every day experience.

1.5 Colour perception in peripheral retina

During colour experiments, observers notice that there are changes in colour perception when stimuli are viewed peripherally. These changes could be expressed in terms of hue and saturation shifts. The general trend that follows these experiments is that colours seem to be more desaturated and hues are changing depending on retinal eccentricity (Gordon & Abramov, 1977; Stabell & Stabell, 1976; Stabell & Stabell, 1984; Murray, Parry, & McKeefry, 2006; McKeefry, Murray, & Parry, 2007; Parry, McKeefry, & Mur- ray, 2006). From a physiological point of view there is much controversy as to whether or not colour perception is preserved in peripheral retina. Martin et al. (2001) showed that red- green cone opponency is foveal-like for low temporal modulations. Their ﬁnding suggests that the peripheral cone sampling in midget ganglion cells compensates the L- and M-

39 1.5. COLOUR PERCEPTION IN PERIPHERAL RETINA cone density decline. On the other hand, Diller et al. (2004) found no cone opponency in peripheral midget ganglion cells but Solomon, Lee, White, Ruttiger, and Martin (2005) argued that this was because of the high temporal frequency they used. Solomon et al. (2005), using lower temporal modulations than Diller et al. (2004), showed that cone opponency is preserved up to 50◦ retinal eccentricity. The main factors that may contribute to the changes in colour perception are the relative changes in L-, M-cones in peripheral retina (Mullen, Sakurai, & Chu, 2005), the rods’ contribution in colour vision (Stabell & Stabell, 1976), the cone sampling as the eccentricity increases (Parry et al., 2006) and the difference in cone inputs in peripheral ganglion cells (Dacey, 1996; Parry et al., 2006) Stabell and Stabell (1976) introduced the notion of rod intrusion as an explanation of the hue and saturation changes into peripheral retina. According to them, while the experimental conditions remain photopic, the cones are the only photoreceptor type that are responsible for colour vision but, as the luminance condition changes to scotopic, rods contribute to colour perception and this leads to the chromaticity shifts. The experimental data of Stabell and Stabell (1976) showed that as the luminance condition changes from photopic to scotopic, no shifts are observed in the central fovea which is rod free, but as the luminance changes, shifts in chromaticity are observed. The term ‘rod intrusion’ was introduced to explain the perceived shifts in hue and saturation and evidence that neural rather than photochemical factors contribute to the chromaticity changes (Stabell & Stabell, 1976). Gordon and Abramov (1977) conducted some colour experiments in foveal and peripheral retina. They found that as the eccentricity increases there were changes in perceived hue and saturation, but these shifts could be compensated by increasing the stimulus size. It was found that the colour perception for large stimuli in peripheral retina was the same as the colour perception for smaller stimuli in the central fovea. In the same

40 1.5. COLOUR PERCEPTION IN PERIPHERAL RETINA study, it was suggested that the sensation of green is the ﬁrst which changes as the stimulus size is decreased (Gordon & Abramov, 1977). The fact that stimulus size can compensate for the loss in colour perception in peripheral retina, led Abramov, Gordon, and Chan (1991) to introduce the term ‘perceptive ﬁeld size’ which is the minimum stimulus size necessary for the same colour experience comparable with the foveal colour perception. Parry et al. (2006) tested a wide range of stimulus size and retinal eccentricities with an asymmetric colour matching experiment. The subjects were required to match the hue and saturation of a circular stimulus appearing at different eccentricities, with a small circular stimulus presented 1◦ from the fovea. The results showed that hue shifts follow a similar pattern regardless of the retinal eccentricity. Hues that were found to be invariant with retinal eccentricity were similar to the unique hues of blue, yellow and red but not to green (Parry et al., 2006). McKeefry et al. (2007) showed that the shifts in hue and saturation are due to decreased activity of the L-M channel, while the S-(L+M) channel showed no or little change in its activity.

41 1.6. REFERENCES

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49 CHAPTER TWO

MATERIALS AND GENERAL METHODS

N this chapter details are provided regarding colour space, cone-activation units, ex- I perimental equipment and its calibration and experimental procedures.

2.1 Colour space

Over time many colour systems have been proposed, but there is no total agreement for which one describes better the chromatic properties of a colour. In this study, it was decided to describe colours in CIE1931 xy colour space for two reasons: 1) because CIE1931 xy colour space is universally accepted and widely used and 2) because previous work, on which this study is based, used that colour space.

The light emitted by an object is described by its spectral radiance distribution (Le,λ) as a function of wavelength across the visible spectrum. This distribution is a physical characteristic of the object. This characteristic undergoes certain transformations by the visual system and thus the objects’ light information is perceived as colour. Colour spaces were developed because there was the need of a system that correlates the physical entity of an object with the observers’ perception. Apart from that, there was the need of a system that is understandable and easily usable by the users of colour information.

50 2.1. COLOUR SPACE

As a result of colour matching experiments, Wright (1928-29) and Guild (1931) presented the colour-matching functions known as r(λ), g(λ) and b(λ). The stimulus consisted of a bipartite ﬁeld, on one side of which was a monochromatic light and at the other side a combination of three spectral primaries whose wavelengths were 435.8nm, 546.1nm and 700nm. The observers could change the weighting factors of the three primaries in order to match the two ﬁelds. Commission Internationale de l’Eclairage (CIE, International Commission on Illumination) adopted in 1931 the colour matching functions (see Figure 2.1a) to form the CIE1931 xy colour space.

Figure 2.1: a) The r(λ), g(λ) and b(λ) colour matching functions. b) The x(λ), y(λ), z(λ) tristimulus functions.

Under certain assumptions, the r(λ), g(λ), b(λ) colour matching functions were transformed to the x(λ), y(λ), z(λ) tristimulus functions. The assumptions were that all the x(λ), y(λ), z(λ) should be real positive values, the y(λ) should exactly match the V (λ) for the standard observer, x(λ), y(λ) and z(λ) should be equal to 1/3 at the equal energy white point and z(λ) should be zero for wavelengths greater than 650nm. This produced the next set of colour matching function, known as x(λ), y(λ) and z(λ) (see Figure 2.1b). To obtain a correlation between the physics (that is the power radiance distribution) and human perception (that is the colour matching functions) the power spectral distribution was multiplied with the colour matching functions and by integrating the product over

51 2.1. COLOUR SPACE the range of the visible spectrum (see Equation 2.1.1), the tristimulus XYZ values were obtained (Kaiser & Boynton, 1996).

R X = Km Le,λx(λ)d(λ) R Y = Km Le,λy(λ)d(λ) (2.1.1) R Z = Km Le,λz(λ)d(λ)

lm The Km is a constant called maximum photopic luminous efﬁcacy and its units are ( W ). These imaginary functions provided the link between the real world characteristics and perception. The advantage of the tristimulus values is that 1) in order to describe a colour you only need the set of its tristimulus values (that is XYZ) and 2) they can be linearly added in order to describe the result of adding two colours of known tristimulus values. The latter means that if two component colours with X1Y1Z1 and X2Y2Z2 have to be added, then the result of their mixture will have X3 = X1 + X2, Y3 = Y1 + Y2 and

Z3 = Z1 + Z2. As the tristimulus values can be negative or positive, CIE transformed them to be only

X Y positive by x = X+Y +Z , y = (X+Y +Z) and L = Y . These equations describe what it is known as the CIE1931 xyL colour space. The x and y are the chromaticity coordinates and L is the luminance. Figure 2.2 depicts an equiluminant plane of that colour space. The L can be regarded as a vector perpendicular to the paper originating from the white point. The horse shoe shaped curve is called the spectrum locus and colours on that line are monochromatic. The straight line that connects the start and the end of the spectrum locus is called the line of purples. Colours on that line can not be described by a single wavelength and more than one monochromatic lights are needed in order to acquire that colour. Judd (1951) modiﬁed slightly the xy coordinates in order to compensate for some imperfections in the short wavelength region of the CIE1931 xy colour space. Equa-

52 2.2. CONE FUNDAMENTALS AND L-, M-, S-CONE ACTIVATION UNITS

Figure 2.2: The horse shoe shaped CIE1931 xy colour space. The curved line is the spectrum locus were all the visible wavelengths lie and the numbers are the wavelengths in nm. The straight line at the bottom of the spectrum locus is line of pur- ple or the locus where no colour can be described by a single wavelength. The points of equal energy white (E) and illuminant C are also plotted as a reference. tions 2.1.2 describe this modiﬁcation resulting in CIE1931 x’y’ colour space. Similarly, there are the X’Y’Z’ tristimulus values after Judd’s modiﬁcation.

1.0271x − 0.00008y − 0.00009 x0 = 0.03845x + 0.01496y + 1

0.00376x + 1.0072y + 0.00764 y0 = (2.1.2) 0.03845x + 0.01496y + 1

2.2 Cone fundamentals and L-, M-, S-cone activation units

Vos and Walraven (1971) and Smith and Pokorny (1975), based on the colour matching functions described before, provided the vision science community with the ﬁrst complete cone fundamentals (or cone sensitivities). Using protanopes, deuteranopes and tritanopes they calculated the chromaticity coordinates of the peak sensitivity of each cone type. By linearly combining the three cone primaries they ﬁtted a model to best describe

53 2.2. CONE FUNDAMENTALS AND L-, M-, S-CONE ACTIVATION UNITS

Figure 2.3: The Smith and Pokorny (1975) cone fundamentals describing the spectral sensitivity of the L-, M- and S-cones. The cone fundamentals are normalised to unity. the colour matching functions. Figure 2.3 depicts the Smith and Pokorny cone sensitivities as a function of wavelength. The only difference between the two sets of fundamentals is that Smith and Pokorny assumed that there is no S-cone input to the luminance channel while this was not the case for the Vos and Walraven cone fundamentals. The cone fundamentals used in this thesis are the normalised Smith and Pokorny (1975) cone fundamentals. The cone-activation units can be calculated using Equa- tion 2.2.1.

      L 0.24368 0.85308 −0.05161 X0              M  = −0.39528 1.16399 0  ×  Y 0  (2.2.1)             S 0 0 0.56098 Z0

The X’Y’Z’ tristimulus values and the matrix above, transform the cone-activation units calculation to a linear procedure. Alternatively, the spectral radiance distribution, the cone-fundamental and advanced mathematical formulas must be used.

54 2.3. CARDINAL DIRECTIONS, CHROMATIC AXES AND PURITY

2.3 Cardinal directions, chromatic axes and purity

Krauskopf, Williams, and Heeley (1982) first showed psychophysical data for three cardinal axes (two chromatic axes and one luminance axis) in a colour space which isolate the activity of either the red-green chromatic channel, the blue-yellow chromatic channel or the luminance channel. Two years later Derrington, Krauskopf, and Lennie (1984) showed physiologically that these chromatic directions isolate certain neurophysiological substrates in the LGN. These results came to verify the existence of the second cone opponent stage in the hierarchy of the visual process. Derrington et al. (1984) proposed the use of a different way of defining chromatic stimuli relatively to these cardinal directions on a CIE1931 xy colour space. Their proposal was based on the MacLeod and Boynton (1979) cone-excitation space on which there are certain directions that isolate the activity of the post-receptoral stage. The two cardinal chromatic axes intersect at the white point, on the CIE1931 xy colour space. From that point the following directions can be distinguished: L-M (responsible for the sensation of redness); -L+M (responsible for the sensation of greenness; S-(L+M) (responsible for the sensation of blueness); -S+(L+M) (responsible for the sensation of yellowness). They assigned these axes to 0◦, 180◦, 270◦, and 90◦. By that convention the two chromatic channels are normal to each other so that if a chromatic change happens in one channel there is no chromatic activity in the other. They also added one more axis passing through the white point, perpendicular to the isoluminance plane. This axis defines luminance. In the MBDKL colour space (from MacLeod - Boynton - Derrington - Krauskopf - Lennie) a rotated vector can be imagined in 3D which originates from the white point. Its angle from the 0◦ axis describes the chromatic axis, its length from the white point defines the purity and its elevation from the isoluminance plane defines the change in luminance. In another way, this colour space could be thought as a sphere, at whose centre is the white point. Knowing the angle, the length and the elevation

55 2.3. CARDINAL DIRECTIONS, CHROMATIC AXES AND PURITY of a vector starting from the centre the xy coordinates and the luminance of the end point of this vector can be deﬁned. In this study the xy coordinates for the 0◦ cardinal axis were adopted from De Valois, De Valois, Switkes, and Mahon (1997). Rotating the vector clockwise, the S-(L+M) axis is at 90◦, the -L+M axis at 180◦ and the -S+(L+M) at 270◦ (see Figure 2.4).

Figure 2.4: The CIE1931 xy colour space on which the cardinal axes (Krauskopf et al., 1982) are shown (grey lines). The grey dots represent the chromaticities used in our experiments (dark grey is purity 1, grey is purity 0.75 and light grey is purity 0.5). The dashed triangle is the monitor gamut. The panel in the upper hand side corner is a zoom-in in the grey shaded area. The dotted line shows a chromatic axis of angle φ and purity `. Each arrow points at a chromaticity of different saturation. The length of each arrow deﬁnes the saturation of the point.

The grey lines are the cardinal directions described before. The 0◦ - 180◦ axes are the L-M and -L+M axes respectively and the 90◦ - 270◦ are the S-(L+M) and -S+(L+M) respectively. These axes coincide at illuminant C (star). The panel at the top right hand side is a zoomed-in view of the grey-shaded area. The dotted line is a vector of angle φ (chromatic axis) and length ` (purity). Knowing these two values the xy coordinates at

56 2.3. CARDINAL DIRECTIONS, CHROMATIC AXES AND PURITY

Figure 2.5: The relationship between the chromatic axes and the wavelengths of the spectrum locus. the end of the vector can be deﬁned. Vector length of 0.0739 is deﬁned as purity 1. So, the purity of the stimuli can be described using fractions of 1. For example, if a stimulus is of 0.5 purity, this means that the length of the vector, pointing to its coordinates, is

0.0739 2 = 0.037. Similarly, purity of 2 means length equal to 0.0739 × 2 = 0.148. In the adjacent graph the grey arrows are of length equal to purity 0.5, 0.75 and 1. Angle φ is calculated in respect to the cardinal 0◦ axis. Chromatic axis of 45◦ means that the √ ◦ ◦ 2 vector falls in the middle of the 0 - 90 space and that the tangent is 2 . In this thesis 24 chromatic axes are used, equally spaced around the white point. The step in chromatic axes is 15◦ and their purity ranges from 0.5 to 1.0 (see Figure 2.4). It should be clariﬁed here that chromatic axis and purity are the physical attributes of a colour stimulus. When the observer’s responses are referred the chromatic axis becomes hue and purity becomes saturation, which are the perceptual equivalents. Figure 2.5 provides an approximate correspondence between monochromatic lights and the chromatic axes used in this thesis. Note that for chromatic axis between 0◦ - 88◦ and 334◦ - 360◦ there is no correspondence to monochromatic lights as these axes fall on the line of purples.

57 2.4. CONE OPPONENT MODEL

2.4 Cone opponent model

In certain parts of this work a cone opponent model is used in order to describe the results. The cone-opponent model adopted here is a linear combination of the L-, M- and S-cone activation units forming the three visual channels: the L+M achromatic luminance channel, the L-M chromatic channel (carrying only red-green information) and the S-(L+M) chromatic channel (carrying only blue-yellow information). This model is described by Stanikunas, Vaitkevicius, Kulikowski, Murray, and Daugirdiene (2005) and can be summarised by the matrix below (Equation 2.4.1).

      L + M 0.63324 0.39577 0 L              L − M  =  2.21907 −2.61269 0  ×  M  (2.4.1)             S − (L + M) −0.35547 −0.35547 1.02296 S

According to this matrix, the luminance channels is formed by an additive combination of L- and M-cone activity, the L-M channel by a subtractive combination of the L- and M-cone activity and the S-(L+M) channel by a linear combination of L-, M- and S- cone activity. This model is based on three assumptions: 1) There is no channel activation under the background illuminant C, 2) the L to M ratio in the luminance channel is 1.6 and 3) the chromatic channels are orthogonal, meaning that on the cardinal directions of colour space (Krauskopf et al., 1982) there is either L-M or S-(L+M) activation. Fig- ure 2.6 depicts the activation of the three channels for the 24 chromatic axes shown on Figure 2.4, for purity 0.5 and luminance 12.5cd/m2. Starting from 0◦ the L-M channel’s activation is reducing and is zeroed at 90◦ while the S-(L+M) channel reaches its maximum. Towards 180◦ the L-M reduces its activity (or the -L+M activation is increasing) and the S-(L+M) channel zeroed at 180◦ where there is

58 2.5. CONE CONTRAST

Figure 2.6: The activation of the three visual pathways, L+M (luminance channel, diamonds), L-M (red-green chromatic channel, squares) and S-(L+M) (blue-yellow chromatic channel, dots) for 24 different chromatic axes, purity 0.5 and constant luminance of 12.5cd/m2 activity only from the red-green chromatic channel. Similarly the L-M channel’s activity is zero again at 270◦ while the -S+(L+M) is maximized. Finally, at 360◦ (which is the same chromatic axis as 0◦) the L-M is maximized and the S-(L+M) channel’s activity is zero. The luminance channel is almost stable as a function of the chromatic axes as the stimuli lie on an isoluminance plane.

2.5 Cone contrast

An achromatic grating consists of bars of higher and lower luminance. For this grating the contrast can be calculated as the difference between the maximum and the minimum luminance over the sum of the maximum and minimum luminance or over the mean background luminance. Its contrast is an index of luminance modulation. In the same way, the cone contrast can be deﬁned, which is an index of cone-activation modulation. The surrounding background of a chromatic stimulus produces Lb, Mb and Sb cone-activations (see Figure 2.7).

A chromatic stimulus which is superimposed on the background produces Ls, Ms and Ss cone activations. The ∆L, ∆M and ∆S cone activation differences over the

59 2.5. CONE CONTRAST

Figure 2.7: The background (light grey area) produces Lb, Mb and Sb cone activations. The stimulus produces (dark grey area) Ls, Ms and Ss. The L, M and S Weber cone contrast is deﬁned as the ∆L, ∆M and ∆S over the Lb, Mb and Sb.

background Lb, Mb and Sb cone activation, respectively, deﬁne the L, M and S Weber cone contrast (see Equation 2.5.1). The Michelson cone contrast can be calculated according to Equation 2.5.2. In this thesis Weber cone contrast is used because it assumes that the observer adapts to the background activation, while Michelson contrast assumes that the observer adapts to the sum of background and foreground activation.

∆L LW cc = Lb ∆M MW cc = (2.5.1) Mb ∆S SW cc = Sb

∆L LMcc = Ls + Lb ∆M MMcc = (2.5.2) Ms + Mb ∆S SMcc = Ss + Sb

60 2.6. EXPERIMENTAL EQUIPMENT AND CALIBRATION PROCEDURE

2.6 Experimental equipment and calibration procedure

The equipment used for this study consisted of a SONY c Trinitron R Multiscan520GS monitor, a ViSaGe (Cambridge Research Systems c , Ltd, Rochester, UK) visual stimulus generator, a CB6 (Cambridge Research Systems c , Ltd, Rochester, UK) infrared response box and specially designed software. There are many factors which affect the characteristics of any given computer monitor, such as intrinsic RGB gun interactions, errors in algorithms used for converting digital inputs into RGB gun intensity values, the every day use of the monitor and the ageing of the phosphors. In the experiments reported here a

PR650 SpectraScan R Colorimeter (Photo Research Inc.) and ColourCal R Colorimeter (Cambridge Research Systems c , Ltd, Rochester, UK) were used to calibrate the system. The graphic card software uses correction factors so as to adjust the output of the monitor RGB channels in order to achieve chromatic accuracy. A gamma function for each monitor channel was obtained by testing 128 voltages using the ColourCal R . The gamma represents a numerical parameter which describes the nonlinearity of intensity reproduction due to the electron guns of a CRT display. The software which is used to generate the stimuli gives the gun voltages of the monitor channels using the monitor gamma function. CIE1931 x, y and L coordinates were set at x=0.31, y=0.316 and L=12.5cd/m2. These values are the coordinates for the illuminant C, used as the background for the experiments. Using these coordinates, the gun voltages were noted. The screen was measured with the PR650 colorimeter and the x, y and L values were adjusted until the colorimeter read the C illuminant coordinates. The new gun voltages were recorded. The difference in the measured values from the adjusted, indicate that the correction factors do not give satisfactory accuracy. The ratios of the post over the pre adjustment gun voltages values are the accurate correction factors and these were entered to the graphic card software. Using these factors, a new correction gamma function was obtained and the monitor was

61 2.6. EXPERIMENTAL EQUIPMENT AND CALIBRATION PROCEDURE

Figure 2.8: The black dots connected with a line are the xy coordinates that were pre-set at the visual stimulus generator. The open circles are the xy coordinates measured with the spectrora- diometer. measured again with the PR650 to be sure that the chromaticity coordinates were correct. At Figure 2.8, the measured xy coordinates and the pre-set xy coordinates are plotted. The difference between theoretical and measured xy coordinates can be regarded as tiny as errors in xy coordinates readings were found only at the third decimal place and the steps used for changing purity and chromatic axes (described in the next section) are much larger. Thus, these differences are not affecting the experimental results.

Figure 2.9: Panel a depicts measured luminances for a wide range of predeﬁned luminances. The black line is the y=x line. Panel b shows how the luminance changes with time. Time zero is when the monitor was turned on. The predeﬁned luminance was 12.5cd/m2 and it can be seen that the monitor was settled at that luminance after about 60min.

62 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

Luminance was measured for a wide range of values to test the monitor’s luminance response characteristics. Figure 2.9a depicts the measured luminance over the adjusted. As the adjusted luminance is increased the error in measured luminance is also increased. That is because the CRT’s electron guns are calibrated at 12.5cd/m2. But as it can be seen from Figure 2.9a there is a satisfactory linear relation for luminance range between 5cd/m2 and 40cd/m2. Finally, the luminance was measured over time to test the stability of the monitor. The predeﬁned luminance was 12.5cd/m2 and it was found that the monitor needs about 60 minutes to reach the correct luminance. So, the monitor should be switched on for at least 60 minutes before any experimental data collection (see Figure 2.9b).

2.7 Experimental procedures and colour vision tests

In this thesis two experimental procedures were employed. The ﬁrst is the asymmetric matching paradigm, and the second is the naming experiment ﬁrst described by Parry, McKeefry, and Murray (2006). Prior to the experiments the observers’ visual acuity was measured and they performed three colour vision tests, the Farnsworth-Munsell 100 Hue test, Ishihara plates and the Nagel anomaloscope. In this section a description of the colour vision tests and the experimental procedures will be provided.

2.7.1 Colour vision tests

The Farnsworth-Munsell 100 hue test

The Farnsworth-Munsell 100 Hue test consists of 85 caps covered by Munsell colour paper. The caps are divided in four sets, each one covering a region in colour space. The four sets describe a complete circle in colour space. Each cap has a number underneath it

63 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS so as to know its position relatively to the others. The numbers range from 1 to 85. If the caps are placed according to their numbering, they form a uniform sequence of colours. The test is performed under a neutral illuminant, such as illuminant C. The observer’s task is to arrange the caps , which presented in random order, so as to form what he/she believes is a uniform sequence of colours. At the end of the test, the tester notes the number sequence of the caps and a score, from the absolute differences between neighbouring caps, is calculated. The score is the sum of the differences between neighbouring caps. This colour vision test was performed twice from each observer. A score lower than 50 was accepted as normal and the observer was classiﬁed as colour normal according to this test (Kinnear & Sahraie, 2002). If the score was greater than 50 the observer did not participate in the main experiment.

Ishihara plates

The Ishihara plates consist of isoluminant small discs. Differently coloured discs form a number or a line on a uniform background. The colours of the different discs are chosen according the confusion lines for protanopes, deuteranopes and tritanopes. That means that a colour normal observer will read the plates easily while a colour deficient observer will not be able to read the plates that contain colours across the confusion lines of his/her colour deficiency. The Ishihara plates is an easy and quick way for identifying if someone has a colour vision defect. It is not though very accurate on categorising the colour deficiency (Birch, 1979). An observer was tested in the first 24 plates of the 38 plates Edition (1979) Ishihara colour vision test. Less than 4 errors in reading the numbers is considered as normal (Committee on Vision, 1981). More than 4 errors indicate that the observer has a colour vision defect and thus he/she was excluded from the main experiments.

64 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

The Nagel Anomaloscope

The Nagel Anomaloscope is a very reliable test for identifying protanopes, deuteranopes and protanomalous. A circular field is divided into two equal semicircular fields. The lower part is a standard monochromatic yellow, of 589nm, the intensity of which can be adjusted. The top is a mixture of red and green monochromatic lights, of 670nm and 545nm respectively and a knob is used to change the mixture ratio of the two wavelengths. The task for the observer is to adjust the ratio of the red green lights to form a yellow that matches the lower field. The Nagel Anomaloscope is calibrated with colour normal observers. Depending on the range of the adjusted values, it is possible to char- acterise dichromats and anomalous trichromats in terms of their anomalous coefficients. The observers did ten matches with their right eye (the only one used for the main experiments). If the mean of their matches was within the normal range then they were regarded as colour normals otherwise they were excluded from the experiments (Committee on Vi- sion, 1981).

2.7.2 Asymmetric matching paradigm

The main method used in this study is an asymmetric matching paradigm. The observers conducted the experiment monocularly using their right eye. The distance was 50cm and a chin rest was used to assure constant distance and minimal head movements. Before the start of the experimental procedure, the observers were adapted for about 10 minutes to the background illuminant C (at 12.5cd/m2) subtending 37.2◦ x 29.3◦. The overall room illumination was dark. The observers had control of an infrared response box to adjust the chromatic axis and purity using the method of adjustment. A trial run was allowed so that the observers familiarised themselves with the response box and the changes of chromatic axes and purity.

65 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

A black ﬁxation cross was always on the screen and from that point a probe (or reference) spot of 1◦ diameter appeared at 1◦ eccentricity for 380ms. Another spot, the test, of 3◦ diameter (depending on the experiment), appeared simultaneously with the probe at variable eccentricities (see Figure 2.10). Different eccentricities and visual ﬁelds were used, depending on the particular experiment.

Figure 2.10: The stimulus configuration for nasal visual field (right eye). The background illuminant C was subtended 37.2◦ × 29.3◦. On the screen there was always a black fixation cross. 1◦ nasally from the cross a 1◦ probe spot was appearing for 380ms. A 3◦ test spot appeared, simultaneously with the probe spot, at 10◦ - 23◦ nasally from the fixation cross

The task for this experiment was to match the two spots in hue and saturation. The observer could change the chromatic axis and purity of the test spot with the response box, using the method of adjustment. The chromaticity of the probe spot was pre-set by the program. The probe purity was usually 0.5 (unless stated otherwise) and the starting axis was always 0◦. The observer had to find a match between the probe, of 0◦ and 0.5 purity, and the test spot. Afterwards, the axis of the probe spot was changed and the observer had to find again a match between the new probe and the test spot. This procedure was carried out for many different chromatic axes, depending on the specific requirements of the experiment.

66 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

Figure 2.11: Chromaticity coordinates of the probe spot (black dots connected with a line) and the chromaticity coordinates of the test spot (open circles connected with a line. The star is illuminant C. Note that this graph does not show which match spot corresponds to which probe spot. Though, hue rotation information can not be extracted but only saturation.

Figure 2.11 and Figure 2.12 show the data from an asymmetric matching experiment, using a test spot of 3◦ diameter at 18◦ eccentricity and probe spot of 1◦ and 0.5 purity. Figure 2.11 is a graph which visualises in colour space the probe and test chromaticities. The black dots are the chromaticities of the probe and the open circles connected with a line are the matched chromaticities of the peripheral test spot. As it is explained in the colour space section the distance from the white point deﬁnes the purity. It can be seen that at some regions of the colour space the purity of the test spot was altered. Figure 2.12a depicts the rotation of the chromatic axis and Figure 2.12b shows the increase or decrease of the purity. Rotation of the actual axis means that the observer had to rotate the axis of the test, clockwise or anticlockwise (positive or negative respectively), to perceive the same hue between the probe and the test. For example, when the probe

67 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

Figure 2.12: Panel a shows the matching results for hue rotation. The x axis is the chromatic axis of the probe. The y axis is the hue rotation of the test spot. For example, when the probe was at 90◦ the observer rotated the chromatic axis of the test spot by about -30◦ in order to match the two spots in hue. Panel b depicts the saturation of the test spot as a function of chromatic axis. The saturation of the probe spot was always 0.5 (straight line). When the probe spot was at 180◦, the observer needed to increase the saturation of the test spot to about 0.9 in order to match the two spots in saturation. was presented at 90◦ (x axis), the observer needed to rotate the axis of the test spot by about −30◦ (y axis). So, while the test spot was at 60◦ and the probe at 90◦, the observer perceived them as equal hue. Figure 2.12b shows the saturation change as a function of chromatic axis. An increase or decrease of saturation means that the observer had to increase or decrease the purity of the test in order to perceive it the same as the probe. So, saturation equal to 0.5 means no change, saturation greater than 0.5 means an increase and saturation less than 0.5 means decrease in saturation. When, for example, a saturation of 1 is given as a match, this means that the observer perceives the peripheral spot of half saturation and needs to double the saturation to ﬁnd a match with the probe.

68 2.7. EXPERIMENTAL PROCEDURES AND COLOUR VISION TESTS

2.7.3 Naming experiment

The naming experiment was used to identify the unique hues. The procedure followed in that experiment is the same as in Parry et al. (2006). The stimulus layout was the same as in the matching experiment but without the probe spot (see Figure 2.10). The observer ﬁxated on the cross and the test spot appeared eccentrically (the eccentricity depended again on the speciﬁc experimental requirements). The task for the observer was to name the colour of the peripheral spot.

Figure 2.13: The four colour naming functions as a function of chromatic axis. The red colour naming function (filled diamonds) defines how many times (y axis) a chromatic axis (x axis) was named as red. The same applies for blue (open diamonds), green (filled triangle) and yellow (open triangles) colour naming functions. The arrows indicate the unique hues which are defined at the central maxima of each colour naming function.

A Four Alternative Forced Choice (4AFC) method was used. The observer had to name the spot as red, blue, green or yellow. 40 different chromatic axes were used, from 0◦ to 360◦ in steps of 9◦. Each chromatic axis was presented 20 times for 380ms each time and all 800 stimuli were presented in random order. For each colour name category, a naming function is obtained. These functions describe how many times the observer

69 2.8. ETHICS named the test spot as red, blue, green or yellow (see Figure 2.13). For example, the 180◦ chromatic axis was identified 95% of the times as green and only 5% as blue (that means 19 times was named as green and just once as blue). The unique hues are defined as the central maxima of each colour naming function. As seen in Figure 2.13 each colour naming function has a plateau. The middle point of each plateau is defined as the unique hue (indicated by the arrows). The red colour naming function gives unique red, the blue naming function unique blue, the green naming function unique green and the yellow colour naming function unique yellow.

2.8 Ethics

The experiments presented in this study are conducted after ethics approval from the University of Manchester Ethics Committee (ref No: 08279). The observers participated voluntarily and prior the beginning of the experiment written consent form was obtained. The experimental procedures where designed to minimise any discomfort and/or incon- venience and observers were free to withdraw at any time.

70 2.9. REFERENCES

2.9 References

Birch, J. (1979). Acquired color vision defects. In J. Pokorny & V. C. Smith (Eds.), Con- genital and acquired color vision defects (pp. 243–348). London: Grune Stratton. Committee on Vision, N. R. C. (1981). Procedures for testing color vision: report of working group 41, National Academy of Science. De Valois, R. L., De Valois, K. K., Switkes, E., & Mahon, L. (1997). Hue scaling of isoluminant and cone-speciﬁc lights. Vision Res, 37(7), 885–97. Derrington, A. M., Krauskopf, J., & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol, 357, 241–65. Guild, J. (1931). The colorimetric properties of the spectrum. Philosophical transactions of the Royal Society of London, 230A, 149–187. Judd, D. (1951). Colorimetry and artiﬁcial daylight, Proceedings 12th Session CIE, Stock- holm, 1(TC7). Bureau Central de la CIE, Paris. Kaiser, P. K., & Boynton, R. M. (1996). Human color vision (Second). Washington, DC: Optical Society of America. Kinnear, P., & Sahraie, A. (2002). New farnsworth-munsell 100 hue test norms of normal observers for each year of age 5-22 and for age decades 30-70. Br J Ophthalmol, 86, 1408–11. Krauskopf, J., Williams, D. R., & Heeley, D. W. (1982). Cardinal directions of color space. Vision Res, 22(9), 1123–31. MacLeod, D. I., & Boynton, R. M. (1979). Chromaticity diagram showing cone excitation by stimuli of equal luminance. J Opt Soc Am, 69(8), 1183–6. Parry, N. R., McKeefry, D. J., & Murray, I. J. (2006). Variant and invariant color perception in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 23(7), 1586– 97.

71 2.9. REFERENCES

Smith, V. C., & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Res, 15(2), 161–71. Stanikunas, R., Vaitkevicius, H., Kulikowski, J. J., Murray, I. J., & Daugirdiene, A. (2005). Colour matching of isoluminant samples and backgrounds: a model. Per- ception, 34(8), 995–1002. Vos, J. J., & Walraven, P. L. (1971). On the derivation of the foveal receptor primaries. Vision Res, 11(8), 799–818. Wright, W. (1928-29). A re-determination of the mixture curves of the spectrum. Trans- actions of the Optical Society London, 30, 141–164.

72 CHAPTER THREE

NASAL-TEMPORAL DIFFERENCES IN CONE OPPONENCY IN THE NEAR PERIPHERAL RETINA

Authors: A. Panorgias, N.R.A Parry, D.J. McKeefry, J.J. Kulikowski & I.J. Murray

HIS chapter has been published in the journal of Ophthalmic and Physiological Op- T tics as part of the proceedings of the 4th European Meeting in Visual and Physio- logical Optics in 2008.

3.1 Abstract

The purpose of this study is to establish whether nasal-temporal differences in cone photoreceptor distributions are linked to differences in colour matching performance in the two hemi-fields. Perceived shifts in chromaticity were measured using an asymmetric matching paradigm. They were expressed in terms of activation levels of L-M and S-(L+M) cone opponent channels. Up to 19◦ eccentricity there was little difference in chromaticity shifts between nasal and temporal retina for either channel. For matches beyond 19◦ eccentricity, L-M activation is significantly lower in the nasal field and the S-(L+M) channel was equally activated in both fields. The data are consistent with the asymmetric distribution of L- and M-cones in the nasal and temporal retinae.

73 3.2. INTRODUCTION

colour matching, cone opponency, nasal-temporal retina, peripheral retina

3.2 Introduction

The quality of colour perception in the peripheral visual field declines with eccentricity. Observers describe a desaturation effect when coloured stimuli in the periphery are compared with similar stimuli placed in the central visual field. Changes in hue are also reported, as described in the early papers by Moreland and Cruz (1959) and Stabell and Stabell (1976b). The most obvious explanation for the reduction in colour vision in the periphery is that sampling of the retinal image by cones declines as their density is reduced. A second issue considered by many authors (Stabell & Stabell, 1976a; Buck, 1997; Buck, Knight, & Bechtold, 2000) is the possible role of rods. Rod density is much greater in the peripheral than the central retina, reaching a peak at around 20◦. Rods have the potential to influence both the hue and the saturation of peripheral targets in many different ways (Volbrecht, Nerger, & Ayde, 1993). When the activity of rods is minimized and perception is mediated primarily by cones, there are indications that stimulus size and other factors, such as cortical magnification, compensate for the reduced quality of colour vision in the peripheral field (Abramov, Gordon, & Chan, 1991; van Esch, Koldenhof, van Doorn, & Koenderink, 1984; Vakrou, Whitaker, McGraw, & McKeefry, 2005). There are many advantages to interpreting these changes in colour vision in terms of cone-opponent pathways. It is well known that the early stages of human and higher primate vision are mediated by three independent mechanisms (Hering, 1964; Hurvich & Jameson, 1955; Ingling & Huong-Peng-Tsou, 1977); one based on antagonistic interactions between L- and M-cones, another based on antagonistic interactions between S-cones and some combination of L-, M- and S-cones

74 3.2. INTRODUCTION

(Lee, Valberg, Tigwell, & Tryti, 1987; Krauskopf, Williams, & Heeley, 1982; Derring- ton, Krauskopf, & Lennie, 1984), and a third which combines the activity of the L- and M-cones and signals luminance. These channels have a well deﬁned neural substrate in the retina and LGN (Lee et al., 1987; Krauskopf et al., 1982; Derrington et al., 1984). They must represent the start of a cascade of neural events that culminate in the perception of colour. There is both neurophysiological and psychophysical evidence for additional colour channels, probably mediated by cortical neurons (but see Tailby et al. (2007); Tailby, Solomon, and Lennie (2008)) . Most cells in the striate cortex (V1) respond to a combination of chromatic and achromatic information (Johnson, Hawken, & Shapley, 2001; Vidyasagar, Kulikowski, Lipnicki, & Dreher, 2002) but a small number, of the order of 10%, respond to pure colour. These show only a slight bias toward the L-M and S-(L+M) opponent clustering which is so obvious in the LGN (Lennie, Krauskopf, & Sclar, 1990; Solomon & Lennie, 2007). Psychophysical evidence for the existence of additional colour mechanisms comes from adaptation experiments. Webster and Mollon (1991) showed that when an observer is adapted to a particular direction in colour space, colour appearance is always distorted away from this direction. They suggested the existence of multiple colour channels, each one orientated to a certain direction in colour space. Recent psychophysical studies suggest that there is a greater decline in the sensitivity of red-green opponency compared with blue-yellow opponency as eccentricity increases (Mullen & Kingdom, 2002; Mullen, Sakurai, & Chu, 2005). It is thought that this reﬂects differences in the neural pathways of the two mechanisms, in particular the substantial difference in distribution across the retina of S-cones compared to L- and M-cones. The latter are arranged in clusters whereas S-cones are randomly distributed outside the central 0.4◦ where they are absent (Williams, MacLeod, & Hayhoe, 1981; Curcio et al., 1991; Hofer, Carroll, Neitz, Neitz, & Williams, 2005) The functional differences between L-M

75 3.3. METHODS and S-(L+M) cone-opponency across the retina were described by Murray, Parry, and McKeefry (2006) and McKeefry, Murray, and Parry (2007), who used an asymmetric matching paradigm to show that activity in the L-M channel declined more rapidly with eccentricity than in the S-(L+M) channel. It is of interest to study the peripheral retina because it is possible that as the numbers of cones available to the chromatic system decreases with eccentricity, there may be a change in the strategy for coding chromatic information. As outlined above, it might be expected that processing which is dependent on S-cones may change in a different manner with eccentricity, to that based on L- and M-cones, simply because of their different retinal distributions. In the present report we are interested in the nasal-temporal differences in peripheral colour perception. Perry and Cowey (1985) have shown that there are substantial differences in numbers of ganglion cells in the nasal and temporal retina. Similar asymmetries are seen in the distributions of photoreceptors (Curcio et al., 1991). The main aim of the present study was to investigate how these nasal-temporal differences in photoreceptor and ganglion cell distributions are reﬂected in the performance of a colour-matching task in the peripheral visual ﬁeld.

3.3 Methods

The equipment used for this study consisted of a SONY c Trinitron R Multiscan520GS monitor, a high resolution ViSaGe visual stimulus generator (Cambridge Research Systems c Ltd, Rochester UK), specially designed software and an infrared CB6 response box (Cam- bridge Research Systems c Ltd, Rochester UK). A PR650 SpectraScan R Colorimeter

(Photo Research Inc) and a ColourCal R Colorimeter (Cambridge Research Systems c Ltd, Rochester UK) were used to gamma correct the monitor and ensure the accuracy of the colour stimuli. The calibration method used is described in detail by Parry, McKeefry,

76 3.3. METHODS and Murray (2006). Four subjects took part in the experiments, aged 25, 28, 30 and 57 years. Prior to the experiment the subjects’ colour vision was tested using the Farnsworth Munsell 100 Hue test and the Nagel Anomaloscope. All were within normal limits. All stimulus adjust- ments were made in CIE 1931 xy space, however the chromaticity of the starting point was chosen to be the equivalent of 0◦ in MBDKL space, following the approach of De Val- ois, De Valois, Switkes, and Mahon (1997). The chromatic axis is described by the angle between a vector and the 0◦ axis and the purity by the length of this vector. The starting point of this vector is the background illuminant C (x=0.31, y=0.316, L=12.5cd/m2). The 0◦ axis coincides with the cardinal red axis, 180◦ is cardinal green, 90◦ is cardinal blue and 270◦ is cardinal yellow. In other words, the 0◦-180◦ axes are the silent S-cone axes and the 90◦-270◦ axes are the silent L- and M-cone axes. For this experiment, the vector length was normalised so that vector length equal to 0.07918 is purity 1 in the CIE1931 xy colour space. Purity of 0.5 means that the vector length is halved (=0.03959) (see Figure 3.1). An asymmetric matching paradigm, as described by Parry et al. (2006), was used. Viewing distance was 50cm and a chin rest was used to assure constant distance and minimal head movements. Before the start of the experimental procedure, the observers were adapted, for about 5 minutes, to illuminant C of luminance 12.5cd/m2, subtending 37.2◦x29.3◦ (WxH). A fixation cross was always at the centre of the screen and a probe (reference) spot of 1◦ diameter was presented at 1◦ eccentricity for 380ms. Another spot, the test (3◦ diameter) appeared simultaneously with the probe at the following eccentricities (11◦, 19◦, 21◦ and 23◦ in both nasal and temporal field). These were chosen to match the previous work (Parry et al., 2006) but to take account of the blind spot in the temporal visual field, where areas between 13◦ and 17◦ could not be tested. The task for the observer was to match the probe and the test spot in terms of hue and saturation, using

77 3.3. METHODS

Figure 3.1: The CIE1931 xy colour space and the monitor gamut. The background was illuminant C (x=0.31, y=0.316, L=12.5cd/m2) shown as a star. The four axes 0◦, 90◦, 180◦ and 270◦ are the cardinal red, blue, green and yellow respectively, described by Derrington et al. (1984). The 8 black dots are the chromaticities of the probe spot. Probe purity was always 0.5 and the hue ranged between 0◦ and 360◦ in steps of 45◦. The numbers on the spectrum locus are the dominant wavelengths. the response box and changing the chromatic axis in steps of 5◦ and purity in steps of 0.1. The probe purity was always 0.5 and the starting chromatic axis was always the 0◦ axis. After a match, the chromatic axis of the probe spot was changed by 45◦ and another match was obtained. The overall process was carried out for 8 different chromatic axis of the probe spot, in steps of 45◦. As soon as the procedure was completed for a given eccentricity, the arrangement of the stimuli was changed to test the same eccentricity but in the other visual hemi-field. The experiment began with the test spot at 11◦ eccentricity in the nasal field. The data analysis is based on the cone opponent model, first described by Stanikunas, Vaitkevicius, Kulikowski, Murray, and Daugirdiene (2005). This linear cone opponent model assumes that the L-M and S-(L+M) channels remain silent under background illuminant C, the two mechanisms are orthogonal and the L/M ratio of the observers is 1.6. This means that the L-M channel is not activated by the 90◦ and 270◦ axes, while

78 3.4. RESULTS the S-(L+M) channel in not activated by the 0◦ and 180◦ chromatic axes. The Equation below (3.3.1) describes the model. The L-M and S-(L+M) activation values have been calculated for both nasal and temporal ﬁeld and each eccentricity.

      L + M 0.63 0.395 0 L              L − M  =  2.21 −2.6 0  ×  M  (3.3.1)             S − (L + M) −0.35 −0.35 1.02 S

The analysis is based in the Root Mean Square Deviation (RMSD) from the probe’s L-M and S-(L+M) activation values. The RMSD is calculated by the formula

s P9 (x − x )2 RMSD = i=1 i oi (3.3.2) N

where xi is the L-M or S-(L+M) i data point, xoi is the probe’s L-M or S-(L+M) activation value and N the number of data points for each data set.

3.4 Results

Figure 3.2 depicts the chromaticities of the probe and the test spot in CIE1931 xy colour space for 23◦ eccentricity for both visual ﬁelds. Note that when an observer alters chromatic axis and purity of the test stimulus to match the chromaticity of the probe, they are compensating for a peripheral hue and saturation shift. For example, setting the purity of the test to 1, meant that the observer needed to double the purity of the test spot to ﬁnd a match with the probe, which was always at 0.5. The same applies for the hue shifts. When the observers rotate the chromatic axis by

79 3.4. RESULTS

Figure 3.2: The chromaticities of the probe and the matched test spot for 23◦ eccentricity in the CIE1931 xy colour space. The grey lines are the four cardinal axes. The black dots are the chromaticities of the probe spot. The black open circles connected with black lines are the averaged chromaticities of the test spot, from four observers. The light grey shaded area depicts ±1S.D. The dashed lines connect the chromaticity of the probe spot, of a given chromatic axis, with the corresponding chromaticity of the test spot. The background illuminant C is plotted as a star. a) nasal ﬁeld, b) temporal ﬁeld.

+20◦, they perceive the hue of the test spot rotated -20◦. The data in Figure 3.2 are the average of four subjects. Each observer made a single series of observations for each condition. The four grey lines are the four cardinal axes. The black dots represent the chromaticities of the probe. Illuminant C is illustrated as a star. The black open circles connected by the black lines indicate the chromaticities of the test spot, averaged across observers. The grey open circles with the grey line are ±1S.D. The dashed lines connect each probe chromaticity with the corresponding test chromaticity, thus showing the perceived rotation of the test hue. The numbers next to test chromaticities are the corresponding chromatic axes. The data in Figure 3.2a are for the nasal ﬁeld. Comparable with other studies (Parry et al., 2006) there is a decrease in perceived saturation along the red-green cardinal axes, while the saturation effects along the blue-yellow cardinal axes are less marked. With

80 3.4. RESULTS the exceptions of 0◦ and 135◦ axes, hues are rotated negatively which means that the hue shifts are either towards red or towards green. Importantly, only minimal hue shifts were seen at around 0◦ and 180◦ as described in Parry et al. (2006) and McKeefry et al. (2007), where they were described as the invariant hues. Figure 3.2b depicts the average data for the same eccentricity and from the same four subjects for the temporal visual field. There is a clear difference in saturation needed to obtain a match, between the nasal and the temporal fields. In the nasal field the observers needed to markedly increase the saturation by several steps in order to achieve a match, while in the temporal field the increase in saturation is smaller. Also, greater hue rotations are seen in the nasal than the temporal field. It is evident that the inter-subject variability is greater for the nasal than for the temporal visual field, especially along the red-green axes. Calculating the area of the CIE1931 xy colour space which is enveloped by the test chromaticities, it can be seen that the area at the nasal field is x2.56 greater than the area of the temporal field, reflecting the increase in saturation needed when stimuli are presented in the nasal field. Overall however, chromaticity matches in the two hemi-fields can be regarded as being only quantitatively different, as outlined below. Using the cone opponent model (Stanikunas et al., 2005; Murray et al., 2006; Mc- Keefry et al., 2007), the activations of the L-M and S-(L+M) channel, for the matching stimuli, were calculated. These data are shown in Figure 3.3. Figure 3.3a shows the averaged activation (N=4) of the L-M channel for the matched peripheral stimulus compared to the central probe for four different eccentricities (11◦, 19◦, 21◦ and 23◦) for the nasal and the temporal visual fields (left and right column respectively). Figure 3.3b depicts the activation of the S-(L+M) channel for nasal and temporal field (left and right column respectively). The solid black line is the activation of the L-M and S-(L+M) channel (Figure 3.3a and b respectively) corresponding to the probe spot at 1◦ eccentricity. The grey line with

81 3.4. RESULTS

Figure 3.3: The averaged activation of the two cone opponent channels as a function of the chromatic axes for four different eccentricities, 11◦, 19◦, 21◦ and 23◦ (first, second, third and fourth row respectively). The black lines depict the channel activation, for the probe. The grey line with the black open circles represents the activation of the channels, induced by the test stimulus. The error bars are ±1S.D. a) L-M channel, b) S-(L+M) channel. the open circles is the activation of the two opponent channels for the matching test spot at different eccentricities. Regarding the L-M channel (Figure 3.3a), it can be seen that, as the eccentricity increases, there is a reduction in the activation of the channel at the nasal visual field (deviation from the foveal activation). For the temporal field, there is still a reduction in activation of the L-M channel, which remains almost stable across the temporal visual field. The difference in activation between the nasal and the temporal field is obvious, especially for eccentricities greater than 19◦. There is a reduction in the activation of the S-(L+M) channel also (Figure 3.3b), but there is little or no difference between the nasal and the temporal field for this channel. For the L-M channel, a statisti-

82 3.5. DISCUSSION cally significant difference in RMSD was found (p=0.015, a=0.05) between the nasal and the temporal visual field (paired sample t-test). No statistically significant nasal-temporal difference in the RMSD was found for the S-(L+M) channel (p=0.9, a=0.05).

3.5 Discussion

In this study an asymmetric matching paradigm was used to investigate how the two different attributes of chromaticity, hue and saturation, are perceived in peripheral retina. As in previous work (Parry et al., 2006; Murray et al., 2006; McKeefry et al., 2007) some hues are found to remain invariant with retinal eccentricity while greater shifts occur for others, especially in the blue and yellow regions. Marked differences between hue and saturation shifts were found as a function of eccentricity, suggesting that these attributes are mediated by different neural mechanisms. Peripheral hue and saturation shifts are not uniform across colour space; areas of colour space showing maximum saturation shifts (along the red-green cardinal axes) exhibit minimal hue shifts, whilst areas with maximum hue shifts (along the blue-yellow cardinal axes) showed minimum saturation shifts. There is substantial physiological data to account for the reduction in colour performance as stimulus eccentricity is increased. For example, L- and M-cone density declines steadily (Curcio et al., 1991), the ganglion cell density decreases (Perry & Cowey, 1985) and the ganglion cell soma-size increases with eccentricity (Stone & Johnston, 1981). Recent experiments have studied the neural circuitry between cones and midget ganglion cells in the peripheral retina, using an in vitro preparation of the macaque retina (Diller et al., 2004) and an in vivo technique to monitor ganglion cell responses (Solomon, Lee, White, Ruttiger, & Martin, 2005). The latter paper reports that L-M cone-opponency is maintained at eccentricities up to 50◦, whereas Diller et al. (2004) show peripheral midget ganglion cells to be mainly non-opponent. The apparent discrepancies between the two

83 3.5. DISCUSSION papers are discussed in Solomon et al. (2005) and are due mainly to the fact that Diller et al. (2004) limited their measurement to a single temporal frequency of 9.7Hz. Solomon et al. (2005) found the opponent responses at lower temporal frequencies and concede that there are many factors that may reduce the quality of the L-M opponent signal, such as peripheral ganglion cells’ limited range of temporal frequencies, greater phase dispersion and the proportion showing non-opponent responses. Psychophysical experiments showed that the L-M cone-opponency falls steadily with eccentricity and becomes functionally absent beyond 25◦-30◦ (Mullen et al., 2005). The S- (L+M) channel appears more robust with eccentricity and preserves its sensitivity across the visual field while the chromatic sensitivity of the L-M channels decreases precipi- tously (Mullen & Kingdom, 2002). This observation is reflected in our findings. The loss in colour performance is greater, as the retinal eccentricity increases, especially for stimuli in the red-green region of the colour space, but only for the nasal visual field. Overall, chromaticity shifts are qualitatively similar in the nasal and temporal visual fields; i) hue and saturation shifts increase with eccentricity, ii) there is an elongation in saturation shifts along the 0◦-180◦ cardinal axes, iii) hue shifts rotate towards either the red or green cardinal axes and iv) hue rotations are greater for 90◦ and 270◦ axes while saturation shifts are greater for 0◦ and 180◦ axes. There are, however, quantitative differences between the two hemi-fields. Chromaticity shifts are greater in the nasal than the temporal visual field. The observations of Curcio et al. (1991) and Perry and Cowey (1985), that cone and ganglion cell density is greater in nasal retina (temporal visual field), support this observation. Other psychophysical studies are in agreement with the nasal- temporal differences described here. Stabell and Stabell (1982) found that colour vision is superior in the temporal visual field and Mullen (1991) reported that red-green sensitivity is higher in the temporal than the nasal field, for eccentricities beyond 15◦. In order to interpret these findings in terms of retinal and LGN physiology the chro-

84 3.5. DISCUSSION maticity shifts in nasal and temporal visual fields, were plotted in terms of the simple cone-opponent model described in Equation 3.3.1. This analysis shows that the apparent specialisation of L-M cone-opponency for central retina applies only to eccentricities within 19◦. Note that the task could not be performed between 13◦ and 17◦ eccentricity because of the blind spot. In the temporal field the L-M channel appears to be more robust for eccentricities greater than 19◦. In contrast, the S-(L+M) cone-opponency is preserved for both visual fields. We might speculate that this is linked to the underlying asymmetry in photoreceptor and ganglion distributions in the two hemi-retinae (Perry & Cowey, 1985; Curcio et al., 1991). Presumably, the veracity of colour matching relies on precise neural circuitry and, as for sensitivity, is compromised when the number of L- and M- photoreceptors and ganglion cells falls below a critical value. This critical value appears to have been reached at around 20◦ in the temporal retina (nasal visual field) for both L-M and S-(L+M) channels. In the nasal retina (temporal visual field) there appear sufficient neurons to support relatively accurate colour matching for both opponent channels. Other authors have derived colour spaces specific to the retinal locus of their stimulus. For example Newton and Eskew (2003) obtained a different colour space for central and peripheral viewing. In order to make direct physical comparisons between the central and matched peripheral stimuli, a single colour space (CIE 1931 xy) has been used which is based on a foveal 2◦ stimulus. The perceptual changes in the periphery reflect the fact that there is no single colour space which can be generalised for the whole retina. This of course is why, for example, the 10◦ colour space was derived. Clearly these issues are related: retinal inhomogeneity underlies the inability to make the same metameric matches at different eccentricities, the necessity to create different colour spaces for different retinal regions, and the colour shifts described here.

85 3.5. DISCUSSION

Author contribution

For this chapter/paper A. Panorgias did the experiments, the analysis and most of the writing. I.J. Murray contributed signiﬁcantly to helping writing the introduction and discussion. The experiments were conducted using software written by N.R.A. Parry. J.J. Kulikowski, N.R.A. Parry and D.J. McKeefry contributed by making corrections on the manuscript and discussing various issues during the experiments and writing.

86 3.6. REFERENCES

3.6 References

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90 CHAPTER FOUR

NAMING VERSUS MATCHING AND THE STABILITY OF UNIQUE HUES

Authors: A. Panorgias, J.J. Kulikowski, N.R.A. Parry, D.J. McKeefry & I.J. Murray

HIS chapter has been published in the journal of Ophthalmic and Physiological Op- T tics as part of the proceedings of the 20th International Color Vision Society meeting (ICVS), 2009.

4.1 Abstract

It is known that there is a distortion of hue and saturation in the peripheral visual ﬁeld. In previous studies, when an asymmetric matching paradigm was used, four hues in the blue, red, yellow and green regions of colour space were unchanged and these were referred to as peripherally invariant (Parry, McKeefry, & Murray, 2006). Three of these invariant hues were similar to unique blue, red and yellow. However, for most observers there was a marked difference between unique and invariant green. To investigate this apparent paradox, unique hues were measured using a range of eccentricities and colourimetric purities. An asymmetric matching and a 4AFC paradigm were used to establish peripherally

91 4.2. INTRODUCTION invariant and unique hues, respectively. In the asymmetric matching task the observer matched a peripheral spot with a parafoveal spot, for 24 different hues at 10◦ and 18◦ eccentricity and at 3 different purities (0.5, 0.75 and 1.0). In the 4AFC paradigm, 40 hues were presented 20 times at three purities (0.5, 0.75 and 1.0) and three eccentricities (18◦, 10◦ and 1◦). The observer had to name the hues as red, blue, green or yellow. Unique hues were found to be constant with eccentricity and purity. The unique green, established with 4AFC, was found to differ from the invariant green, determined using the matching task. However, red, blue and yellow invariant hues correspond well with unique hues. The data suggest that different mechanisms mediate the matching of green compared with the identiﬁcation of unique hues. This is similar to the difference between detection and discrimination of spectral stimuli: the detection process is dominated by the cone opponent mechanisms and is most sensitive, whereas more central processes, serving unique hues, inﬂuence discrimination.

Keywords: unique hues, peripherally invariant hues, colour naming, colour matching, peripheral colour vision

4.2 Introduction

How the basic hue mechanisms are encoded in human vision is an enduring problem. Ewald Hering’s qualitative description (Hering, 1964) of four colour sensations based on red, green, blue and yellow, was conﬁrmed quantitatively by Hurvich and Jameson (1955) who showed, using hue cancellation, that red-green and blue-yellow are organised as a pair of perceptually opposite hue mechanisms. What this means is that those with normal colour vision do not see reddish-greens or bluish-yellows. This simple observation relies on verbal expression to convey the four basic hue sensations, but it is universal; all colour

92 4.2. INTRODUCTION normal humans, regardless of language or culture (Berlin & Kay, 1969; Saunders & van Brakel, 1997) and age (Schefrin & Werner, 1990), can easily adjust a colour so that it is neither red nor green or neither blue nor yellow (Valberg, 1971). The four unique hues are the most overt and fundamental manifestation of the higher order organisation of colour processing (Mollon & Jordan, 1997). They represent the centres of the basic colour categories (De Valois, De Valois, Switkes, & Mahon, 1997), in that red and green are the colours seen when the yellow-blue mechanism is in equilibrium and blue and yellow are seen when the red-green mechanism is in equilibrium. They have been described as fundamental colour categories and how they depend on detection thresholds was described by Mullen and Kulikowski (1990). How they vary under different viewing conditions should provide clues for assessing models of the red-green and blue-yellow mechanisms and the locus of a putative physiological substrate. There is some evidence that neurons tuned to unique hues are present in the posterior inferior cortex of macaque monkey. This remains controversial but the idea is not new ( Stoughton and Conway (2008), but see: Mollon (2009); Conway and Stoughton (2009); Neitz and Neitz (2008)). It stems from the concept introduced in the 1970 of whether aspects of perception and thought are represented by the operation of specific ‘trigger-feature’ neurons Barlow (1972). Abramov and Gordon (2005) systematically investigated the influence of size, duration, intensity, purity and peripheral location on the colour appearance of yellow, green and blue coloured stimuli. Their participants used the ‘four necessary and sufficient terms’ of red, blue, green and yellow (see also Sternheim and Boynton (1966)). Abramov and Gordon (2005) found that unique yellow remained constant for all conditions. This is significant because it is known that the relative number of L- (long-wavelength sensitive) and M- (medium-wavelength sensitive) cones varies across the retina and it implies a central compensating mechanism that takes account of this. This mechanism must recalibrate

93 4.2. INTRODUCTION the inputs to the cone-opponent mechanism according to prior visual experience. A similar mechanism must exist to normalise the perception of yellow across the colour-normal population to allow for the different relative number of L- and M-cones in different individuals (Miyahara, Pokorny, Smith, Baron, & Baron, 1998). In a detailed investigation of hue and saturation shifts in the near peripheral visual ﬁeld, Parry et al. (2006) and McKeefry, Murray, and Parry (2007) highlighted the existence of what they called invariant hues. These colours were relatively unchanged in hue, for a range of different eccentricities and purities. With the exception of green, the peripherally invariant hues were close to the unique hues for 9 observers. It was also suggested that hue and saturation shifts were driven by different physiological mechanisms; peripheral shifts in the two attributes varied with eccentricity in different ways and although peripheral saturation shifts varied with size as is well known, hue shifts were largely independent of size. More recently, all four unique hues were found to be stable between two eccentricities (1◦ and 18◦), when tested with a four alternative forced choice naming paradigm (Kulikowski et al., 2009). The main aim of the experiments reported here is to investigate further the link between peripherally invariant hues, based on an asymmetric matching technique and the unique hues, determined using naming. Green is perceived as more desaturated in the periphery than other hues and it was considered important to eliminate purity as a confounding factor in the apparent disparity between peripherally invariant and unique green. Furthermore, the two paradigms may introduce bias. Naming may tap higher order, cognitive mechanisms whilst asymmetric matching may be mediated by lower order mechanisms.

94 4.3. METHODS

4.3 Methods

4.3.1 Stimuli

Stimuli were presented on a SONY c Trinitron R Multiscan520GS monitor using a high resolution ViSaGe visual stimulus generator (Cambridge Research Systems c Ltd., Rochester, UK). Specially designed software controlled the experiment and responses were obtained with an infrared CB6 response box (Cambridge Research System c Ltd., Rochester, UK). Prior to the experiments the monitor was calibrated using a PR650

SpectraScan R colorimeter (PhotoResearch Inc., Chatsworth, CA, USA) and a ColourCal R colorimeter (Cambridge Research Systems c Ltd., Rochester, UK), as described in Parry et al. (2006).

4.3.2 Colour space

The CIE1931 xy colour space, based on the 2◦ standard observer, was used and the description of the chromaticities was made in modiﬁed MacLeod-Boynton colour space in an isoluminant plane, as described in Derrington, Krauskopf, and Lennie (1984). Chro- maticity is described as the length and rotation of a vector originating from the background illuminant C (x=0.31, y=0.316 at 12.5cd/m2). In these experiments purity is de- ﬁned equal to 1 as a vector with length = 0.07918 in xy space. Stimuli of equal vector length form a circle. Hence, for example purity of 0.5 corresponds to half vector length of purity 1 (0.03959) and so on. Note that the observers manipulated the perceptual attributes of hue and saturation while their physical correlates are chromatic axis and purity. The 0◦, 90◦, 180◦ and 270◦ axes are the red, blue, green and yellow cardinal axes, respectively, described by Derrington et al. (1984). The xy coordinates for these axes are those described in De Valois et al. (1997).

95 4.3. METHODS

Figure 4.1: The CIE1931 xy colour space. The numbers at the border of the spectrum locus are the dominant wavelengths in nm. The dotted lines depict the cardinal red, blue, green and yellow axes (0◦, 90◦, 180◦ and 270◦ respectively). The dashed lines are the intermediate axes at 45◦ from each cardinal axis. The triangle (thin black lines) represents the monitor gamut. The three co-centre dotted circles show the three different purities used in this study. The inner light-grey dots is purity 0.5, the middle grey 0.75 and the outer black dots is purity 1.

The CIE1931 xy colour space is illustrated in Figure 4.1. The numbers at the border of the space are the dominant wavelengths in nm. The three dotted circles show the three different purities used for the experiments reported here. The outer dots is purity 1, the intermediate dots 0.75 and the inner dots is purity 0.5. The triangle shows the monitor gamut and the dashed lines depict the intermediate axes (deviating 45◦ from the cardinal axes). The point where the cardinal axes cross is the background illuminant C.

4.3.3 Observers

Two male observers (aged 27 and 29 years) took part in the experiments. Both have normal colour vision, assessed with Nagel Anomaloscope, Farnsworth-Munsell 100 Hue test and Ishihara plates (38-plate edition, 1979). The two subjects had prior experience of psychophysical experiments and cannot be considered as naive observers. Note that the data obtained from these two observers are totally compatible with the data obtained from

96 4.3. METHODS a larger population, described in Parry et al. (2006) who also used the same technique for peripheral matching and naming of unique hue experiments. Before the experimental procedure the observers were adapted for ten minutes to the background illuminant. Mild head restrain was achieved using a chin and forehead rest, placed at 50cm from the monitor. The data were collected in several sessions, within a two-week period.

4.3.4 Procedures

Naming - Unique hues

A 4 alternative forced choice (4AFC) paradigm was used to determine unique hues. Effectively subjects named a spot as red, blue, green or yellow, in that they indicated its appearance according to these terms. Three different eccentricities (1◦, 10◦ and 18◦) and three different purities (0.5, 0.75 and 1) were tested. The size of the spot was 3◦ for the 10◦ and 18◦ eccentricity and 1◦ for the 1◦ eccentricity. Eccentricity was determined from the centre of each spot. The presentation time was 380ms. 40 chromatic axes were used (from 0◦ to 360◦ in steps of 9◦) each one presented 20 times. Hence, at a particular eccentricity and purity a total of 800 spots were presented in random order. The number of the colour responses in each colour category was plotted as a function of the chromatic axes and the unique hues were deﬁned as the central maxima of these colour functions. For further details of the 4AFC paradigm see Parry et al. (2006).

Matching - Invariant hues

The asymmetric matching paradigm, described by Parry et al. (2006), was used to determine perceived hue and saturation shifts in the peripheral retina. A 1◦ probe (with its centre being always 1◦ from the ﬁxation point) and a 3◦ test spot (at 10◦ and 18◦ eccentricity) were presented simultaneously for 380ms. While the spots were absent,

97 4.4. RESULTS the mean monitor chromaticity was illuminant C at 12.5cd/m2 and so the observer was adapted to it all the time. The observer matched the probe with the test in terms of hue and saturation, to compensate any saturation change or any hue distortion in the peripheral spot. 24 chromatic axes were used (0◦ to 360◦ in step of 15◦) and three different purities of the probe (0.5, 0.75 and 1) were tested. The subject could adjust the chromatic axis, in steps of 5◦, and the purity, in steps of 0.1. The inter-stimulus interval was dependent on the observer’s strategy; in that, they initiated the presentation of the next stimulus by pressing a button. The minimum inter-stimulus interval was 500ms. The starting axis for the probe was always the 0◦ axis (the reddish part of the L-M cardinal axis) and the chromaticities were changed in sequence. Randomising the sequence had no effect on the results. The invariant hues are deﬁned as those that remain unchanged in hue with eccentricity.

4.4 Results

Data from two observers (HJT and AP) are shown in Figure 4.2, which shows the unique hues obtained by the naming paradigm for two eccentricities (1◦ and 10◦) and three purities (0.5, 0.75 and 1.0). The y axis plots the chromatic axes in degrees while in the x axis there are four categories, each one for one unique hue. Light grey bars represent 0.5 purity, grey bars 0.75 and black bars 1.0. For observer HJT, at 1◦ and 10◦ eccentricity and three purities (0.5, 0.75 and 1.0), unique red ranges between 9◦ and 18◦, unique blue between 117◦ and 126◦ (481.5 ± 1.2nm), unique green between 225◦ and 236◦ (532.5±7.1nm) and unique yellow between 288◦ and 306◦ (577.3 ± 4.6nm). The values in parentheses are the averaged computed dominant wavelengths across the two eccentricities and three purities. The dominant wavelength of a colour is calculated by drawing a line, on a chromaticity diagram, which

98 4.4. RESULTS

Figure 4.2: Data from the naming paradigm. Each cluster of three bars is a unique hue measured at 1◦ (left side graphs) and 10◦ eccentricity (right side graphs) for observers HJT and AP. The y axis is the chromatic axis in degrees. Each one of the three bars represent the unique hue measured at a different purity. Light grey is for purity 0.5, grey for 0.75 and black for purity 1.0. The numbers at the top of the bars are the averaged wavelengths in nm for each cluster. Note that the unique red occurs in the line of purples where hues cannot be described by a single wavelength. starts at the white point and passes through the chromaticity coordinates of that colour. The point where that line intersects the spectrum locus is identiﬁed as the dominant wavelength of that colour. Note that unique red cannot be described in terms of wavelengths because it falls on the line of purples, where chromatic axis cannot be expressed in terms of a single wavelength. For observer AP unique red lies between 13.5◦ and 36◦, unique blue is between 121.5◦ and 130.5◦ (483.7 ± 1.4nm), unique green is between 216◦ and 234◦ (532.8 ± 4.1nm) and unique yellow falls between 279◦ and 288◦ (574.8 ± 1.6nm).

99 4.4. RESULTS

There are minimal differences in the setting of unique hues within observers. How- ever, the data suggest that unique hues remain relatively stable across eccentricities and are independent of purity. A paired sample t-test for both observers shows no statistical difference between the two eccentricities (p=0.397 for HJT and p=0.169 for AP). Minor differences between observers are to be expected, as described by Webster, Miyahara, Malkoc, and Raker (2000).

Figure 4.3: Data from both naming and matching paradigms at 18◦ eccentricity, plotted in CIE1931 xy colour space. The light grey dots are the chromaticities of the probe. The black open circles, connected with a solid black line, are the peripheral matches (obtained by the matching experiment). The open diamonds are the invariant hues (those hues which remain unchanged with eccentricity) and the asterisks are the unique hues (obtained by the naming experiment). For each unique hue there are three data points, depicting the three different purities. The dotted lines are the cardinal axes. The dashed lines connect the invariant hues with the origin (Illuminant C).

Figure 4.3 shows results from both matching and naming experiments. The matching data are for 18◦ eccentricity and probe purity of 0.5. Unique hues were obtained at 18◦ eccentricity and at the three standard purities used for this study. The small grey dots depict the chromaticity of the probes and the open circles, connected with a solid black line, are the peripheral matches. When the observers decrease or increase purity or chromatic axis, they are compensating for a peripheral saturation or hue shift. For example if the observer ﬁnds a match by rotating the chromatic axis by +20◦ and increasing purity to 1,

100 4.4. RESULTS this means that they perceive the hue of the peripheral spot rotated by −20◦ and that its saturation is halved compared with the probe. The open diamonds indicate the hues that remain invariant for this eccentricity (invariant hues). Note that Parry et al. (2006) also showed that invariant hues are independent of eccentricity and our deﬁnition of invariant hue is based on this work (see Methods). The asterisks are the unique hues for three purities (0.5 for the inner, 0.75 for the middle and 1.0 for the outer asterisk). The solid lines through the unique hues are best-ﬁtted linear functions originating from the background (illuminant C).

Table 4.1: The table summarises data from matching and naming paradigm for HJT and AP at 18◦ eccentricity. Invariant and unique hue data are given in degrees ±1 S.D. The numbers in parentheses are the chromatic axes transformed in wavelengths (nm) ±1 S.D. The data are the averaged values of three purities (0.5, 0.75 and 1.0).

HJT AP Matching Naming Matching Naming (invariant) (unique) (invariant) (unique) Red 8◦ ± 1◦ 12◦ ± 5.2◦ 18.7◦ ± 1.5◦ 18◦ ± 4.5◦

Blue 112.3◦ ± 9.1◦ 123◦ ± 5.2◦ 114.6◦ ± 4.6◦ 121.5◦ ± 4.5◦ (478 ± 5nm)(483 ± 1.7nm)(479 ± 2.3nm)(482 ± 1.5nm)

Green 180◦ ± 5◦ 228◦ ± 5.2◦ 196◦ ± 5.3◦ 219◦ ± 2.6◦ (496 ± 1.5nm)(530 ± 7.5nm)(501 ± 2.5nm)(518 ± 2.9nm)

Yellow 285◦ 294◦ ± 10.4◦ 305◦ ± 19◦ 288◦ ± 4.5◦ (575nm)(580 ± 5.2nm)(587 ± 12.6nm)(577 ± 4.5nm)

Table 4.1 summarises invariant and unique hues for both observers at 18◦ eccentricity. For observer HJT unique red, blue and yellow match reasonably well with the corresponding invariant red, blue and yellow. There is a difference of 48◦ (34nm) between invariant and unique green, with the ﬁrst being on the cardinal green axis. For observer AP, invariant red and blue are almost identical to unique red and blue, respectively. Here, there is

101 4.5. DISCUSSION a slightly larger difference between invariant and unique yellow. The difference between invariant and unique green is 24◦ (19nm). Interestingly, for both observers, unique hues are rotated clockwise, departing in a non-systematic way from the cardinal axes (Webster et al., 2000). With only one exception (AP, yellow) unique hues occur at a greater chromatic axis than invariant hues, which seem to be biased towards cardinal axes.

4.5 Discussion

One of the main objectives of these experiments was to establish the stability of unique hues with eccentricity and purity under the experimental conditions described here and compare them with invariant hues. Although based on a relatively small number of observers, the unique hues identiﬁed in these experiments are very similar to previously determined values. Traditionally, monochromatic lights have been used to obtain unique hues (Jordan & Mollon, 1995; Schefrin & Werner, 1990) and therefore expressed in wavelength. The data presented here have been obtained using a colour monitor and are therefore presented in chromatic angle in cone opponent space. To allow comparison with other studies, the data are expressed in terms of dominant wavelength and chromatic axis in Figure 4.3 and in Table 4.1. For example, Kuehni (2004) obtained a range of 568nm to 589nm for unique yellow compared with values obtained here of 580nm (HJT) and 577nm (AP); 455nm to 495nm for unique blue, whereas the values in this report are 483nm (HJT) and 482nm (AP); and 487 to 567nm for green compared with the values found here of 530nm (HJT) to 501nm (AP). The data in Table 4.1 are also compatible with many other studies (Webster et al., 2000; Wuerger, Atkinson, & Cropper, 2005) and it can be concluded that they are representative of the colour normal population. Al- though there appears to be a consensus regarding the approximate location of unique hues

102 4.5. DISCUSSION in colour space there is substantial individual variation when measurements are conﬁned to an isoluminant plane and moderate purity (Webster et al., 2000). The main message to emerge from the latter study is that unique hues cannot be linearly transformed from the cone-opponent axes. In the present study, the unique hues were stable across eccentricity and purity as reported by Abramov and Gordon (2005). Figure 4.2 illustrates this for three purities and two eccentricities and Figure 4.3 presents data for the same observers at a different eccentricity, namely 18◦ and the same purities. This observation eliminates the possibility that variations in unique hues at different eccentricities and purities might account for the difference between peripherally invariant and unique green. It is clear from Figure 4.3 that, as suggested in Parry et al. (2006), the unique hues represent perceptual anchor points which are transformed from the sub-cortical cone opponent mechanisms. The cardinal axes, based in the retinal ganglion cells, must undergo a rotation to account for the unique hues and this rotation almost certainly occurs in the visual cortex (Abramov & Gordon, 2005; De Valois et al., 1997) or may occur as early as in the primary visual cortex (Parkes, Marsman, Oxley, Goulermas, & Wuerger, 2009). Arrows in Figure 4.3 indicate this shift from cone opponent to colour opponent mechanisms. As reported previously (De Valois et al., 1997; Webster et al., 2000; Wuerger et al., 2005), the chromaticity for cardinal green is very different to pure green, having a distinct bluish appearance. Unique blue is similarly shifted with respect to the extreme blue end of the cardinal blue-yellow, which has a violet, rather than a blue appearance. Figure 4.3 also illustrates that whilst the blue-yellow opponent mechanism may be a monotonic linear function derived from equal inputs from L-cones and M-cones, the red- green mechanism does not exhibit the same symmetry; unique red and unique green do not lie on a line through the origin. This non-linearity shows that different S- and (L+M) cone weightings are needed for the sensation of pure red and pure green. In other words,

103 4.5. DISCUSSION this suggests two different red-green mechanisms, as described in Wuerger et al. (2005); Knoblauch and Shevell (2001); Webster et al. (2000) and Burns, Elsner, Pokorny, and Smith (1984). Hues that do not undergo a shift in the periphery appear to occupy a similar region in colour space to the unique hues in the case of red, blue and yellow but not for green. Invariant green is closer to the cardinal red-green axis in all observers, as reported in Parry et al. (2006) but, in contrast, unique green appears in the region between 180◦ and 270◦ (close to leaf-green) and is stable across eccentricities and purities. Unlike invariant red, blue and yellow, peripherally invariant green seems to be dictated by the cone opponent system. If it is assumed that data from the invariant hue experiment (the matching task) originate in sensory mechanisms (Foster & Nascimento, 1994) and those from the unique hue experiment (the naming task) from cognitive mechanisms, it should be expected that peripherally invariant hues would correspond to the cardinal axes, but this is patently not the case for invariant red, blue and yellow. Of course, the discrepancy between invariant and unique green could not be attributed neither to macular pigment density nor to cone photopigment density. It is known that macular pigment absorbs maximally at 460nm and 485nm (Snodderly, Brown, Delori, & Auran, 1984), while invariant green lies around 500nm and unique green at around 520nm for both observers. So, it is expected that macular pigment does not affect the ﬁndings in this region of the colour space. As far as the cone pigment absorption is concerned, there is a decline from central to peripheral retina and it is proportional to the number of cones (Elsner, Burns, & Webb, 1993). If cone pigment would have an impact in the results, should affect ﬁrst the region of the colour space where L-cones are excited the most, as they are the more numerous either in the central or in the peripheral retina. But this is not the case for the results described here. Discrepancy between invariant and unique hue is only observed in the green region of the colour space.

104 4.5. DISCUSSION

In this report purity and eccentricity are ruled out as possible confounding factors in the lack of correspondence between unique and peripherally invariant green. We ﬁnd that all four unique hues are stable with eccentricity and purity, using a four alternative forced choice naming paradigm. Hence, eccentricity and purity are not responsible for the discrepancy between unique and peripherally invariant green.

Author contributions

For this chapter/paper A. Panorgias did the experiments, the analysis and most of the writing. I.J. Murray contributed signiﬁcantly to preparing the introduction and discussion. The experiments were conducted using a software written by N.R.A. Parry. D.J. McKeefry, N.R.A. Parry and J.J. Kulikowski contributed by making corrections on the manuscript and discussing various issues during the experiments and writing.

105 4.6. REFERENCES

4.6 References

Abramov, I., & Gordon, J. (2005). Seeing unique hues. J Opt Soc Am A Opt Image Sci Vis, 22(10), 2143–53. Barlow, H. B. (1972). Single units and sensation: a neuron doctrine for perceptual psy- chology? Perception, 1(4), 371–94. Berlin, B., & Kay, P. (1969). Basic color terms: their universality and evolution. Berkeley and Los Angeles: University of California Press. Burns, S. A., Elsner, A. E., Pokorny, J., & Smith, V. C. (1984). The abney effect: chromaticity coordinates of unique and other constant hues. Vision Res, 24(5), 479– 89. Conway, B., & Stoughton, C. (2009). Response: towards a neural representation for unique hues. Curr Biol, 19(11), R442–443. De Valois, R. L., De Valois, K. K., Switkes, E., & Mahon, L. (1997). Hue scaling of isoluminant and cone-speciﬁc lights. Vision Res, 37(7), 885–97. Derrington, A. M., Krauskopf, J., & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol, 357, 241–65. Elsner, A. E., Burns, S. A., & Webb, R. H. (1993). Mapping cone photopigment optical density. J Opt Soc Am A, 10(1), 52–8. Foster, D. H., & Nascimento, S. M. (1994). Relational colour constancy from invariant cone-excitation ratios. Proc Biol Sci, 257(1349), 115–21. Hering, E. (1964). Outlines of a theory of the light sense. Harvard Univ., Cambridge, Massachusetts. Hurvich, L. M., & Jameson, D. (1955). Some quantitative aspects of an opponent-colors theory. ii. brightness, saturation, and hue in normal and dichromatic vision. J Opt Soc Am, 45(8), 602–16.

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Jordan, G., & Mollon, J. D. (1995). Rayleigh matches and unique green. Vision Res, 35(5), 613–20. Knoblauch, K., & Shevell, S. K. (2001). Relating cone signals to color appearance: failure of monotonicity in yellow/blue. Vis Neurosci, 18(6), 901–6. Kuehni, R. (2004). Variability in unique hue selection: a surprising phenomenon. Col Res App, 29(2), 158–162. Kulikowski, J., Daugirdiene, A., Panorgias, A., Murray, I., Stanikunas, R., & Vaitkevicius, H. (2009). Stages for extracting colour information: how the brain processes colour. Psichologija, 39, 71–92. McKeefry, D. J., Murray, I. J., & Parry, N. R. (2007). Perceived shifts in saturation and hue of chromatic stimuli in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 24(10), 3168–79. Miyahara, E., Pokorny, J., Smith, V. C., Baron, R., & Baron, E. (1998). Color vision in two observers with highly biased lws/mws cone ratios. Vision Res, 38(4), 601–12. Mollon, J. D. (2009). A neural basis for unique hues? Curr Biol, 19(11), R441–2; author reply R442–3. Mollon, J., & Jordan, G. (1997). On the nature of unique hues. In C. Dickinson, I. Murray & D Carden (Eds.), John dalton’s colour vision legacy. London: Taylor and Francis. Mullen, K. T., & Kulikowski, J. J. (1990). Wavelength discrimination at detection threshold. J Opt Soc Am A, 7(4), 733–42. Neitz, J., & Neitz, M. (2008). Colour vision: the wonder of hue. Curr Biol, 18(16), R700– 2. Parkes, L., Marsman, J., Oxley, D., Goulermas, J., & Wuerger, S. (2009). Multivoxel fmri analysis of color tuning in human orimary visual cortex. Journal of Vision, 9, 1–13.

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Parry, N. R., McKeefry, D. J., & Murray, I. J. (2006). Variant and invariant color perception in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 23(7), 1586– 97. Saunders, B. A., & van Brakel, J. (1997). Are there nontrivial constraints on colour categorization? Behav Brain Sci, 20(2), 167–79; discussion 179–228. Schefrin, B. E., & Werner, J. S. (1990). Loci of spectral unique hues throughout the life span. J Opt Soc Am A, 7(2), 305–11. Snodderly, D., Brown, P., Delori, F., & Auran, J. (1984). The macular pigment. i. ab- sorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Invest Ophthalmol Vis Sci, 25, 660–673. Sternheim, C. E., & Boynton, R. M. (1966). Uniqueness of perceived hues investigated with a continuous judgmental technique. J Exp Psychol, 72(5), 770–6. Stoughton, C. M., & Conway, B. R. (2008). Neural basis for unique hues. Curr Biol, 18(16), R698–9. Valberg, A. (1971). A method for the precise determination of achromatic colours including white. Vision Res, 11(2), 157–60. Webster, M. A., Miyahara, E., Malkoc, G., & Raker, V. E. (2000). Variations in normal color vision. ii. unique hues. J Opt Soc Am A Opt Image Sci Vis, 17(9), 1545–55. Wuerger, S. M., Atkinson, P., & Cropper, S. (2005). The cone inputs to the unique-hue mechanisms. Vision Res, 45(25-26), 3210–23.

108 CHAPTER FIVE

CONE CONTRAST IN PERIPHERAL RETINA

Authors: A. Panorgias, J.J. Kulikowski, N.R.A. Parry, D.J. McKeefry & I.J. Murray

5.1 Abstract

HE perceived colour of a target depends on its background. If both the stimulus and T the background are modiﬁed in a way which maintains cone contrast, then colour perception is expected to remain largely unchanged. Here, the deterioration of colour perception with eccentricity is interpreted in terms of cone contrast. The neurophysiological changes in the peripheral retina result in well known hue and saturation shifts. However, four hues remain relatively invariant with eccentricity and three of these correlate well with their corresponding unique hues. The exception is in the green region of the colour space. In the present study, 38 observers (26±8years, mean ±1S.D.) performed an asymmetric colour matching paradigm. 24 chromatic axes were presented as a 1◦ spot at 1◦ eccentricity. A 3◦ spot presented at 18◦ eccentricity. The task for the observers was to ﬁnd a match between the two spots by changing the chromatic axis and purity. Moreover, 3 observers performed a 4 alternative forced choice (4AFC) naming experiment to determine their unique hues. They had to name the coloured stimuli, presented at 18◦ eccentricity,

109 5.2. INTRODUCTION as either red, blue, green or yellow. Unique hues were deﬁned at the central maxima of the resultant four colour naming functions. The results show that despite obtaining a match between parafoveal and peripheral stimuli, the peripheral L- and M-cone contrast do not match with the parafoveal L- and M-cone contrast. S-cone contrast calculations indicate good adherence between parafoveal and peripheral stimuli. The peripheral RMS cone contrast matches the parafoveal with a few exceptions. These were most apparent in the bluish-green region of the colour space, and were particularly evident for invariant green. The results suggest that cone contrast, between matched parafoveal and peripheral stimuli, remains unchanged if the stimuli excite equivalent number of cones. If for example the stimuli are spatially separated on the retina and excite different number of cones, a mismatch in cone contrast is inevitably observed. The discrepancy between invariant and unique green might therefore, be attributed to reduced numbers of M-cones in the peripheral retina.

keywords: peripheral retina, cone contrast, invariant hues, unique hues, colour matching, colour naming

5.2 Introduction

It is well established that the physiological cascade which results in colour perception starts in the retina with photon absorption by the L-, M- and S-cones, and terminates in higher brain centres. An electrical signal is generated by each cone type which in turn is combined with the signal of neighbouring cones to form the second stage in the perception of colour. According to cone opponent theory, the L-cone signal is subtracted from that of M-cones to form the ‘red-green’ cone opponent channel. The signal of the S-cones is subtracted from a combination of L- and M-cone signals to form a second

110 5.2. INTRODUCTION

‘blue-yellow’ cone opponent channel. These two chromatic channels form distinct physiological pathways which terminate in different laminae of LGN and remain segregated in the input layer of V1. This description seems quite straight forward and simple; a signal is generated and it is transmitted through cells and neurons to the brain and gives rise to colour. If a change/modification occurs at the primary information, in the quanta absorbed by the different photoreceptors, then an equivalent shift should be expected in the output, i.e. perceived colour. But, as always in nature, difficulties are encountered when explain- ing observations that at first sight seem simple. One example is the constancy of colour perception despite changes in the physical spectral characteristics of a surface. A second example is that foveal-viewed colours undergo certain distortion as they are viewed eccentrically.

5.2.1 Contrasted colours and colour constancy

For simple sensory tasks, such as detection, the relative properties of a stimulus and not its absolute magnitude, are important. For example, visual sensitivity to a simple grating depends on the contrast between the low and high luminance stripes. It could be simpliﬁed by saying that the larger the difference in luminance the easier it is to detect the grating. In a similar manner, colour vision is due to the contrast between a stimulus and its background. Whittle (2003) very nicely demonstrates how, by changing only the background on which a stimulus is superimposed, its colour can be changed quite dramatically without changing its chromaticity. This phenomenon is what Whittle (2003) refers to as contrasted colours. Equivalently, by changing the stimulus and background chromaticity, but maintaing their cone contrast, colour perception is not changed. However, under certain circumstances, changing the cone contrast does not necessarily lead to a perceived colour change.

111 5.2. INTRODUCTION

An example is the relative stability of perceived colour under different illumination conditions. Imagine a surface under the midday light of the sun. That surface absorbs a part of the incident illumination and reflects a part of it. The reflected illumination is what reaches the eye of an observer. The observer perceives the surface as, lets say a green leaf, regardless of the background. As the hours are passing, the incident illumination from the sun on the leaf is changing and with it the reflected spectral characteristics which in turn means that the reflected illumination which reaches the eye of the observer is changed. But the observer still perceives the leaf as green. This phenomenon is described by Helmholtz as ‘discounting the illumination’ which means that the visual system, somehow, takes into account the change in illumination from the surroundings so as to perceive the same surface with the same colour. Many models and many theories have been suggested to describe this type of colour constancy. From cone coefficients of von Kries (1905/1970) to the Retinex model by Land and McCann (1971) and many others (Smithson (2005) offers a review on colour constancy). Foster and Nascimento (1994) showed that a different type of colour constancy (they referred to this as relational colour constancy) can be achieved only when the relative cone excitations of two surfaces remain unchanged under two different illuminations. This finding fits nicely the experimental data for natural scenes. It also provides a theoretical framework which might explain the basis of the distortion of colour in the peripheral visual field.

5.2.2 Colour perception in the periphery

Many studies have been conducted to describe peripheral colour vision and there is an agreement between them that there is a change in perceived colour by increasing eccentricity. Some examples of peripheral studies are those of Abramov and Gordon (1977), Stabell and Stabell (1976), Stabell and Stabell (1984) who found that the perceived sat-

112 5.2. INTRODUCTION uration of chromatic stimuli is reduced with eccentricity and that the judgement of some hues becomes ambiguous. Abramov, Gordon, and Chan (1991) showed that the peripheral deterioration described above could be eliminated by increasing the size of the peripheral stimuli and they concluded that there is a critical perceptive field, under which changes in peripheral colour vision are observed in respect with the foveal colour vision. How- ever, the saturation of their stimuli could not be restored even for the largest perceptive fields they used, for eccentricities more than 40◦. Mullen and Kingdom (2002) measured cone contrast sensitivity across the visual field and found a decline in the sensitivity of the red-green cone opponent mechanism while that of blue-yellow was relatively unchanged. While all the above studies on peripheral colour vision were using just one stimulus, to measure either sensitivity, saturation change or hue change in peripheral retina, Parry, McKeefry, and Murray (2006) introduced the asymmetric matching paradigm. With that experiment, the observers were asked to match a peripheral stimulus to a parafoveal one so as to compare central and peripheral vision. They concluded, in agreement with other studies, that there is a loss in saturation with increasing eccentricity but they also found a systematic change in hue appearance. They found that some parafoveal hues do not exhibit any change with eccentricity and these are what they called invariant hues (Parry et al., 2006). Three of them, in red, blue and yellow region of the colour space, were also found to be highly correlated with the corresponding unique hues. The forth, invariant green, was found to be different to unique green. Interestingly, almost none of the above studies analysed their findings in terms of cone contrast (the exception being Mullen and Kingdom (2002) and Sakurai and Mullen (2006) who measured sensitivity) to test whether peripheral cone contrast match the foveal cone contrast when a match is obtained. The idea behind this report is to fill this gap and to ask how cone contrast of peripheral colour matching relates to foveal cone contrast. In other words, does peripheral colour matching mean that the cone contrast remain the

113 5.3. METHODS same for peripheral and central targets? Another question to answer is what is the cone contrast status of invariant and unique hues. Using the same paradigm used by Parry et al. (2006) cone contrasts of 24 hues are calculated for peripheral perceptual matches and for parafoveal chromatic stimuli along with cone contrasts of the four invariant and unique hues.

5.3 Methods

45 male and female observers participated in the study. All were tested for colour vision deficiency using Farnsworth-Munsell 100 Hue test, Ishihara plates (38-plate edition, 1979) and Nagel anomaloscope. In total, 7 observers were excluded, as they were either protanopes or deuteranopes. A total of 38 colour normals (aged 26 ± 8years, mean ±1S.D.) participated in the main asymmetric matching experiment. Three of them also participated in the naming experiment. The colour space employed for this experiment is a modified version of a 2 dimensional MBDKL colour space (Derrington, Krauskopf, & Lennie, 1984) using CIE1931xy coordinates. It is 2 dimensional as the luminance was maintained constant during the experimental procedure. A calibration procedure was carried out before the experiments to ensure that the display presented the colours accurately. Details on the experimental setup and the calibration procedure can be found in Parry et al. (2006) and Chapter 2. Chromatic axis, which is the physical equivalent of hue, is defined as the rotation of a vector (spanning 360◦) that originates from the background illuminant C(x = 0.31, y = 0.316 at 12.5cd/m2) and purity, which is the physical equivalent of saturation, as the length of that vector. If a vector of length 0.0739 equals to purity of 1, then the parafoveal spots are defined as having purity 0.5. The 0◦, 90◦, 180◦ and 270◦ chromatic axes coincide with the cardinal red, blue, green and yellow axes, respectively (Derrington et al., 1984).

114 5.3. METHODS

Figure 5.1: The stimuli conﬁgura- tion

5.3.1 Colour matching

The task for the observers was to match a peripheral 3◦ spot (18◦ eccentricity, nasal visual field) with a parafoveal 1◦ probe spot (1◦ eccentricity, nasal visual field) in hue and saturation (Figure 5.1 depicts the experimental configuration). This asymmetric paradigm is described in detail elsewhere (Parry et al. (2006); McKeefry, Murray, and Parry (2007) and Chapter 2). The observer had full control of the chromaticity of the peripheral spot, within the colour gamut of the display, and used the method of adjustment to match the two spots. Prior to the experiment, about 10 minutes were given to the observer to familiarise him/herself with the equipment and to adapt to the background illuminant C (subtending 37.2◦ × 29.3◦). A chin and forehead rest was used to minimise head movements. The first probe axis presented was the 0◦. The observer changed the chromatic axis and the purity of the peripheral spot until he/she found a satisfactory match with the parafoveal spot. As soon as a match was obtained, the experimenter changed the probe’s chromatic axis by 15◦ and the participant again matched the next probe chromaticity. In one trial, 24 matches were obtained in total. After a break of about 10 minutes, the whole procedure was repeated. Each trial took around 40 minutes.

115 5.3. METHODS

5.3.2 Colour naming

The procedure employed was a 4 alternative forced choice paradigm described by Parry et al. (2006). The observers were presented only with the peripheral 3◦ spot while they were fixating on a cross (the same configuration as in Figure 5.1 but without the parafoveal spot). The spot was presented for 380ms and the task was to name it as red, blue, green or yellow. The chromaticities formed a circle but the step was 9◦ instead of 15◦. In total, 40 different chromaticities were used, all of saturation 0.5. Each colour was presented 20 times and randomly. That means the observer had to name 800 spots in total. For each colour category a naming function was obtained. Each unique hue (ie unique red, unique blue, unique green and unique yellow) was defined as the central maxima of the respective naming function.

5.3.3 Cone contrast

The cone excitations are based on the Smith and Pokorny (1975) cone fundamentals. The cone contrast calculations are based on the weberian formula for contrast. That is

∆L Lcc = (5.3.1) Lb

where ∆L = Ls − Lb and Ls is the L-cone excitation induced by the stimulus and Lb the L-cone excitation because of the background (illuminant C). The same formula is used for M- and S-cone contrast by replacing the L-cone excitations with the M- and S-cone excitations respectively. As the majority of the stimuli, used in this report, do not isolate a single cone class, but stimulate all three cone types one more metric is used in this report. This is the RMS cone contrast (Kaiser & Boynton, 1996) which takes into account all the

116 5.4. RESULTS three cone contrasts and is deﬁned as

r L2 + M 2 + S2 RMS = cc cc cc (5.3.2) cc 3

5.4 Results

Figure 5.2 depicts the results of the asymmetric matching experiment. The curves are an 8 degree Fourier equation (f(x) = a0 + a1cos(x) + b1sin(x) + a2cos(2x) + b2sin(2x) + ··· + a8cos(8x) + b8sin(8x)) fitted on the data from the 38 normal observers who performed the matching paradigm. That type of equation was chosen as it approximates very well the average and gives the highest R2. The upper panel shows the hue rotation at 18◦ eccentricity. There is major hue distortion close to cardinal blue (75◦) and in the greenish-yellow region of the colour space (about 250◦). There are, however, four colour axes which show no hue distortion (hue rotation = 0) in the periphery (empty diamonds on the upper panel of Figure 5.2). That means that they are perceived the same in the parafoveal and peripheral visual field. These chromatic axes are at 2◦ (invariant red), 120◦ (invariant blue), 167◦ (invariant green) and 310◦ (invariant yellow) Parry et al. (2006) call them invariant hues as their hue remains invariant across the visual field. The lower panel shows the saturation that the observers needed in order to match the 0.5 purity of the parafoveal stimuli. There is substantial saturation loss in the bluish-green and green-yellowish region of the colour space with a peak saturation loss at about 210◦ (which is close to unique green determined by 4AFC naming task). The asterisks, on both panels, show the mean unique hues of the 3 observers who performed the naming paradigm. The mean values of the unique hues are 13◦ ± 4.6◦ (unique red), 120◦ ± 3.1◦ (unique blue), 224◦ ± 4.6◦ (unique green) and 290◦ ± 3.5◦ (unique yellow). As shown by other experiments (Chapter 4) unique hues, identified by

117 5.4. RESULTS

Figure 5.2: Colour matching and naming results. The upper panel shows the hue rotation and the lower panel the saturation match of the peripheral spots. The asterisks show the average unique hues for 3 observers. The empty diamonds on the upper panel show the invariant hues. the naming paradigm, remain unchanged with eccentricity and saturation. In accordance with the results of Parry et al. (2006), the unique hues, identified here, correlate well with the invariant hues (note that blue invariant and unique blue are superimposed). There is though an exception in the green area; invariant green and unique green do not correlate very well as also it is described in Parry et al. (2006). It is surprising that three unique hues, identified by the naming paradigm, correlate well with the corresponding invariant hues, identified by the matching paradigm but the green pair does not. Figure 5.3 shows the L- (upper), M- (middle) and S-cone contrast (lower) for the matching experiment. The left hand side panels depict the cone contrast as a function of chromatic axis while the right hand side panels are the correlation between probe and test cone contrast. Note the different scales between each cone type. The probe L-cone contrast is maximised on the cardinal red axis (0◦), it is zeroed at cardinal blue and yellow (90◦ and 270◦ respectively) and it is minimised at the opposite

118 5.4. RESULTS

Figure 5.3: Average L- (upper), M- (middle) and S-cone contrast (lower) of 38 observers. The left hand side panels plot the probe (ﬁlled circles) and test (open circles) cone contrast as a function of chromatic axis. The error bars are ±1S.D. Below each graph the difference between test and probe cone contrast is plotted as a function of chromatic axis. The right hand side panels are the correlation of probe and test cone contrast for each cone type. The solid line is the equity x=y line. 119 5.4. RESULTS axis of cardinal red which is cardinal green (180◦). Exactly the opposite happens for the minimum and maximum of the probe M-cone contrast, as expected, which again is zeroed at cardinals blue and yellow. Probe S-cone contrast is maximised and minimised at cardinals blue and yellow, respectively, and zeroed at cardinals red and green (0◦ and 180◦ respectively). Under each cone contrast graph the difference between probe and test cone contrast is plotted as a function of chromatic axis. As it can be also seen from these plots the observers’ S-cone contrast changes little in order to achieve a match. The cone contrast remains reasonably unchanged for the S-cones as it can be seen from the probe-test cone contrast correlation (lower right hand panel). More signiﬁcant changes occur for the L- and M-cone contrast especially in the green region of the colour space (around cardinal green). The L-cone contrast of the 38 observers is lowered in the green region while M-cone contrast is altered. The opposite change is seen in the red region of the colour space but to a slightly smaller extent. The correlation plots for L- and M-cone contrast show that there is an increase and decrease in cone contrast depending on the region of the colour space. The L- and M-cone contrast varies between parafoveal and peripheral viewing, while it is virtually unchanged for S-cone contrast. However, there are some regions in colour space where there is exact correspondence in cone contrast between probe and test stimuli and this is seen in cases where the data points fall on the x=y line. As it would be interesting to investigate the apparent discrepancy between invariant and unique green, it is necessary to specify the exact cone contrast for invariant and unique hues. Figure 5.4 plots the L-, M- and S-cone contrast for these eight hues (four invariant and four unique hues). Empty diamonds are the invariant hues and asterisks are the unique hues. It can be seen that the cone contrast of the red, blue and yellow pairs does not change with eccentricity. That is, there is no change in cone contrast between the parafoveal and

120 5.4. RESULTS

Figure 5.4: Probe versus test cone contrast for invariant and unique hues. L- (left), M- (middle) and S-cone contrast (right) correlation between the probe and the test stimuli. The empty diamonds are the invariant hues and the asterisks the unique hues. Note that invariant and unique blue are superimposed. Letter G indicates the pair of invariant and unique green that does not ﬁt the x=y line. peripheral stimuli. However, the L- and M-cone contrast changes for invariant and unique green while S-cone contrast (right hand side panel) applies almost perfectly for these two hues. Both invariant and unique green seem to require different amounts of L- and M-cone contrast for peripheral compared with central viewing. As colour vision relies on signal combination from the three cone types and the stimuli used in this study do not isolate only a single cone type further insight might be gained by calculating the RMS cone contrast (according to Equation 5.3.2). Accordingly, Figure 5.5 is presented which plots the probe versus test RMS cone contrast. Panel a shows the probe versus test RMS cone contrast for the 24 chromatic axes used for the matching experiment. It can be seen that the RMS cone contrast is relatively constant for the majority of the chromatic axes. There are some exceptions, especially in the bluish-green region of the colour space (these axes are marked on panel a). Panel b iso- lates the RMS cone contrast for invariant (empty diamonds) and unique hues (asterisks). Next to each symbol there is a letter which indicates whether it belongs to the Red, Blue, Green or Yellow pair of invariant and unique hues. Invariant and unique red, blue and yellow again fall on or very close to the equity line. Interestingly, unique green remains

121 5.5. DISCUSSION

Figure 5.5: Probe versus test RMS cone contrast. a) Probe versus test RMS cone contrast for the 24 chromatic axes. b) Probe versus test RMS cone contrast for invariant and unique hues. Empty diamonds depict the invariant hues and asterisks the unique hues. The letters next to each symbol identify in which pair they belong. The solid lines are the x=y. virtually the same; there is no change in RMS cone contrast between parafoveal and peripheral unique green. But, in the case of invariant green, parafoveal and peripheral RMS cone contrasts are quite different suggesting that it accounts for the discrepancy observed between invariant and unique green. It can be seen from Figure 5.5 that the RMS cone contrast is altered for invariant green even though the perception between parafoveal and peripheral stimuli is the same.

5.5 Discussion

The ﬁndings of this report are two-fold. First, the L-, M- and S-cone contrast results suggest that despite matching, the cone contrast does not remain unchanged for all the three cone types when peripheral retina is involved. Probe S-cone contrast correlates well with the test S-cone contrast while this is not the case for L- and M-cones. For the latter cone types there is an increase and decrease in cone contrast depending on the region of

122 5.5. DISCUSSION the colour space. The second ﬁnding is that RMS cone contrast remains unchanged for peripheral and parafoveal stimuli with only a few axes deviating from the line of equity. These axes lie on the bluish-green region of the colour space (about 130◦ − 180◦). The RMS cone contrast of seven out of eight ‘special’ hues (these are invariant and unique hues) does not change with eccentricity. The only exception is invariant green which belongs to the bluish-green region mentioned above and which is probably responsible for the discrepancy observed between invariant and unique green.

5.5.1 Peripheral L-, M- and S-cone contrast

Although the cone contrast concept and its approaches are controversial, Jordan and Mollon (1997) stated that ‘a colour match requires the standard and the matching fields to lead to the same triplet of quantum catches in the three classes of retinal cone’. This could be interpreted as meaning that the same triplet of cone contrasts produces the same perceptual output (requiring many assumptions and cannot be universally applied). However, the results presented here offer an exception to that rule. When the testing and matching fields are spatially separated on the retina it is not necessary to have the same cone contrast triplet in order to match them perceptually. In other words, despite the fact that the chromaticity of the two spots matches perceptually, the corresponding peripheral L- and M-cone contrast do not match with the parafoveal cone contrast. This may be expected as there is major hue and saturation distortion in the peripheral visual field as seen in Figure 5.2. The question addressed here is whether this applies to all the cone types. In fact, the cone contrast remains unchanged for the S-cones but not for the L- and M-cones. It is known that S-cone density remains relatively stable after about 1◦ retinal eccentricity and they constitute around 7% of the total cone population (Curcio et al., 1991) while L- and M-cone density falls dramatically from fovea to more eccentric retina.

123 5.5. DISCUSSION

The fact that increasing the stimulus size restores peripheral colour perception (Abramov et al., 1991), along with the cone density distribution, suggests that the cone contrast would possibly remain the same only if there are sufﬁcient cones being activated by the stimulus. Increasing the size probably restores some of the hue distortion and saturation loss which would result in better cone contrast match. In the case presented here, there is approximately 26% difference (according to Curcio, Sloan, Kalina, and Hendrickson (1990) in the number of cones activated by the two stimuli. The 1◦ parafoveal spot encir- cles more cones than does the peripheral 3◦ spot. If an increase of the test stimulus would compensate for that difference maybe then the cone contrast between the parafoveal and peripheral stimulus would perfectly match. This means that the cone contrast of itself is not solely responsible for peripheral colour perception. It rather may be linked to the number of cones available to detect the stimulus or the cone sampling by ganglion cells may play a role in the transformation of the signal.

5.5.2 Peripheral RMS cone contrast

If the signal of the three cone classes is combined, according to Equation 5.3.2, in most cases of the 24 chromatic axes the cone contrast does not change, but there are some conspicuous exceptions (see Figure 5.5). The chromatic axes lying between 130◦ − 180◦ exhibit most departure from the x=y line of equity. Note that this effect can be seen weakly in the S-cone contrast data in Figure 5.3 (panel c). Interestingly the range of chromaticities between 130◦ − 180◦ corresponds reasonably well to the region where there is positive hue rotation. In the upper panel of Figure 5.2 there is an area where hue rotation becomes positive while for the majority of the chromatic axes hue rotation is negative. The RMS cone contrast can be analysed in more detail by focusing only on the invariant and unique hues. From Figure 5.5b it is evident that invariant green deviates the

124 5.5. DISCUSSION most from the x=y line. As stated above, previous reports (Parry et al., 2006) have described the fact that, with the exception of green, unique and invariant hues match well. Those papers haven’t established whether the oddity of green was due to the invariant or unique green. This RMS analysis allows us to conclude that as far as RMS cone contrast is concerned unique green is represented in the same way as the other unique hues when comparing parafoveal and peripheral stimuli. In contrast, RMS cone contrast is greater for the peripheral invariant green suggesting that the non-correspondence between invariant and unique green is linked in some way to how green is coded in cone signal. Someone could argue that two factors that should be taken into consideration are the macular pigment and the cone photopigments. Macular pigment is present at the central 8deg while its negligible at the more peripheral retina. Macular pigment absorbs maximally at 460nm and in a lesser extent at 485nm (Snodderly, Brown, Delori, & Auran, 1984). If the presence of the macular pigment at 1◦ eccentricity affected the results then a difference should have been found in the region where it absorbs maximally. This is not the case for the ﬁndings presented here as the colour region, which deviates from the RMS cone contrast, lies between 490nm and 497nm (135◦ − 180◦). As far as the cone photopigments is concerned, their density declines with eccentricity as the cones are getting sparser and their outer segments, where photopigment is located, are getting shorter (Elsner, Burns, & Webb, 1993). A region which should be affected ﬁrst by cone photopigment density difference between the peripheral and parafoveal spots, is the red region of the colour space as L-cones have the highest density from all three cones and are relatively the more numerous either in the central or in the peripheral retina.

125 5.5. DISCUSSION

5.5.3 The oddity of green

The fact that 3 invariant hues correspond to 3 of the categorical hues, red, blue and yellow, and that unique hues remain stable with eccentricity (Chapter 4), suggests that invariant hues could be a manifestation of veridical colour perception but based on the retina (where colour matching is mediated). There is always, of course, the overt discrepancy between invariant and unique green (Parry et al., 2006). As described before, this discrepancy is due to invariant green which is the one ‘special’ hue for which the RMS cone contrast changes dramatically between parafoveal and peripheral viewing. It could be speculated that this is due to reduced number of M-cones in peripheral retina and consequently due to reduced sensitivity in the green region of the colour space. Somebody could argue that this should be the case for unique green, but it should be noted that unique hues are determined using a naming paradigm whose results are dictated by higher cognitive brain loci. As stimulus size restores to some extent colour perception in peripheral retina, it could possible restore the invariant green to its ‘expected’ location, that is close to unique green. However, testing this idea would require large number of observers as invariant hues are highly variable across the population.

5.5.4 Cone versus colour opponency

The results shown here conﬁrm the idea that there are more than two cortical chromatic mechanisms which rotate the LGN cardinal axes to the unique hue axes (Chapter 4, Webster, Miyahara, Malkoc, and Raker (2000), Wuerger, Atkinson, and Cropper (2005), De Valois, De Valois, Switkes, and Mahon (1997)). This transformation surely happens after the LGN otherwise colour perception would coincide with the electrophysiological recordings from the LGN substrate found by Derrington et al. (1984). Where exactly unique hues are encoded remains controversial; reports state that cell clusters, which re-

126 5.5. DISCUSSION spond optimally to unique hues, are found as early as in the primary visual cortex (Parkes, Marsman, Oxley, Goulermas, & Wuerger, 2009) or in other brain centres as in the visual cortex (Abramov & Gordon, 2005; De Valois et al., 1997) or in the posterior inferior cortex of macaques (Stoughton & Conway, 2008). Previous work is based on central colour vision but here the notion is supported by the fact that in peripheral matching the same asymmetries in the rotation of cardinal axes into unique hue axes are observed. This suggests that the coding process that rotates the cardinal axes into veridical colour perception does not change with eccentricity but remains universal across the visual field. In addition to that, the fact that despite perceptual match the cone contrast is changing when the stimuli are viewed peripherally suggests that some sort of signal transformation occurs between the two first stages of the colour pathway; that is between photoreceptors and LGN. Maybe that could be explained by the findings of Calkins (2004) and Tailby, Solomon, and Lennie (2008). Calkins (2004) found that the majority of spectrally opponent LGN cells respond maximally in spatial properties whereas only a small portion of LGN cells show the appropriate spectral properties for colour perception (Neitz & Neitz, 2008). When Tailby et al. (2008) specifically recorded electrophysiologically the responses of this cell minority, found by Calkins (2004), they found that the cells responded optimally not to the known cardinal directions of LGN, but to the perception of veridical colours.

Author contribution

The experiments, the analysis and the writing were made by A. Panorgias. I.J. Mur- ray contributed to correcting the manuscript and helping put the ideas in context. J.J. Kulikowski contributed by discussing the beneﬁts of cone contrast analysis. The experiments were conducted using a software written by N.R.A. Parry. D.J. McKeefry and N.R.A. Parry helped by discussing the ﬁndings

127 5.6. REFERENCES

5.6 References

Abramov, I., & Gordon, J. (1977). Color vision in the peripheral retina. i. spectral sensitivity. J Opt Soc Am, 67(2), 195–202. Abramov, I., & Gordon, J. (2005). Seeing unique hues. J Opt Soc Am A Opt Image Sci Vis, 22(10), 2143–53. Abramov, I., Gordon, J., & Chan, H. (1991). Color appearance in the peripheral retina: effects of stimulus size. J Opt Soc Am A, 8(2), 404–14. Calkins, D. (2004). Linking retinal circuits to color opponency. In L. Chalupa & J. Werner (Eds.), The visual neurosciences. Cambridge, MA: MIT Press. Curcio, C. A., Allen, K. A., Sloan, K. R., Lerea, C. L., Hurley, J. B., Klock, I. B., & Milam, A. H. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J Comp Neurol, 312(4), 610–24. Curcio, C. A., Sloan, K. R., Kalina, R. E., & Hendrickson, A. E. (1990). Human photoreceptor topography. J Comp Neurol, 292(4), 497–523. De Valois, R. L., De Valois, K. K., Switkes, E., & Mahon, L. (1997). Hue scaling of isoluminant and cone-speciﬁc lights. Vision Res, 37(7), 885–97. Derrington, A. M., Krauskopf, J., & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol, 357, 241–65. Elsner, A. E., Burns, S. A., & Webb, R. H. (1993). Mapping cone photopigment optical density. J Opt Soc Am A, 10(1), 52–8. Foster, D. H., & Nascimento, S. M. (1994). Relational colour constancy from invariant cone-excitation ratios. Proc Biol Sci, 257(1349), 115–21. Jordan, G., & Mollon, J. (1997). Adaptation of colour vision to sunlight. Nature, 386, 135–136.

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Kaiser, P. K., & Boynton, R. M. (1996). Human color vision (Second). Washington, DC: Optical Society of America. Land, E. H., & McCann, J. J. (1971). Lightness and retinex theory. J Opt Soc Am, 61(1), 1–11. McKeefry, D. J., Murray, I. J., & Parry, N. R. (2007). Perceived shifts in saturation and hue of chromatic stimuli in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 24(10), 3168–79. Mullen, K. T., & Kingdom, F. A. (2002). Differential distributions of red-green and blue- yellow cone opponency across the visual ﬁeld. Vis Neurosci, 19(1), 109–18. Neitz, J., & Neitz, M. (2008). Colour vision: the wonder of hue. Curr Biol, 18(16), R700– 2. Parkes, L., Marsman, J., Oxley, D., Goulermas, J., & Wuerger, S. (2009). Multivoxel fmri analysis of color tuning in human orimary visual cortex. Journal of Vision, 9, 1–13. Parry, N. R., McKeefry, D. J., & Murray, I. J. (2006). Variant and invariant color perception in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 23(7), 1586– 97. Sakurai, M., & Mullen, K. T. (2006). Cone weights for the two cone-opponent systems in peripheral vision and asymmetries of cone contrast sensitivity. Vision Res, 46(26), 4346–54. Smith, V. C., & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Res, 15(2), 161–71. Smithson, H. E. (2005). Sensory, computational and cognitive components of human colour constancy. Philos Trans R Soc Lond B Biol Sci, 360(1458), 1329–46. Snodderly, D., Brown, P., Delori, F., & Auran, J. (1984). The macular pigment. i. ab- sorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Invest Ophthalmol Vis Sci, 25, 660–673.

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Stabell, B., & Stabell, U. (1976). Rod and cone contribution to peripheral colour vision. Vision Res, 16(10), 1099–104. Stabell, U., & Stabell, B. (1984). Color-vision mechanisms of the extrafoveal retina. Vi- sion Res, 24(12), 1969–75. Stoughton, C. M., & Conway, B. R. (2008). Neural basis for unique hues. Curr Biol, 18(16), R698–9. Tailby, C., Solomon, S. G., & Lennie, P. (2008). Functional asymmetries in visual pathways carrying s-cone signals in macaque. J Neurosci, 28(15), 4078–87. von Kries, J. (1905/1970) In D. MacAdam (Ed.), Handbook of human physiology (En- glish translation). Sources of color science. Cambridge, Mass: MIT Press. Webster, M. A., Miyahara, E., Malkoc, G., & Raker, V. E. (2000). Variations in normal color vision. ii. unique hues. J Opt Soc Am A Opt Image Sci Vis, 17(9), 1545–55. Whittle, P. (2003). Contrast colour. In R. Mausfeld & D. Heyer (Eds.), Colour perception, mind and the physical word. New York: Oxford University Press. Wuerger, S. M., Atkinson, P., & Cropper, S. (2005). The cone inputs to the unique-hue mechanisms. Vision Res, 45(25-26), 3210–23.

130 CHAPTER SIX

PHASES OF DAYLIGHT AND THE STABILITY OF COLOUR PERCEPTION IN PERIPHERAL HUMAN RETINA

Authors: A. Panorgias, J.J. Kulikowski, N.R.A. Parry, D.J. McKeefry & I.J. Murray

6.1 Abstract

N higher primates there are two anatomically distinct visual pathways, one specialised I for blue-yellow and the other for red-green information. The perception of colour mediated by these pathways is known to be distorted in the peripheral visual field. There are, however, four so-called unique hues, ‘each of which shows no perceptual similarity to any of the others’ (Wyszecki & Stiles, 1982), that do not vary across the visual field. On a colour space, daylight can be represented by the daylight locus that extends from ice blue (northern morning sky) to deep orangey red (evening-like sky). In this study we set out to investigate the relationship between the stability of perceived colours across the human retina, unique hues, and the different phases of daylight. 38 colour normal human observers performed an asymmetric colour-matching task in the nasal visual field, where the chromaticity of a parafoveal (1◦ eccentricity) 1◦ diameter probe spot was matched, in

131 6.2. INTRODUCTION terms of hue and saturation, with a peripherally viewed test spot at 18◦ eccentricity. 24 different colours, forming a circle in CIE 1931 xy colour space, were tested. Unique hues were identified using a 4 alternative forced choice (4AFC) naming paradigm in which a coloured spot was identified as only red, blue, green or yellow. The mean of the maxima of the naming functions defined the position of the unique hues in colour space. In the matching task, the observers’ performance was almost perfect in the vicinity of the daylight locus, that is, in the blue and yellow regions of colour space. For regions more remote from the phases of daylight, characteristic distortions in terms of hue and saturation were evident, resulting in the colour circle becoming elongated along the red-green axis. In the additional 4AFC task, the unique blue and yellow were virtually coincident with the daylight locus. The inter-observer variability is also minimised in the vicinity of the daylight locus and is maximised in the red and yellowish-green regions of the colour space. The results suggest that colour perception mediated by the phylogenetically older (blue-yellow) colour pathway has been strongly influenced by the different phases of daylight. It has evolved to be more stable in the near peripheral visual field than the more recent red-green mechanism.

keywords: peripheral retina, colour vision, daylight, colour variability, evolution, unique hues

6.2 Introduction

Colour vision in catarrhines, that is Old World monkeys, apes and humans is based on three different types of photoreceptors having different absorption spectra (Jacobs & Dee- gan, 1999). Each cone photoreceptor express a different photosensitive opsin which accounts for their spectral sensitivity. Depending on the wavelength of their maximum sensitivity (λmax) cones are identiﬁed as Short-wavelength (or S) cones, Middle-wavelength

132 6.2. INTRODUCTION

(or M) cones and Long-wavelength (or L) cones. S-cones have their λmax at about 420nm, M-cones at around 530nm and L-cones at circa 565nm (Bowmaker, 1984; Dartnall, Bow- maker, & Mollon, 1983; Smith & Pokorny, 1975; Schnapf, Kraft, & Baylor, 1987). Note that the difference between the two latter cone types is only about 30nm resulting in a substantial overlap of their sensitivity spectra. Apart from that, the L- and M-cone opsins appear to have 96% genome similarity whilst they have only 43% mutual identity with the S-cones (Nathans, 1987). These cells are the sensory mechanisms for transforming the light information of the outer world into a signal usable from the inner world, that is the brain. After the light information is translated into a cone signal, it is contrasted in different ways to form the three visual pathways, or cone opponent mechanisms (Hering, 1964; Hurvich & Jameson, 1955). There are two chromatic pathways and one achromatic pathway which carry the light information into higher brain centers to process it accordingly. There is the S-(L+M) pathway which is a combination of S-, M- and L-cones and gives rise to the sensation of blue and yellow. There is the L-M pathway which differentiates the L- and M-cone signals to give the perception of red and green. Finally, there is the L+M pathway, which adds the L- and M-cone signals and is responsible for the achromatic luminance information, that is from black to white including the intermediate grey. Most mammals posses the same S-cone photopigment and a second cone class at the long-wavelength side of the spectrum resulting in a blue-yellow channel which is a common feature of mammalian colour vision (Jacobs, Bowmaker, & Mollon, 1981). Thus, the blue-yellow channel can be regarded as phylogenetically more ancient as it is common to all our ancestors (Nathans, Thomas, & Hogness, 1986; Mollon, 1989). There are also some birds, ﬁsh and other mammals having four types of cones that allow them to detect in the ultraviolet region. It is surprising, that among about ﬁve thousands mammals around the globe, only three distinct types, Old World monkeys, apes and humans,

133 6.2. INTRODUCTION have developed trichromatic colour vision, that is carrying only three cone types (Jacobs, 2009). Since the development of the science of colour vision and how it relates to human evolution there has been always the question: Why do catarrhines posses these three and only these three types of cones? Is it serendipitous, is it the results of evolutionary pressures or a natural law? On the other hand, New World monkeys are mostly dichromats, with only two exceptions. The ﬁrst is that the one third of their female population are trichromatic because of X chromosome inactivation (Mollon, Bowmaker, & Jacobs, 1984). The second are the howler monkeys which are routinely trichromats but there are arguments that their trichromacy is not related to their Old World monkeys ancestors (Jacobs, Neitz, & Krogh, 1996). New World monkeys have been evolved together with the Old World monkeys until the separation of South-central america from the African-asian territory (Dominy, Svenning, & Li, 2003). What was the difference in the route of Old World monkeys to develop the well known trichromacy? There is the school saying that this happened because at some point, the genes encoding the cone pigments of a female catarrhine were mutated and resulted in giving not one cone type but two cone types. This mutation is then become progressively dominant, via reproduction and so the catarrhines became trichromats (Ja- cobs & Nathans, 2009). The other school, and probably the most dominant so far, supports the idea that the Old World primates needed at some point to change their gastronomic habits, that is they become frugivores or folivores. As the fruit’s chromaticities occupy a large region in the middle to long wavelength spectrum, these species needed a mechanism capable to discriminate the coloured fruit against the green foliage of the trees. So, their long- wavelength cone was mutated and gave rise to two different cone types, one at the middle and another at the long-wavelength domain of the spectrum locus (Mollon, 1989; Oso- rio & Vorobyev, 1996). In that group there is also the idea that the need for this colour

134 6.2. INTRODUCTION discrimination was not because of the need for fruit but because of the need for tender, nutritionally rich baby leaves which colour is slightly different from the older leaves (Lu- cas et al., 2003). Either way, they support the development of trichromacy at the fact that the catarrhines needed the red-green discrimination surviving from starvation. There is also the school that supports the idea that the sensory mechanisms, and consequently the brain, could not have been evolved in a different way because of the terrestrial illumination (Shepard, 1992). As the earth spins around itself and around a very bright star, that is the sun, the terrestrial illumination follows a speciﬁc pattern since the earth and its atmosphere were created. Because of the air molecules and other microscopic particles in the atmosphere, the short wavelengths of the visible spectrum are scattered (Rayleigh scattering) resulting in the blue sky colour. The remaining direct sunlight is composed only by middle and long wavelengths, which average wavelengths are lying in the yellow region of the colour space. So, the Rayleigh scattering gives a blue-yellow chromatic variation (Shepard, 1992). On the other hand, as the sun is approaching the horizon the sunlight has to penetrate a longer and of greater density column of air resulting on scattering of long wavelengths. Even though the proximity of the horizon is the same at sunrise and sunset, the earth temperature is different. The higher temperature during the sunset results in elevated water molecules in the atmosphere which scatter the long-wavelength component of the sunlight, giving the distinct orangey-red sky during sunset. The remaining sunlight is composed of short and middle wavelengths, which average wavelengths are lying on the green region of the colour space (Shepard, 1992). So, the elevation of the sun and the water’s vapor presence in the atmosphere give a red-green chromatic variation. Also, during a 24 hour circle, there is an overall change in intensity of illumination from the very bright midday to the dark shades of moonlight. This intensity change is said to have provided the luminance variation (Shepard, 1992). Anyone can easily understand that these three variations on terrestrial illumination remind us the

135 6.2. INTRODUCTION three cone-opponent channels first described by Herring’s cone opponent theory (Hering, 1964). In humans and Old World monkeys the genes encoding the M- and L-cone pigments are highly polymorphic (Neitz, Neitz, & Jacobs, 1993; Mollon, 1989). This polymorphism leads to the expression of slightly different M- and L-cone pigments. Thus, among the colour normal population there are at least two M- and two L-cones. This normal variation in the spectra characteristics of the middle and long-wavelength cones can be responsible for the variation in colour vision that is often observed among colour normal human observers. For example, there is said to be great inter-individual variability in the mixture of red and green monochromatic lights in matching a yellow light (Neitz et al., 1993). Central colour perception becomes significantly distorted in the periphery (Parry, Mc- Keefry, & Murray, 2006) and chromatic channels (especially the L-M) are deteriorating (Mullen, Sakurai, & Chu, 2005). There are however some hues that appear no to be affected as a function of retinal eccentricity (Parry et al., 2006). Also, there are the unique hues that, depending on the experimental approach remain relatively stable across the visual field no matter how the chromatic sensitivity declines and the M- and L-cone density drops. In a colour space, there is the daylight locus which describes the phases of daylight (Wyszecki & Stiles, 1982). This locus describes the colour of the early morning sky up to the colour of the sky during sunset. In other words, approximates the colour of the sky during the different phases of daylight. Interestingly, this locus falls close enough to our primordial blue-yellow chromatic channel and divides the colour space into warm, cool and neutral colours (Mollon, 1989). With the present study we are trying to understand how the stability and variation in peripheral colour perception is correlated with the two chromatic systems and in what

136 6.3. METHODS extent, if any, the phases of terrestrial illumination affect it. In other words, we wanted to investigate how the modern and ancient roots of the two chromatic channels along with the daylight phases are manifested in colour matching and colour naming data. These two types of experiments were selected as they are tapping different mechanisms on the visual pathway; colour matching is driven by the ﬁrst and second stage of the visual pathway while colour naming involves higher stages in the brain hierarchy.

6.3 Methods

45 male and female observers took part at the study. Most of them were undergradu- ates from across the university. Their colour vision was tested with Farnsworth-Munsell 100 Hue test, Ishihara plates (38-plate edition, 1979) and Nagel anomaloscope. 7 observers were found to be either protanopes or deuteranopes and were excluded from the study. In the main experiment 38 colour normal observers (aged 26 ± 8 years, mean ±1S.D.) took part.

The equipment used was a CRT monitor (SONY c Trinitron R Multiscan520GS) and a stimuli generator graphic card (ViSaGe, Cambridge Research Systems c Ltd, Rochester, UK) driven by a PC. Prior to the experiments a calibration procedure was carried out, with a PR650 SpectraScan R Colorimeter (Photo Research Inc) and a ColourCal R (Cambridge Research Systems c Ltd, Rochester, UK), to ensure that the stimulus chromaticities were presented correctly. Details for the calibration procedure can be found in Parry et al. (2006). The 38 observers performed an asymmetric colour matching paradigm and 3 of them participated in a colour naming paradigm. The three observers (the author and two col- leagues) who took part at the second experiment performed it on a different day as it is would be time consuming and tiring to do both experiments on a single day.

137 6.3. METHODS

Figure 6.1: The CIE1931 xy colour space. The dots are the probe chromaticities. The dashed line is the daylight locus. Its left end represents the morning sky colour and the far right end the sky colour during sunset. The grey lines depict the cardinal axes. The light grey triangle is the monitor gamut.

The colour space employed in this experiment is a modiﬁed MBDKL colour space using CIE1931 xy coordinates. The rotation of a vector in CIE1931 xy colour space describes chromatic axis and its length purity. The 0◦, 90◦, 180◦ and 270◦ coincide with the cardinal axes described in Derrington, Krauskopf, and Lennie (1984) (see Figure 6.1). Length of that vector equal to 0.0739 is purity of 1. That means that purity of 0.5 results

0.0739 in vector length equal to 2 = 0.03695. The 1◦ spot appears at 1◦ eccentricity and the peripheral 3◦ spot at 18◦ eccentricity. The monitor subtended 37.2◦ × 29.3◦ and the background chromaticity was illuminant C (x=0.31, y=0.316) at 12.5cd/m2.

6.3.1 Matching experiment

The observer, using a remote control could change the chromaticity of the peripheral spot (ie chromatic axis and purity). Prior to the experiment 10 minutes were given to

138 6.4. RESULTS the observers to familiarise themselves with the equipment and adapt at the background illuminant. The observer was presented with the spots for 380ms (in order to avoid chromatic adaptation) and then he/she had to change either the chromatic axis or purity. As soon as the choice was made, the two spots were presenting again and the observer had to make the next choice (ie to change again chromatic axis or purity). This procedure was continued until he/she found that the chromaticity of the two spots is matched. After the match, the chromaticity of the parafoveal spot was changing so as the observer had to ﬁnd the next match. In total, the parafoveal spot was presented in 24 chromaticities, from 0◦ to 360◦ in steps of 15◦ and always at 0.5 purity. After a 10min break the whole experiment was repeated.

6.3.2 Naming experiment

The procedure employed was a 4 alternative forced choice naming paradigm (4AFC) (Parry et al., 2006). The observers were presented only with the peripheral 3◦ spot while they were ﬁxating on a cross. The spot was presented for 380ms and the task was to name it as red, blue, green or yellow. The chromaticities formed a circle but the step was 9◦ instead of 15◦. In total, 40 different chromaticities were used, all of saturation 0.5. Each colour was presented 20 times and randomly. That means the observer had to name 800 spots in total. For each colour category a naming function is obtained. Each unique hue (ie unique red, unique blue, unique green and unique yellow) was deﬁned as the central maxima of the respective naming function (see Figure 6.2).

6.4 Results

Figure 6.3 summarises the results of both the matching and the naming experiment. The open circles, connected with a solid line, represent the averaged matches of the 38

139 6.4. RESULTS

Figure 6.2: Colour naming functions. We deﬁne unique hues as the central maxima of each colour naming function. The arrows show the point of central maximum of each function and respectively the unique hue. observers. We avoided plotting error bars for each data point for clarity and instead shaded the area that represents ±1S.D from the average curve. The four asterisks show the average unique hues for the 3 observers who performed the naming task (see Table 6.1 for individual unique hues).

Table 6.1: Unique hues for 3 observers as deﬁned by the naming paradigm at 18◦

observer unique red unique blue unique green unique yellow HJT 12◦ 123◦ 228◦ 294◦ AP 18◦ 121.5◦ 219◦ 288◦ AD 9◦ 117◦ 225◦ 288◦ Mean 13◦ ± 4.6◦ 120◦ ± 3.1◦ 224◦ ± 4.6◦ 290◦ ± 3.5◦

The unique hues are plotted in slightly higher saturation than 0.5 so as not be superimposed with the probe chromaticities. The asterisk closest to 0◦ axis is unique red, the one closest to 90◦ and the daylight locus is unique blue, the next one between 180◦ and 270◦ is unique green and the one close to 270◦ and the daylight locus is unique yellow. It can be seen from Figure 6.3 that there is a greater saturation loss across the 0◦-180◦ cardinal axis (red-green) whilst it is minimised for the blue and yellow region and even red. Interestingly, unique blue and unique yellow almost coincide with the daylight locus,

140 6.4. RESULTS

Figure 6.3: The average matches of 38 observers. The black dots are the probe chromaticities and the open circles are the corresponding matches. The grey shaded area depicts ±1S.D. from the matches. The dashed curve is the daylight locus and the dark grey lines the cardinal axes. The asterisks are the average unique hues from three observers. which intersects the probe circle at 120◦ and 283◦. As it is difficult in Figure 6.3 to illustrate hue distortion, in Figure 6.4 we plot separately the two chromaticity attributes. The upper panel shows hue distortion as a function of chromatic axis and the lower panel shows the matched saturation as a function of chromatic axis. The black lines are fitted 8th order Fourier functions because they best approximate the mean data and give the best R2. The dotted lines are the 95% confidence bounds of the fitted functions. The asterisks are the unique hues and the dashed lines are the chromatic axes where the daylight locus intersects the circle describing probe chromaticities. By hue distortion we mean how much the observer needs to rotate the hue of the test

141 6.4. RESULTS

Figure 6.4: Hue rotation (upper panel) and saturation match (lower panel) for 38 observers. The black curves are ﬁtted Fourier functions on the data. The dotted curves depict 95% conﬁdence bounds. The dashed lines are the points where the daylight locus intersects the probe circle. The asterisks are the averaged unique hues from 3 observers. spot in order to match its hue to that of the probe. For example, if the probe’s hue is 60◦ the observer rotates the hue of the test spot by−20◦ in order to obtain a match. That means that he/she perceives the 40◦ hue as 60◦ whilst viewing it peripherally. The saturation graph shows the saturation of the test spot required to match that of the parafoveal spot. For example the saturation match for 60◦ is about 0.65. That means that the observer needed to increase saturation of the test spot from 0.5 to 0.65 in order to perceive it as the same as the parafoveal spot. These two examples mean that it is needed to set the hue and saturation of the test spot to 40◦ and 0.65 saturation in order to be perceived as the 60◦ and 0.5 saturation chromaticity. From the upper panel it can be seen that there are two regions of major hue distortion at around 70◦ and 240◦ chromatic axes. From the lower panel it is evident that there are areas where altering the saturation is required (in red-bluish and green-yellowish regions) whilst there are others where there is no need for

142 6.4. RESULTS change (around cardinal blue and yellow-orangey region). Interestingly unique blue and unique yellow fall in areas where there is minimum hue distortion and saturation change. We can see from the upper panel that at the point of unique blue and unique yellow there is virtually no hue distortion. The hues are perceived the same centrally and peripherally. From the lower panel it can be seen that unique yellow falls where there is no need for saturation change while unique blue falls slightly off the minimum saturation change area. From Figure 6.4 it can be concluded that at the areas of unique blue and yellow there is least chromatic distortion in the peripheral visual field, while this is not the case for the areas of unique red and green. Unique red is close to the minimum hue distortion point but needs increased saturation in periphery (see Figures 6.3 and 6.4). Unique green axis is by no means close to either minimum hue distortion point and minimum saturation change. Another common feature of unique blue and unique yellow, apart from the fact that they fall in minimum distortion areas according to the matching task, is that both are almost coincident with the axes where the daylight locus intersects the probe circle. Thus, two interesting regions can be identified in the colour space: one in the blue and one in the yellow region where unique blue, unique yellow, invariant blue and invariant yellow coincide with the daylight locus. In other words, these two regions appear the following 3 characteristics: 1) their chromaticity shows no perceptually similarity to any other colour (Wyszecki & Stiles, 1982) 2) they show no hue distortion and no saturation loss by increasing the retinal eccentricity and 3) they are part of the daylight locus. In order to find out how the inter-subject variability changes around the colour space and the extent to which it is influenced by the phases of daylight, a different approach to the data is employed. For each chromatic axis there are 38 subjects per 2 trials = 76 data points (matching points). For these 76 data points ellipses are fitted using least squares method and an ellipse of the form ax2 + bxy + cy2 + dx + ey + f = 0. The area ( = πa0b0 where a0 is the semi-length of the long major axis and b0 the semi-length of the short

143 6.4. RESULTS

Figure 6.5: Fitted ellipses. The small dots show the matching raw data of 38 observers. Data shown here are for the 0◦, 90◦, 120◦, 210◦ and 285◦ axes. The ellipses are fitted using least squares method. The large dots are the probe chromaticities and the dashed curve the daylight locus. The grey axes are the cardinals major axis) of the fitted ellipse is assumed to be an index of inter-subject variability for that particular axis. The larger the area the more the variability is across observers for a particular axis whilst the smaller the area the least inter-subject variability. Figure 6.5 shows five sets of data points for 0◦, 90◦, 120◦, 210◦ and 285◦ chromatic axes and the best-fitted ellipses around each data set. From Figure 6.5 it can be seen that the elliptical area is smaller for the 285◦ and 90◦ axes whilst it is larger for the 0◦ and 210◦ axes. Normalising the elliptical area to the maximum area found (210◦) Figure 6.6 is obtained. In that graph the normalised elliptical area is plotted as a function of chromatic axes (open circles). The black curve is again a best fitted 8th order Fourier function. It can be seen from the fitted function that the area is minimised around 105◦ and 290◦ chromatic axes and it is getting larger at 210◦ and 0◦ axes. Interestingly, it can be seen that from 0◦ up to 105◦ axis there is a negative correlation with elliptical area. After 120◦ axis there is substantial increase in

144 6.5. DISCUSSION

Figure 6.6: The elliptical area as a function of chromatic axis. The open circles is the normalised elliptical area. The black curve is ﬁtted on the data. The dashed lines are the daylight locus intersec- tions with the probe circle. The asterisks represent the four unique hues. the area which remains stable up to 240◦ axis. A decrease in the area is following until about 290◦ and then it is increasing to reach again the area of the 0◦ axis. In general, we can say that the inter-subject variability is minimised around the daylight locus while is maximised in the red and green area of the colour space. Especially for the yellow region it can be concluded again that there is a point with a four-fold characteristic, that is 1) unique yellow, 2) invariant yellow, 3) daylight locus point and 4) minimum inter-subject variability.

6.5 Discussion

The data presented in this report point to three main observations . The ﬁrst is that two out of four invariant hues, measured by an asymmetric colour matching paradigm, coincide with the daylight locus. These are the invariant blue and yellow. The second point is that, two out of the four unique hues, speciﬁed by a 4AFC naming paradigm coincide again with the daylight locus. These are unique blue and yellow. The third point is that the inter-subject variability in colour matching performance is minimised around the daylight locus and is maximised in the green region of the colour space and to a lesser

145 6.5. DISCUSSION extent in the cardinal red region of the colour space.

6.5.1 Invariant blue and yellow

Across the visual field there are four hues that remain virtually unchanged as a function of eccentricity (Parry et al., 2006; McKeefry, Murray, & Parry, 2007). Each one of the four invariant hues correspond to one of the red, blue, green and yellow regions of the colour space. It is generally accepted that matching tasks are undertaken by sensory mechanisms as early as in the retina and the cone-opponent stage (Foster & Nascimento, 1994). Thus, it is expected that these four invariant hues are attributed to the first or/and the second stage of colour vision. It is shown in this report that invariant blue and invariant yellow, based on 38 colour normal observers, fall exactly on the axes of the daylight locus. This is compelling evidence that colour matching is strongly influenced by the phases of daylight and that, close to terrestrial illumination, it remains stable across the visual field. In other regions of colour space chromaticity is strongly distorted as eccentricity is increased.

6.5.2 Unique blue and yellow

In general, there is large inter-observer variability in the settings of unique hues. Web- ster, Miyahara, Malkoc, and Raker (2000) measured unique hues for 51 colour normal observers and found that unique red is clustered around the cardinal L-M axis at the end of the red component, the mean unique blue for his observers is at 477nm, unique green at 545nm and unique yellow at 574nm. The range for unique blue is 21nm, for unique green is about 70nm and for unique yellow is 10nm while unique red was found to show least variation . From the data presented here, (see Table 6.1), the unique hues can be expressed in terms of dominant wavelengths. For the three observers who participated in

146 6.5. DISCUSSION the naming task the mean unique blue is 482 ± 1nm, unique green is 525 ± 7nm, unique yellow is 578 ± 2nm and unique red is closer to the cardinal red axis than any other pair of unique hues and cardinal axes. Comparing these two studies (but comparable also with Wuerger, Atkinson, and Cropper (2005) and Kuehni (2004)) it can be concluded that the unique hues reported here are within the normal range of unique hues. Webster’s mean unique blue, in terms of the chromatic axes employed in this study is 111◦ and unique yellow is 283◦. It can be seen that even for a bigger population, mean unique blue and yellow fall, if not exactly, very close to the daylight locus (which is at 120◦ at the blue end of the daylight locus and 283◦ at the yellow end for the saturation used in this report). One could argue that the method employed to measure unique hues is actually measuring focal colours. The latter are the ‘best examples’ of a colour category (Berlin & Kay, 1969) while the former are the hues that can not be reconstructed with a combination of any other two hues. Miyahara (2003) showed that focal colours and unique hue judgements are virtually identical, occupying the same regions in a colour space. There has been much discussion regarding the possibility of a cortical location for the coding of the unique hues (Abramov & Gordon, 2005; De Valois, De Valois, Switkes, & Mahon, 1997). The primary visual cortex (Parkes, Marsman, Oxley, Goulermas, & Wuerger, 2009) and the posterior-inferior temporal cortex (Stoughton & Conway, 2008) have been suggested (but see also Neitz and Neitz (2008); Mollon (2009) and Conway and Stoughton (2009)). The identification of unique hues almost certainly involves higher order brain loci rather than the first and second stage in the visual pathway. There are, however, other reports stating that there are no specific cells to account for unique hue perception and that they may arise from experience and be internalised by the mix of illuminants to which individuals are exposed in their everyday environment (Mollon, 2006). New terminology was introduced recently to describe the skylight and sunlight chromaticities (ie ‘caerulean line’ adopted by Mollon (2006) and Mollon and Lee (2008). This line

147 6.5. DISCUSSION

Figure 6.7: Unique hues on the MacLeod-Boynton cone space. The thick line is the daylight locus between 4000K and 25000K. The dotted line is the ‘caerulean line’ introduced by Mollon (2006) and Mollon and Lee (2008) connecting the 576nm (unique yellow) with the 476nm (unique blue). The asterisks are the average unique hues from the three observers. The empty star is illuminant C.

(which connects the spectral 476nm (unique yellow) with the spectral 576nm (unique blue)) almost coincides with the daylight locus (see Wyszecki and Stiles (1982) p:6) for colour temperatures between 4000K and 25000K (the recommended colour temperatures for the daylight phases by CIE) . Figure 6.7 plots in the physiological MacLeod-Boynton cone space the daylight locus, the ‘caerulean line’ and the unique hues measured by the non-spectral chromaticities with the 4AFC paradigm. Notice that unique blue and unique yellow (measured with non spectral colours on a computer screen) are located, almost exactly, on the daylight locus (and the ‘caerulean line’) that describes the physical properties of these illuminants. It seems that the visual system is not affected by whether a light is multispectral, monochromatic or if it is generated on a simulated environment (screen) or in real physical space. From the above we can speculate that the two perceptual categorical hues, blue and yellow, are based around terrestrial illumination, but this does not necessarily rule out some cor-

148 6.5. DISCUSSION tically located trigger features to account for that inﬂuence, as Conway and Stoughton (2009) explicitly state.

6.5.3 Inter-observer variability

The ellipses described in Figure 6.5 should not be confused with the MacAdam ellipses (MacAdam, 1942) or the work of Wyszecki and Fielder (1971) and Nagy, Eskew, and Boynton (1987) which are discrimination ellipses. The ellipses of Figure 6.5 are variability ellipses, that is they describe the population variability in a peripheral asymmetric matching task. In other words they describe a locus in colour space which is perceived the same as the corresponding parafoveal chromaticity by 38 colour normal observers. The group of 38 observers examined in the current report shows a large inter-observer variability in the green region and less variability in the red. Interestingly the inter- observer variability is minimised again when the probe samples are relatively close to the daylight locus. So, terrestrial illumination can be regarded as linked to this phenomenon for two reasons. The ﬁrst is that L- and M-cones are highly polymorphic. Neitz and Ja- cobs (1990), Neitz, Neitz, and Jacobs (1991) and Neitz et al. (1993) found that colour normal observers need different amounts of monochromatic red and green lights to produce the same yellow light. Their genetic studies showed that an amino acid substitution in the photopigment opsin could produce a spectral shift of 5-7nm in both L- and M-cones. This spectral variation is used to explain ‘a larger minimum color vision difference between color-normal individuals’ as Neitz et al. (1993) state. That spectral shift could explain the inter-observer variability shown here. The chromatic cone-opponent L-M channel combines the signals of the two variable L- and M-cones and the areas with maximum L-M cone opponent activity are those where the larger inter-observer variability is found. Interestingly, the same highly variable L- and M-cones are combined to form the unique

149 6.5. DISCUSSION yellow, that is at 578nm (or 285◦), but the inter-observer variability is minimised at that point. The minimum inter-observer variability in the unique yellow loci could probably be explained with a neural normalisation routine that weights the L- and M-cone signals differently for each observer in order to obtain the unique yellow which is part of the daylight locus (Neitz, Carroll, Yamauchi, Neitz, & Williams, 2002). The same observation is proposed to explain the fact that despite the highly variable L to M ratio in the colour normal population, from 0.6 to 12 (Carroll, McMahon, Neitz, & Neitz, 2000; Kremers et al., 2000), colour perception, particularly of yellow, remains relatively constant. The colour matching ellipses presented here, as stated above , should be attributed to the ﬁrst and/or second stage of the visual pathway which could lead to the proposition that not only higher order mechanisms (Neitz et al., 2002) are normalised to give the perception of standard/ unique yellow but also the lower order mechanisms are subject to some form of normalisation process. A second line of reasoning is that there is better colour discrimination along the daylight locus. Looking carefully at the MacAdam ellipses (MacAdam, 1942) or at the more recent colour-matching ellipses described by Wyszecki and Fielder (1971) it is evident that the elliptical area (which quantiﬁes the discrimination in that case) is highly variable but it is reduced in the regions close to the daylight locus. Discrimination thresholds were measured around the categorical blue and yellow by Danilova and Mollon (2010) and they found that discrimination is again better along the daylight locus for non saturated non-spectral colours. It is surely no coincidence that better discrimination, unique hues, invariant hues and less variability in colour matching are observed in the vicinity of the daylight locus. It is known that macular pigment optical density and cone photopigment density varies a lot between colour normal observers (Webster & MacLeod, 1988). Thus, somebody would expect greater variability in the region where macular pigment absorbs maximally

150 6.5. DISCUSSION

(around 460nm and 485nm) (Snodderly, Brown, Delori, & Auran, 1984) and around the red region of the colour space as L-cones are the more numerous and thus the L-cone photopigment would present the highest variability (Elsner, Burns, & Webb, 1993). But, the maximum variability found here is at about 510nm (green region of colour space). This result conﬁrms that neither macular pigment nor cone photopigment density have a major impact on the results of the asymmetric matching paradigm.

6.5.4 Conclusions

In this report two different tasks have been used. The asymmetric colour matching which is due to the first and/or second stage of colour vision and the naming task which involves higher brain loci as it requires more complex identification skills. The results of both tasks show that two invariant and two unique hues are strongly influenced/driven by the phases of daylight. But why do only three distinct primate groups (Old World monkeys, apes and humans) exhibit that influence by developing trichromatic colour vision? Why do other organisms not show the very specific three-dimensional colour vision seen in these species? The answer should lie not only on one or another theory, but should be a combination of the theories on the origin of trichromatic colour vision. Old World monkeys, apes and humans probably needed to evolve their colour vision because of nu- tritional needs but the evolution of their cones must have been strongly influenced by terrestrial lighting.

Author contribution

The experiments, the analysis and the writing of this chapter/paper were made by A. Panorgias. I.J. Murray contributed to correcting the manuscript. A. Panorgias ﬁrst noticed that inter-individual variability is minimized around the phases of daylight and J.J.

151 6.5. DISCUSSION

Kulikowski noticed that two unique hues fall close to the daylight locus. The experiments were conducted using a software written by N.R.A. Parry. All the four co-authors helped by discussing the ﬁndings

152 6.6. REFERENCES

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157 CHAPTER SEVEN

SEX-RELATED DIFFERENCES IN PERIPHERAL HUMAN COLOUR VISION; A COLOUR MATCHING STUDY

Authors: A. Panorgias, N.R.A. Parry, D.J. McKeefry & I.J. Murray

7.1 Abstract

T is well established that there are genetic differences in cone pigments between males I and females. However, there is much controversy as to whether these are reﬂected in the colour perception. Many studies have examined this question by testing central colour vision either with colour vision tests or psychophysical experiments but none have investigated whether there are sex-related differences in peripheral colour vision. In this study, 19 male (aged 29 ± 10years; mean ± S.D.) and 19 female (aged 24 ± 6 years) observers were tested . All the 38 observers had normal colour vision according to the 100 Hue Farnsworth-Munsell test, the Ishihara plates (38-plate edition, 1979) and the Nagel Anomaloscope . They performed an asymmetric colour-matching paradigm, in which a 1◦ probe (at 1◦ eccentricity) and a 3◦ test spot (at 18◦ eccentricity) were presented simultaneously, in the nasal visual ﬁeld, for 380ms. The chromatic axis of the probe was changed

158 7.2. INTRODUCTION in 24 directions in CIE 1931 xy colour space, in 15◦ steps. All stimuli had the same starting purity in terms of vector length, so that they formed a circle in CIE colour space. The white point (purity = 0) was illuminant C at 12.5cd/m2 (x=0.31, y=0.316). The observers matched the test spot with the probe, for hue and saturation. All subjects demonstrated the chromatic axis-dependent distortion in hue that we have previously reported (Parry, McK- eefry, & Murray, 2006) but there was no significant sex-related difference. A statistically significant male-female difference was found in saturation match in the green-yellow region of the colour space between 520nm and 550nm (p<0.001, independent sample t-test) with females showing less saturation loss in peripheral retina. No statistically significant difference for saturation was found between the two groups in other regions of colour space. The two groups showed no different post-receptoral cone opponent activity on both red-green and blue-yellow chromatic channels. Possible explanations, based on genetics, pre-receptoral filters and psychological differences, are discussed.

keywords: sex differences, colour vision, peripheral retina, polymorphism

7.2 Introduction

Sex-related differences have always been controversial not only in colour vision but also in other aspects of visual function. Even though men are believed to have better spatial abilities, Silverman and Eals (1992) present evidence to the contrary. But again, it is not clear if the superiority of their female observers in spatial cognitive tests is due to a physiological difference or to superior memory for example. Almost the same ambiguity applies in sex-related differences in colour vision. The results so far are inconsistent and there is great deal of speculation in their interpretation. From the 19th century much effort

159 7.2. INTRODUCTION has been made to prove that females have superior colour vision than males or vice versa. If somebody will follow the literature of all these years at the end he/she will be more ‘puzzled’ regarding gender colour vision abilities. But why should we expect any differences between colour normal males and females in the population? From a psychological point of view it is believed that there are cul- tural differences between the two genders. Females for example are more interested on selecting colourful objects (like clothes and facial pigments) and therefore use an ex- tended colour vocabulary when compared with that used by males. This ability is spread across languages and cultures (Thomas, Curtis, & Bolton, 1978) and could be attributed to the fact that females follow different patterns of socialisation (Bimler, Kirkland, & Jameson, 2003). From a physiological point of view there are differences between males and females at least at the first stage of the chromatic process: the photoreceptors. Colour vision deficiencies are sex-linked inherited conditions from mothers to sons. The gene encoding the pigment of the S-cones is located on chromosome 7 while the genes encoding the pigments of L- and M-cones are located on the sex-linked X-chromosome (Nathans, Thomas, & Hogness, 1986). Genetic mutations in the gene code of the photopigments of L- and M-cones cause colour vision deficiencies, from mild to complete absence of a cone type. Males carry an X- and a Y-chromosome while females possess two X-chromosomes. That difference is responsible for the high prevalence of colour vision defects in the male population. If the genes in the male X-chromosome are different from the normal, then this results in the expression of colour vision deficiency, in other words his genotype will match his phenotype. If a female inherited a normal X-chromosome and a deficient X-chromosome from her parents, then she becomes a carrier for a colour vision defect with a chance of 50% passing this defect to her sons. The female has only the genotype and not the phenotype of the defect because of the random X-chromosome inactivation or Lyonization (Lyon, 1972). That is, while still in an embryonic stage, the normal X-

160 7.2. INTRODUCTION chromosome is expressed in some cells and silenced in others and the same happens with the abnormal X-chromosome. The result is that some photoreceptors in the female retina will express the normal photopigment while others will express the abnormal one. These females are called heterozygous as they have two different cones of the same type in their retina. Women who carry only a single version of a cone type are referred to as homozygous. The above procedure can happen for either L- or M-cones. Consequently, the heterozygous females posses four types of cones. Let’s say that a female is a carrier for protanomaly. Then she possesses one normal S-cone, one normal M-cone, one normal L-cone and one abnormal L-cone which has different peak sensitivity from the normal. Thus in her retina there are four different photopigments and that is why they are called tetrachromats. Whether these tetrachromats have three or more colour dimension is controversial. It has been argued that the forth photopigment may give them superior colour vision compared with males (Jordan & Mollon, 1993; Jameson, Highnote, & Wasserman, 2001). Another physiological aspect that may play a role in gender related differences is the prevalence of L- and M-cone polymorphism. The genes encoding the photosensitive opsins in these two cones are polymorphic because of the presence of a different amino acid at the 180 site of the gene sequence (Neitz & Jacobs, 1986; Neitz, Neitz, & Jacobs, 1993). The two amino acids that can be alternatively present on the above site are alanine and serine. Thus both L- and M-cones can be expressed with either alanine or serine in their photopigment opsin. The prevalence of cone polymorphism in colour normal populations is 56.3% for serine L-cones, 43.7% alanine L-cones, 94% alanine M-cones and 6% serine M-cones (Sharpe, Stockman, Jagle, & Nathans, 1999). These substitutions result in difference in the spectral peak sensitivities of the two cones. The difference between alanine and serine L-cones are 3.0nm and the difference between alanine and serine M-cones is more ambiguous and ranges from 3.0nm to 6.0nm depending the

161 7.2. INTRODUCTION method used to measure their spectra (Sharpe et al., 1999). Both serine L- and M-cones have their spectral sensitivity peaks at longer wavelengths than the alanine alternatives. This spectral difference may result in spectral sensitivity difference between observers with different opsins expressed in their retinae. Neitz and Jacobs (1986) showed that the polymorphism of the L-cones affects the red-green ratio required for Rayleigh matches and that also there is a bimodality of the red-green Rayleigh matches for male colour normal population, attributing it to the two different polymorphic L-cones. Others were not able to demonstrate that bimodality (Jordan & Mollon, 1993). While in the male colour normal population the prevalence of serine/alanine L-cones is as described above, in female populations, because of two X-chromosomes, the prevalence in serine/alanine L-cones is different. 50% of females posses both L-cone types in their retina while the other 50%, almost equally divided, have either serine or alanine L-cone (Neitz, Kraft, & Neitz, 1998). As mentioned before, many studies have been conducted to investigate whether there is a gender related difference in colour vision. In cognitive colour lexicon studies it was found that females have a larger word repertoire and use more elaborate terms to describe colours (Nowaczyk, 1982; Simpson & Tarrant, 1991). Hurlbert and Ling (2007) found a signiﬁcant difference in colour preference between the two genders with females showing more preference to the red end of the L-M cone-opponent axis while males showed more weighting to the green end of the same axis. They attribute their ﬁndings to the evolution of the male-female society; that is, females were the gatherers in a hunter-gatherer society and needed better discrimination to pick up reddish fruits against a green foliage (Hurlbert & Ling, 2007). Hood, Mollon, Purves, and Jordan (2006) offers an interesting historical insight for hue discrimination and sensitivity experiments from 1884 to more recently 1962. In a study of Nichols (1884) males were found to have better hue discrimination in red and

162 7.2. INTRODUCTION yellow colours, according to Hood et al. (2006), while females were found to perform better than males in ordering pigments according to their saturation (Nichols, 1884). Hennon (1910) found females to have better hue discrimination in the red and orange region while Pickford (1951) concluded that male colour vision is the same as that of the females (Hood et al., 2006). Verriest, Vandevyvere, and Vanderdonck (1962), found no difference in Farnsworth-Munsell 100-Hue test scores between males and females of all ages but they found an age effect in hue discrimination; young females performed better in the test from males in the same age group (Hood et al., 2006). In more recent studies the results are still inconsistent. Birch, Young, and David (1991) showed that females have a wider matching range in Rayleigh matches than men meaning poorer discrimination. Jordan and Mollon (1993) showed that colour normal female carriers of colour deficiency showed again wide matching range in Nagel anomaloscope. Kuehni (2001) in a unique hue experiment found that there is a difference in mean unique hue settings between males and females and that females show a wider range than males in all unique hues except yellow. In another report it was shown that females who posses more than three pigments in their retina (tetrachromats) perceive more chromatic bands in the range of 380nm to 780nm than normal male and female trichromats (Jame- son et al., 2001). Bimler et al. (2003) found that the only gender related difference in colour vision is that males pay more attention to luminance changes while females put more emphasis on the green-yellow axis. Hood et al. (2006) argues that if any colour deficient observers and female carriers are excluded from the population then no differences along the red/green axis is observed between the two groups. On the other hand, Pardo, Perez, and Suero (2007) found significant sex-related differences in a modified Rayleigh matching procedure with females requiring more red light in order to obtain a match between a test field, composed by red and green light, and a reference orange field. In the most recent study on this topic, Rodriguez-Carmona, Sharpe, Harlow, and Barbur (2008)

163 7.3. METHODS using a colour vision test showed that there is substantial difference between genders in red-green chromatic sensitivity with males being more sensitive than females. But they argue that this difference is because of the presence of female carriers in their population. By excluding them the difference in sensitivity thresholds reduces and it almost becomes non signiﬁcant. As it can be understood from the above, there is no clear evidence for neither sex- related difference nor for no sex-related difference in colour vision. Thus, the question still remains open for further investigation. All the studies mentioned relied on central colour vision using either spectral or metameric lights. It may be that any male-female differences may be exaggerated as the number of L- and M-cones is reduced. Parry et al. (2006) using an asymmetric matching paradigm showed that matching two coloured spots, one parafoveally and the other eccentrically, could show how colour perception deteriorates with eccentricity and other factors (i.e. size). Also, McKeefry, Murray, and Parry (2007), using the same paradigm showed that the post-receptoral cone-opponent channels, especially the red-green, deteriorate again with eccentricity. As there are no peripheral sex-related colour vision studies so far, the rationale behind the present study is to investigate whether there is any difference in deterioration of peripheral colour perception between males and females.

7.3 Methods

45 male and female observers participated in the study. All were tested for colour vision deﬁciency using Farnsworth-Munsell 100 Hue test, Ishihara plates (38-plate edition, 1979) and Nagel anomaloscope. The participants performed the 100 Hue test twice, read the ﬁrst 24 Ishihara plates once and did 10 matches with the anomaloscope using the test (right) eye only. Subjects who exhibited Farnsworth-Munsell error scores greater

164 7.3. METHODS than 50 (after the second trial) or more than 4 errors in Ishihara plates or made abnormal matches on the anomaloscope were excluded from the main experiment. In total, 7 observers were excluded, as they were either protanopes or deuteranopes. A total of 19 male (29 ± 10years; mean ± 1S.D.) and 19 female (24 ± 6years) colour normals participated in the main asymmetric matching experiment. The task for the observers was to match a peripheral 3◦ spot (18◦ eccentricity, nasal visual field) with a parafoveal 1◦ probe spot (1◦ eccentricity, nasal visual field) in hue and saturation. This asymmetric paradigm is described in detail elsewhere (Parry et al., 2006; McKeefry et al., 2007). The colour space employed for this experiment is a modified version of a 2 dimensional MBDKL colour space (Derrington, Krauskopf, & Lennie, 1984) using CIE1931xy coordinates. It is 2 dimensional as the luminance was maintained constant during the experimental procedure. A calibration procedure was carried out before the experiments to ensure that the display presented the colours accurately. Details on the experimental setup and the calibration procedure can be found in Parry et al. (2006). The CIE1931 xy chromaticity coordinates of the chromatic axes used for this experiment are given in Table 7.1. The 0◦, 90◦, 180◦ and 270◦ axes coincide with the cardinal red, blue, green and yellow axes, respectively (Derrington et al., 1984). Chromatic axis, which is the physical equivalent of hue, is defined as the rotation of a vector (spanning 360◦) that originates from the background illuminant C (x=0.31, y=0.316 at 12.5cd/m2) and purity, which is the physical equivalent of saturation, as the length of that vector. If a vector of length 0.0739 equals to purity of 1, then the parafoveal spots are defined as having purity 0.5. The observer had full control of the chromaticity of the peripheral spot, within the colour gamut of the display, and used the method of adjustment to match the two spots. Prior to the experiment, about 10 minutes were given to the observer to familiarise him/herself with the equipment and to adapt to the background illuminant C (subtending 37.2◦ × 29.3◦).

165 7.4. RESULTS

Table 7.1: CIE1931 xy probe chromaticity coordinates.

axis x y axis x y 0◦ 0.346 0.299 195◦ 0.280 0.341 15◦ 0.340 0.291 210◦ 0.287 0.348 30◦ 0.333 0.284 225◦ 0.296 0.353 45◦ 0.324 0.279 240◦ 0.306 0.355 60◦ 0.314 0.277 255◦ 0.317 0.355 75◦ 0.303 0.277 270◦ 0.327 0.352 90◦ 0.293 0.280 285◦ 0.335 0.346 105◦ 0.285 0.286 300◦ 0.342 0.339 120◦ 0.278 0.293 315◦ 0.347 0.330 135◦ 0.273 0.302 330◦ 0.349 0.320 150◦ 0.271 0.312 345◦ 0.349 0.309 165◦ 0.271 0.323 360◦ 0.346 0.299 180◦ 0.274 0.333

A chin and forehead rest was used to minimize head movements. The ﬁrst probe axis presented was the 0◦ axis. The observer had to change the chromatic axis and the purity of the peripheral spot until he/she found a satisfactory match with the parafoveal spot. As soon as he/she had a match between the two spots, the experimenter changed the probe’s chromatic axis by 15◦ and the participant again matched the probe chromaticity. In one trial, 24 matches were obtained in total. After a break of about 10 minutes, the whole procedure was repeated.

7.4 Results

Figure 7.1 shows the results of the asymmetric task. In this ﬁgure the average of 19 males (left hand panel) and 19 females (right hand panel) are shown. The black dots are the probe chromaticities and the open symbols (squares for males and circles for females) are the matches. The dark grey curves depict ±1S.D. and the light grey lines are the

166 7.4. RESULTS cardinal axes.

Figure 7.1: Male (left) and female (right) matches in CIE1931 xy colour space. The black spots are the probe chromaticities and the open symbols (square for males and circles for females) are the averaged matched chromaticities. The dark grey curves and the grey shaded areas are ±1S.D. The light grey lines are the cardinal axes. The open star is the background illuminant C.

Note that both groups show a saturation loss mainly along the 0◦ - 180◦ axis. It should be clariﬁed that when an observer matches the peripheral spot using a higher saturation this is effectively compensating for a saturation loss. Matching for example the probe and the peripheral spot in 0.5 and 1 saturation, respectively, means that the observer needs to double the saturation of the peripheral spot so as to perceive the two spots the same. From Figure 7.1 it is obvious that there is substantial inter-individual variability. Males exhibit a greater range of matches than the females, especially in the green-yellow region of the colour space. It would be interesting to see if there is any difference in either the hue or the saturation or on both chromatic attributes between the two groups. For that reason, the two attributes are considered separately in Figures 7.2 and 7.3.

167 7.4. RESULTS

7.4.1 Hue rotation difference

Figure 7.2 shows the rotation results for the two groups (left hand panel for males (a) and right hand panel for females (b)). The black lines with the open symbols are best-ﬁtted Fourier functions. That is a series of cosines and sines. For hue rotation an 8th degree

Fourier function is used, described by f(x) = a0 + a1cos(x) + b1sin(x) + a2cos(2x) + b2sin(2x) + ··· + a8cos(8x) + b8sin(8x). That type of equation was used because it better approximates the mean data and gives the best R2. Also, as the data move around a circle it is reasonable to use a sum of sines and cosines. For the number of data points (N=950) the R2 = 0.696 (males) and R2 = 0.725 (females) are high, revealing a high level of association (p<0.0001 for both graphs) . Both groups show the same pattern of hue rotation. For some hues there is greater rotation than others (especially around the 90◦ and 270◦ cardinal axes) while for other hues there is no hue distortion (rotation = 0). This means that the observers do not need to change the hue of the peripheral spot to match it with the probe spot. These are what Parry et al. (2006) called invariant hues. Again, males have a slightly greater inter-individual variability compared with the females, according to the confidence bounds. As it is not possible to compare these two graphs by eye, the following statistical analysis was conducted. Hue, by its definition, is a vector rotating around a white point. The difficulty here is that hue has to be treated as circular data and no conventional statistical tests should be applied on it. To perform a parametric test on linear data, these data should be drawn from a normal distribution, thus they should be tested for normality. The equivalent of normality for circular data is that these should be drawn from a von Mises distribution which is described by mean angle θ and a concentration parameter k, analogous to mean and variance of a normal distribution. The hue rotation data shown on Figure 7.2 were tested for ‘circular normality’ and they are found not to be drawn from the von Mises distribu-

168 7.4. RESULTS

Figure 7.2: Hue rotation for male (left) and female (right) observers. The graphs depict the hue rotation that both groups exhibited as a function of chromatic axis. The dashed lines are the 95% confidence bounds of the fitted functions. The small black data points are the raw data for all the observers tion. That means that parametric tests should not be applied on them. The non-parametric test used here is the Wilcoxon-Mann-Whitney rank sum test (Batschelet, 1981). This test showed no statistically significant difference in the hue rotation between the two groups in any chromatic axis. The statistical p value ranges between 0.175 and 0.965 (a=0.05) for the 24 chromatic axes.

7.4.2 Saturation difference

Figure 7.3 depicts the results for saturation only. As previously, the two upper panels are the male (left, a) and female (right, b) saturation matches as a function of chromatic axes. The lower panel (c) shows the differences in saturation match between the two groups as a function of chromatic axis. For both groups there is again substantial inter- individual variability, with that of males being slightly higher. Both groups show the same pattern of saturation match to different extents. For both males and females there is greater saturation loss in the green region with males exhibiting higher loss. Females show a slightly greater saturation loss in the red region of the colour space. The same ﬁtting

169 7.4. RESULTS function, as in hue graphs, is used for saturation giving R2 = 0.196 and R2 = 0.161 for males and females respectively (p<0.0001 for both graphs).

Figure 7.3: Saturation match for male and female observers. The graphs depict the matched saturation that both groups exhibited as a function of chromatic axis (males are on the upper left hand side panel (a) and females on the upper right hand side panel (b)). The dashed lines are the 95% confidence bounds of the fitted function. The small black data points are the raw data for all the observers. Panel c (lower panel) depicts the differences between panel a and b as a function of chromatic axis (see text for details). The black line is the mean of the differences and the dashed lines are the mean ±1.96S.D. The arrow shows the area where there is a statistically significant difference between males and females in saturation match.

In this analysis there is no reason to establish a difference between different axes, ie between the 180◦ axis of males and the 210◦ axis of females. The saturation, also, is an axial chromatic attribute and not a circular. So, compared with the hue data, a different approach can be followed.

170 7.4. RESULTS

An analysis of variance (ANOVA) is performed to investigate whether there are any statistically significant differences between the two groups. This analysis shows that there is statistically significant difference for axes 210◦, 225◦ and 240◦ (p=0.04, 0.02 and 0.006 respectively with post hoc power being between 62%-83%). No statistically significant difference is found for the rest of the axes (0.09

171 7.4. RESULTS

7.4.3 Chromatic channel difference

It would be interesting to see how hue rotation and saturation match are represented in the L-M and S-(L+M) chromatic cone-opponent channels because the results could rule out or not any post-receptoral effects. For both groups the L-M and S-(L+M) activation units were calculated using the cone-opponent model described by Stanikunas, Vaitkevicius, Kulikowski, Murray, and Daugirdiene (2005).

Figure 7.4: L-M activation for male and female observers. The upper left hand and right hand side panel depict the L-M channel activation for males and females respectively, as a function of chromatic axis. The dashed lines are the 95% conﬁdence bounds of the ﬁtted functions. The small black data points are the raw data for all the observers. Panel c (lower) depicts the differences between the two upper panels as a function of chromatic axis. The black line is the mean of the differences and the dashed lines are the mean ± 1.96S.D.

Figure 7.4 shows the L-M channel activation as a function of chromatic axis for both males (upper left hand side panel) and females (upper right hand side panel). The inter-

172 7.4. RESULTS subject variability is now reduced for both groups. A simple function of the form f(x) =

2 a0sin(x + a1) is now used and high R values are obtained for the number of data point used (p<0.0001). From these two panels again it is difficult to judge whether there is a gender difference in the L-M channel activation. As the channel activation values are actually the projections of a rotating vector on the cone-opponent axes (these are the L-M and the S-(L+M) axes) and not values expressed in degrees, the same analysis as in the saturation results can be employed. Panel c in Figure 7.4 plots the differences between the two groups for the L-M chromatic channel. Interestingly this shows that there is no statistically significant difference in the L-M channel activation between males and females. That is, the cone-opponent channel responsible for the perception of red and green does not differ significantly between males and females. Figure 7.5 depicts the results for the S-(L+M) cone-opponent channel. The two upper panels show the S-(L+M) channel activation for males (left) and females (right). As in the L-M channel activation, the inter-subject variability is reduced, in comparison with the inter-subject variability for hue rotation and saturation. The same sine function, as in L-M channel, is fitted to the data giving R2 = 0.775 and R2 = 0.792 for males and females respectively (p<0.0001). Panel c results show no statistically significant difference in the S-(L+M) channel activation between the males and females.

7.4.4 Female observers with wide anomaloscope matching range

As mentioned before, all subjects were tested for colour vision defects with a battery of conventional colour vision tests. Several studies have shown that Nagel anomaloscope data could provide an insight as to whether a female observer is a carrier for colour deﬁ- ciency (Jordan & Mollon, 1993) or whether in a group of male observers there are more than one L- and/or M-cone pigments present (Neitz & Jacobs, 1986; Neitz et al., 1993).

173 7.4. RESULTS

Figure 7.5: S-(L+M) activation for male and female observers. The a and b panels depict the S-(L+M) channel activation for males and females respectively, as a function of chromatic axis. The dashed lines are the 95% conﬁdence bounds of the ﬁtted functions. The small black data points are the raw data for all the observers. Panel c (lower) depicts the differences between the two upper panels as a function of chromatic axis. The black line is the mean of the differences and the dashed lines are the mean ± 1.96S.D.

Figure 7.6 provides the midpoints and matching ranges of the 19 male and 19 female colour normal observers who participated in the present study. The data in Figure 7.6 data show no statistically signiﬁcant difference in the means of the midpoints between males and females (p=0.519, a=0.05, independent sample t- test) and no statistically signiﬁcant difference in the matching range (p=0.465, a=0.05, independent sample t-test), even though females show a slightly higher matching range. Pokorny, Smith, Verriest, and Pinckers (1979) argue that the anomaloscope range is a measure of hue discrimination and Jordan and Mollon (1993) found that this is the case

174 7.4. RESULTS

Figure 7.6: Nagel anomaloscope results. Midpoints (open squares and circles) and matching ranges (x axis’ error bars) for males (left hand side panel) and females (right hand side panel). The x axis is the Red-green mixture scale of the Nagel anomaloscope and the y axis are the 19 observers of each group in ascending order of midpoints. The arrows indicate the four females with the wider matching range (for explanation see text). for carriers of colour vision deﬁciency. They found that the matching range of the carriers was signiﬁcantly greater than that of colour normal females. In Figure 7.6 one can see that there are a few female observers with wider matching range than the rest (see arrows in Figure 7.6). Also, the prevalence of total carriers in the colour normal population is about 15% (Sharpe et al., 1999; Jordan & Mollon, 1993) and 15% of the 19 females would be 3 observers. So, from the female group the three observers with the widest matching range can be excluded because of the possibility of being carriers of a colour defect (a similar approach was carried out by Rodriguez-Carmona et al. (2008)). Because female observers No2 and No11 have the same matching range (7 units), both of them are excluded. That

175 7.5. DISCUSSION results in a total of 15 female observers. Comparing the saturation match between the two groups (19 males and 15 females), a statistically signiﬁcant difference found again for axes 225◦ and 240◦ (p=0.0015, a=0.05, independent sample t-test, power of 89%). Following the logical argument above, by excluding the worst females, according to their matching range, it would expected the female group to have less saturation loss and thus the difference between the two groups should have increased. Instead, the p value of the t-test decreased by excluding these 4 females. That means that the exclusion of the 4 females did not improve at all the overall saturation match of the group in the given region of the colour space. An explanations that could be considered here is that the 4 females performed better than the rest of the group in this given region of the colour space, meaning that their wide anomaloscope matching range is not necessarily an index of abnormality. On the contrary their ability in peripheral matching is better than that of the rest of the group in the particular region of the colour space. For the sake of completeness, the 4 females were excluded from the hue rotation and channel activation data. This did not change the conclusions of the analysis.

7.5 Discussion

A strong statistically signiﬁcant difference (p=0.0006, a=0.05) is found in saturation loss between male and female colour normal observers in the region between the chromatic axes of 221◦ and 244◦. Females exhibit less saturation loss by 36% when compared with males indicating increased female chromatic sensitivity in this region of the colour space. Also, no signiﬁcant difference was found in either the Nagel anomaloscope mid- point or the matching ranges in accordance with some studies and contrary to others (Rodriguez-Carmona et al., 2008; Pardo et al., 2007; Neitz & Jacobs, 1986). It is clear that there are substantial differences between the experimental procedure

176 7.5. DISCUSSION employed here and previous studies. For example Jameson et al. (2001) used a psychophysical test to assess how many different colour bands are present in the range of the visible spectrum and, as they say, their experiment make use of higher order brain processes. In stark contrast, the simple colour matching task used in this study is, almost certainly, based on the first and second stage of colour perception. Pardo et al. (2007) used a modified version of Rayleigh matching procedure concentrating on hue discrimination only ignoring potential differences in sensitivity. Rodriguez-Carmona et al. (2008), on the other hand, used a test for colour vision deficiencies based on chromatic sensitivity only, ignoring any possible differences in hue discrimination. The unique aspect of the present study is that it investigates peripheral colour vision taking into account both hue discrimination (expressed as peripheral hue distortion differences) and chromatic sensitivity (expressed as saturation loss). Of course, the more profound and novel difference between all studies for sex differences in colour vision and the present study is the fact that colour performance is assessed in the peripheral visual field instead of the central foveal field. It could be argued that in everyday life observers use mostly central vision which is specialised for colour due to high cone and neural density. However, it should be noted that in the central visual field there are major physiological differences between individuals. Webster and MacLeod (1988) identified as sources for colour vision variation the macular pigment density, the lens-pigment density, the position of the cone spectral sensitivity (in other words the cone- polymorphism), the cone-pigment density and rod-intrusion. Macular pigment density for example, not only differs substantially between observers but also differs between males and females, with males having on average 38% more macular pigment density than females (Hammond et al., 1996). Macular pigment may affect predominantly short- wavelength absorption but may plays a more subtle role when metameric colours are used (ie computer screens) instead of spectral lights. In this study, by moving the stimuli at 1◦

177 7.5. DISCUSSION parafoveal and 18◦ eccentrically the possible effect of macular pigment is avoided. Cone density is known to be highly variable among individuals in the central one degree (Curcio, Sloan, Packer, Hendrickson, & Kalina, 1987) while it converges with increasing the retinal eccentricity and of course there are compensating mechanisms to take into account the variation in L/M ratio (Neitz, Carroll, Yamauchi, Neitz, & Williams, 2002). This foveal variability is expected to influence the cone-pigment density and consequently the quanta catches (Elsner, Burns, & Webb, 1993) while eccentrically it is expected to be less variable among individuals. However, male-female differences between foveal and peripheral visual field in lens-pigment density and rod intrusions are not expected. Macular pigment density, cone and cone-pigment density may be enough to either exaggerate or camouflage any potential sex related differences in central chromatic visual performance. As no sex-related difference found in the chromatic cone-opponent channel (luminance was not a variable so as to neither agree with nor contradict Bimler et al. (2003)) it could be assumed that any male-female differences are due to the first stage of the visual pathway. The region of the colour space where significant difference is identified is between about 520nm and 550nm in terms of spectral colours. This corresponds to the region of the colour space where M-cones have their peak spectral sensitivity. A possible explanation for the finding described here could therefore be the M-cone polymorphism. The prevalence of M-cone polymorphism in the male population is 6% for serine M-cone and 94% for alanine M-cone (Sharpe et al., 1999) while for females, due to X-chromosome inactivation, is 0.3% for serine M-cone, 88.4% for alanine M-cone and 11.3% for possessing both serine and alanine M-cones. It is likely these percentage differences are enough to account for the difference in saturation loss. Another possible explanation could be the finding of Bimler et al. (2003) in which they showed that females put more weight in their discrimination judgements in a green-red direction. That could

178 7.5. DISCUSSION mean that the female group is more alert than males when colours in the green region of the colour space are presented for testing. Consequently they are more careful in their matching task resulting in more precise settings. But again, the data do not confirm the same for the red region of the colour space where no significant difference is found. As far as the argument for female carriers, at the end of the results section, is concerned, by excluding the worst females for Nagel anomaloscope matching range the female group should have shown less saturation match and thus the difference between the two groups should have been larger. Instead, the p value of the t-test decreased by excluding these 4 females. That means that the exclusion of the 4 females did not improve at all the overall saturation match of the group in the given region of colour space. Paradoxi- cally, the performance of the 4 females improved the overall performance of the female group in this particular region. That means that their wide matching range is not necessarily an index of abnormality. Hood et al. (2006) argue that carriers of protan deficiency do not differ from colour normals. Only the carriers of deutan deficiency showed different chromatic performance from the colour normals. If this is the case, then the four females, as they have an effect on the overall chromatic sensitivity in this particular region of the colour space, could be carriers of deutan defect possessing a normal and an abnormal M-cone in their retinae. But, this extra abnormal M-cone does not necessarily make them worse observers than the others but offers them a ‘richer colour experience’ as Jameson et al. (2001) argue. Maybe there are more carriers in the group of females, resulting in better sensitivity due to the extra M-cone. No rigorous conclusions can be drawn on whether the unambiguous difference found in the present study is due to carriers or due to another factor unless the psychophysical results will be combined with gene analysis.

179 7.5. DISCUSSION

Author contribution

The experiments, the analysis and the writing for this chapter/paper were made by A. Panorgias. I.J. Murray contributed to correcting the manuscript and he is the ﬁrst who noticed a possible male-female difference in a 2005 colour matching study. The experiments were conducted using a software written by N.R.A. Parry. Both N.R.A. Parry and D.J. McKeefry helped by discussing the ﬁndings.

180 7.6. REFERENCES

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Nowaczyk, R. (1982). Sex-related differences in the color lexicon. Language and Speech, 25, 257–265. Pardo, P., Perez, A., & Suero, M. (2007). An example of sex-linked color vision differences. Col Res Appl, 32, 433–439. Parry, N. R., McKeefry, D. J., & Murray, I. J. (2006). Variant and invariant color perception in the near peripheral retina. J Opt Soc Am A Opt Image Sci Vis, 23(7), 1586– 97. Pickford, R. (1951). Individual differences in colour vision. London: Routledge and Kegan Paul. Pokorny, J., Smith, V., Verriest, G., & Pinckers, A. (1979). Congenital and acquired color vision defects. New York: Grune Stratton. Rodriguez-Carmona, M., Sharpe, L. T., Harlow, J. A., & Barbur, J. L. (2008). Sex-related differences in chromatic sensitivity. Vis Neurosci, 25(3), 433–40. Sharpe, L., Stockman, A., Jagle, H., & Nathans, J. (1999). Opsin genes, cone photopigments, color vision and color blindness. In K. Gegenfurtner & L. Sharpe (Eds.), Color vision. from genes to perception. Cambridge: Cambridge University Press. Silverman, I., & Eals, M. (1992). Sex differences in spatial abilities: evolutionary theory and data. In J. Barkow, L. Cosmides & J. Tooby (Eds.), The adapted mind. Oxford: Oxford University Press. Simpson, J., & Tarrant, A. W. (1991). Sex- and age-related differences in colour vocabulary. Lang Speech, 34 ( Pt 1), 57–62. Stanikunas, R., Vaitkevicius, H., Kulikowski, J. J., Murray, I. J., & Daugirdiene, A. (2005). Colour matching of isoluminant samples and backgrounds: a model. Per- ception, 34(8), 995–1002. Thomas, L., Curtis, A., & Bolton, R. (1978). Sex differences in elicited color lexicon size. Percept Mot Skills, 42, 77–78.

183 7.6. REFERENCES

Verriest, G., Vandevyvere, R., & Vanderdonck, R. (1962). Nouvelles recherches se rap- portant a l’inﬂuence du sexe et de l’age sur la discrimination chromatique ainsi qu’a la signiﬁcation pratique des resultats du test 100 hue de farnsworth-munsell. Revue d’Optique, 41, 499–509. Webster, M. A., & MacLeod, D. I. (1988). Factors underlying individual differences in the color matches of normal observers. J Opt Soc Am A, 5(10), 1722–35.

184 CHAPTER EIGHT

CONCLUSIONS AND FUTURE EXPERIMENTS

N this last chapter a summary of the conclusions from this work is provided. Addi- I tional experiments, which will provide further insight and help to draw more rigorous conclusions regarding peripheral colour vision are discussed.

8.1 Conclusions

In the present work two experimental procedures were used. First, an asymmetric colour matching paradigm, where the observer had to match the chromaticities of two spots, one seen parafoveally and the other one eccentrically. Second, a 4 alternative forced choice naming paradigm where the observer had to name the chromaticity of a spot as red, blue, green or yellow. The experimental conditions changed slightly for each chapter so as to address its aims. In Chapter 3 a nasal-temporal asymmetry was described in colour matching performance. Less peripheral saturation loss is seen in the temporal than the nasal visual field. L-M cone opponent activity differs significantly between the two visual fields (showing least change in the temporal visual field) while S-(L+M) cone opponent activity is unchanged across the horizontal meridian. The results suggest that colour matching relies

185 8.1. CONCLUSIONS on the intricacies of neural circuitry and that sensitivity is reduced with the number of L- and M-cones and ganglion cells. The results in Chapter 4 showed that unique hues remain stable with eccentricity and purity, when identified with the naming paradigm, and that three out of four invariant hues (defined as those hues that remain unchanged with eccentricity) match reasonably well with three of the corresponding unique hues. As reported previously, unique green does not correspond to invariant green for any of the observers. Hence it is shown that colour matching results, mediated presumably by retinal mechanisms correspond to some extent with the results from the colour naming experiment which taps higher brain loci. It is shown that the discrepancy between invariant and unique green is not due to eccentricity and purity. In order to investigate further the origin of the discrepancy between invariant and unique green, data were obtained for a large number of observers. The results, analysed in terms of cone contrast, showed that the RMS cone contrast of invariant green, unlike that of unique green, changes markedly between parafoveal and peripheral viewing. A possible explanation for the mismatch between invariant and unique green may be the reduced number of M-cones in peripheral retina. This in turn suggests that the cone contrast match is valid only in the case where the reference and testing fields occupy/stimulate either the same or similar regions of the retina. In the case when the two fields are spatially separated on the retina and do not excite the same number of cones the cone contrast for L- and M-cones changes but it remains the same for S-cones whose distribution does not change dramatically across the visual field. The origins of the ‘special’ hues are discussed in Chapter 6. Invariant blue and yellow fall exactly on the daylight locus showing that colour matching, is strongly influenced by the phases of daylight and remains stable across the visual field while in other regions of the colour space matching undergoes substantial hue and saturation distortion. Unique

186 8.2. FUTURE EXPERIMENTS blue and yellow fall on the daylight locus suggesting that discrimination is also influenced by terrestrial illumination. Inter-observer variability is also found to be reduced around the daylight locus, pointing to the possibility that the blue-yellow system is more stable than the red-green, because of its more ancient phylogeny. An attempt to find out whether there are male-female differences in peripheral colour vision was described in Chapter 7. There is compelling evidence that females exhibit less saturation loss by 36% between 520nm and 550nm than males. As no difference was found in post-receptoral activation of the chromatic channels, the results suggest that any difference can be attributed to the first stage of colour vision, i.e. the photoreceptors and namely the M-cones, as their peak spectral sensitivity corresponds to the region in colour space where the difference was found. A possible explanation of this difference is the polymorphism of the M-cones and the X-inactivation which can lead to more than three cone types in the female retina.

8.2 Future experiments

In Chapter 5 it is speculated that the discrepancy between invariant and unique green is due to the reduced number of M-cones in the periphery. This idea could be tested by increasing the peripheral stimulus’ size so as to activate the same or similar number of cones as the parafoveal stimulus. That way it would be interesting to see how much, if any, invariant green is shifted closer to unique green’s chromatic axis. This would conﬁrm the speculation that the reduced number of M-cones accounts for the position of invariant green. Of course, it is not only the cone density that it is changing, but the connectivity between cones, bipolar and ganglion cells. With increasing eccentricity each ganglion cell receives inputs from more than two neighbouring cones which results in larger receptive ﬁelds in peripheral retina. There is no way to control the cone input to ganglion cells, so

187 8.2. FUTURE EXPERIMENTS the speculation should be limited to cone density and distribution. In the same chapter it is found that parafoveal and peripheral L- and M-cone contrast do not match despite colour matching. This is attributed to the reduced number of L- and M-cones that are activated in periphery compared with the number of cones activated parafoveally. An experiment to reinforce this idea is to identify two retinal regions, one in the nasal and one in the temporal visual field, which have the same cone density. If the cone contrast would not change between these two different conditions this would confirm the notion that number of cones stimulated influences whether or not the cone contrast changes between parafoveal and peripheral matching. As seen in Chapter 5, the chromatic axes employed in this work produce variable RMS cone contrast. Blue and yellow regions exhibit the highest RMS cone contrast while the red and green regions the lowest. An important follow-up experiment would be to employ chromatic axes which produce the same RMS cone contrast. That way, more perceptually uniform stimuli would be used for the colour matching experiment and maybe other distortions in colour perception in the peripheral retina will be observed. Finally, in Chapter 7 it is shown that there is a significant difference in saturation loss between males and females and it was speculated that this is due to M-cone polymorphism and X-inactivation. One way of testing this hypothesis would be to repeat the peripheral colour matching experiment and divide the observers into those having only alanine M- cones or only serine M-cones, according to their genetic profile,

188 APPENDIX A

CIE1976 LU’V’ COLOUR SPACE

189 In this study the CIE1931 xy colour space is selected to represent the chromaticities of the stimuli and of the results. In this appendix the matching results are plotted in another colour space space which is regarded as being more perceptually uniform. This colour space is called Lu’v’ where l is the luminance and u’, v’ the coordinates of the abscissa and the ordinate. In Figure A.1 the matching results of Figure 6.3 are plotted in the Lu’v’.

Figure A.1: The average matches of 38 observers. The black dots are the probe chromaticities and the open circles are the corresponding matches. The grey shaded area depicts ±1S.D. from the matches. The dashed curve is the daylight locus and the dark grey lines the cardinal axes. The asterisks are the average unique hues from three observers. UR, UB, UG and UY stand for unique red, blue, green and yellow respectively.

As it can be seen from the above graph, there is the same elongation on the matching data along the L-M cardinal axis. The variability is maximised again close to cardinals

190 red and green and minimised close to unique blue and unique yellow. Unique hues deviate from the cardinal axes to the same extent as they deviate in the CIE1931 xy colour space from the cardinal axes. In conclusion, the use of CIE1976 u’v’ colour space is not affecting the matching and the naming results.

191 APPENDIX B

ELLIPSES

192 In Chapter 6 ellipses are ﬁtted on the matching data (in CIE1931 xy coordinates) using the method described by Halir and Flusser (1998). The general equation of a conic section is ax2 + bxy + cy2 + dx + ey + f = 0 (B.0.1)

Using MatLab code the a, b, c, d, e and f coefficients of equation B.0.1 are defined. From these, the centre, the major and minor semi-axes and the orientation of the ellipse are found. The centre (xo, yo) is defined as:

2cd − be x = o b2 − 4ac

2ae − bd y = (B.0.2) o b2 − 4ac

The semi-axis length is given by:

s 2(ae2 + cd2 + fb2 − bde − 4acf) a0 = (b2 − 4ac)[p(a − c)2 + b2 − (a − c)]

s 2(ae2 + cd2 + fb2 − bde − 4acf) b0 = (B.0.3) (b2 − 4ac)[−p(a − c)2 + b2 − (a − c)]

193 The orientation φ of the ellipse is given by:

 0 when b = 0, a < c     π  2 when b = 0, a > c φ = (B.0.4)  1 cot−1( a−c ) when b 6= 0, a < c  2 b    π 1 −1 a−c  2 + 2 cot ( b ) when b 6= 0, a > c

Matlab code

The MatLab code used to ﬁt the ellipses on the (x, y) data points is given in Halir and Flusser (1998) and has as follow: function a= fit _ellipse (x, y)

D1 = [x * x, x * y, y * y] D2 = [x, y, ones(size(x))]

S1 = D1 * D1 S2 = D1’ * D2 S3 = D2’ * D2 T = -inv(S3) * S2 M = S1 + S2 * T M = [M(3, :) ./ 2; -M(2, :); M(1, :) ./2] [evec, eval] = eig(M) cond = 4*evec(1, :).* evec(3, :) - evec(2, :) .* evec(2, :) a1 = evec(:, find(cond>0)) a = [a1; T * a1]

The a, b, c, d, e, and f coefﬁcients are the elements of matrix a.

194 B.1. REFERENCES

B.1 References

Halir, R., & Flusser, J. (1998). Numerically stable direct least square ﬁtting of ellipses, 125–132. 6th International Conference in Central Europe on Computer Graphics and Visualization. WSCG ’98. CZ. Plzeo.

195 APPENDIX C

NON PARAMETRIC STATISTICAL TEST FOR CIRCULAR DATA

196 In Chapter 7 a statistical comparison was necessary to test whether there is any statistically significant difference in hue rotation (expressed in degrees) between the male and female population. Since the data are circular and not normal (they are not drawn from von Misses distribution), non-parametric tests have to be used in order to establish if there is statistically significant difference or not (Batschelet, 1981). Here, the non-parametric test used for this comparison is described briefly.

◦ ◦ Let the two populations have vector rotations (ranging form 0 to 360 ) φ1, φ2, ... ,

φn and ψ1, ψ2, ... , ψm and the chromatic axis in comparison is θ. The absolute difference between the vector rotation and the chromatic axis results in hue rotation θRm and θ f for i Ri the males and females respectively.

θ m = |φ − θ|, i = 1, 2, 3, . . . , n (C.0.1) Ri i

θ f = |ψi − θ|, i = 1, 2, 3, . . . , m (C.0.2) Ri

The hue rotations θRm and θ f of both groups are then ranked in ascending order and the i Ri sum of the ranks is calculated (Sm and Sf ) for the male and female group respectively. According to the Wilcoxon-Mann-Whitney test we calculate the

n(n + 1) U m = Sm − (C.0.3) 2 m(m + 1) U f = Sf − (C.0.4) 2

Comparing the smaller of U m and U f (test statistic) with the critical U(α) value (from U distribution tables) a decision of whether there is statistically signiﬁcant difference or not is made. If U is less than or equal to U(α) then a statistically signiﬁcant difference is established between the two groups, otherwise the hue rotation of the two groups is not different (Batschelet, 1981).

197 C.1. REFERENCES

C.1 References

Batschelet, E. (1981). Circular statistics in biology. Mathematics in biology. London: Academic Press Inc.

198 APPENDIX D

REPRINT: NASAL-TEMPORAL DIFFERENCES IN CONE OPPONENCY IN THE NEAR PERIPHERAL RETINA.

The ﬁrst page of the published paper described in Chapter 3 and the Copyright License Agreement.

199 Ophthal. Physiol. Opt. 2009 29: 375–381

Nasal-temporal differences in cone- opponency in the near peripheral retina A. Panorgias1, N. R. A. Parry2, D. J. McKeefry3, J. J. Kulikowski1 and I. J. Murray1 1Faculty of Life Sciences, Moffat Building, University of Manchester, Manchester M60 IQD, 2Vision Science Centre, Manchester Royal Eye Hospital, Manchester, and 3Optometry and Vision Sciences, University of Bradford, Bradford, UK

Abstract The purpose of this study is to establish whether nasal-temporal differences in cone photoreceptor distributions are linked to differences in colour matching performance in the two hemi-fields. Perceived shifts in chromaticity were measured using an asymmetric matching paradigm. They were expressed in terms of hue rotations and relative saturation changes and also in terms of activation levels of L)M or S)(L+M) cone-opponent channels. Up to 19° eccentricity there was little difference in chromaticity shifts between nasal and temporal retina for either channel. For matches beyond 19° L)M activation is significantly lower in the nasal field and the S)(L+M) channel was equally activated in both fields. The data are consistent with the asymmetric distribution of L- and M-cones in the nasal and temporal retinae.

Keywords: colour matching, cone-opponent channels, nasal-temporal retina, peripheral retina

saturation of peripheral targets in many different ways Introduction (Volbrecht et al., 1993). The quality of colour perception in the peripheral visual When the activity of rods is minimized and perception field declines with eccentricity. Observers describe a is mediated primarily by cones, there are indications that desaturation effect when coloured stimuli in the periph- stimulus size and other factors, such as cortical magni- ery are compared with similar stimuli placed in the fication, compensate for the reduced quality of colour central visual field. Changes in hue are also reported, as vision in the peripheral field (Van Esch et al., 1984; described in the early papers by Moreland and Cruz Abramov et al., 1991; Vakrou et al., 2005). There are (1959) and Stabell and Stabell (1976b). The most many advantages to interpreting these changes in colour obvious explanation for the reduction in colour vision vision in terms of cone-opponent pathways. It is well in the periphery is that sampling of the retinal image by known that the early stages of human and higher cones declines as their density is reduced. A second issue primate vision are mediated by three independent considered by many authors (Stabell and Stabell, 1976a; mechanisms (Hurvich and Jameson, 1955; Hering, Buck, 1997; Buck et al., 2000) is the possible role of 1964; Ingling and Tsou, 1977); one based on antagonis- rods. Rod density is much greater in the peripheral than tic interactions between L- and M-cones, another based the central retina, reaching a peak at around 20°. Rods on antagonistic interactions between S-cones and some have the potential to influence both the hue and the combination of L-, M- and S-cones (Krauskopf et al., 1982; Derrington et al., 1984; Lee et al., 1987), and a third which combines the activity of the L- and M-cones and signals luminance. These channels have a well- Received: 30 October 2008 defined neural substrate in the retina and lateral Revised form: 27 January 2009 geniculate body (LGN) (Krauskopf et al., 1982; Der- Accepted: 3 February 2009 rington et al., 1984; Lee et al., 1987). They must Correspondence and reprint requests to: I. J. Murray. represent the start of a cascade of neural events that Tel.:+44 161 3063886; Fax: +44 161 308887. culminates in the perception of colour. There is both E-mail address: [email protected] neurophysiological and psychophysical evidence for

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https://s100.copyright.com/AppDispatchServlet Page 4 of 4 APPENDIX E

REPRINT: NAMING VERSUS MATCHING AND THE STABILITY OF UNIQUE HUES

The ﬁrst page of the published paper described in Chapter 4 and the Copyright License Agreement.

200 Ophthal. Physiol. Opt. 2010 30: 553–559

Naming versus matching and the stability of unique hues A. Panorgias1, J. J. Kulikowski1, N. R. A. Parry2, D. J. McKeefry3 and I. J. Murray1 1Faculty of Life Sciences, Moffat Building, University of Manchester, Manchester, M60 1QD, 2Vision Science Centre, Manchester Royal Eye Hospital, Manchester, and 3Bradford School of Optometry & Vision Sciences, University of Bradford, Bradford, UK

Abstract It is known that there is a distortion of hue and saturation in the peripheral visual field. In a previous study, when an asymmetric matching paradigm was used, four hues in the blue, red, yellow and green regions of colour space were unchanged and these were referred to as peripherally invariant (Parry et al., J Opt Soc Am A, 23, 2006, 1586). Three of these invariant hues were similar to unique blue, red and yellow. However, for most observers there was a marked difference between unique and invariant green. To investigate this apparent paradox, we have measured unique hues using a range of eccentricities and colourimetric purities. An asymmetric matching and a 4-AFC paradigm were used to establish peripherally invariant and unique hues, respectively. In the asymmetric matching task the observer matched a peripheral spot with a para-foveal spot, for 24 different hues at 18° eccentricity. In the 4-AFC paradigm, 41 hues were presented 20 times at three purities (0.5, 0.75 and 1.0) and three eccentricities (18°, 10° and 1°). The observer had to name the hues as red, blue, green or yellow. Unique hues were found to be constant with eccentricity and purity. The unique green, established with 4-AFC, was found to differ from the invariant green, determined using the matching task. However, red, blue and yellow invariant hues correspond well with unique hues. The data suggest that different mechanisms mediate the matching of green compared with the identification of unique hues. This is similar to the difference between detection and discrimination of spectral stimuli: the detection process is dominated by the cone opponent mechanisms and is most sensitive, whereas more central processes, serving unique hues, influence discrimination.

Keywords: colour matching, naming, peripheral colour vision, peripherally invariant hues, unique hues

blue-yellow are organized as a pair of perceptually Introduction opposite hue mechanisms. What this means is that How the basic hue mechanisms are encoded in human those with normal colour vision do not see reddish- vision is an enduring problem. Ewald HeringÕs qualita- greens or bluish-yellows. This simple observation relies tive description (Hering, 1964) of four colour sensations on verbal expression to convey the four basic hue based on red, green, blue and yellow, was conﬁrmed sensations, but it is universal; all colour-normal hu- quantitatively by Hurvich and Jameson (1955) who mans, regardless of language or culture (Berlin and showed, using hue cancellation, that red-green and Kay, 1969; Saunders and van Brakel, 1997) and age (Schefrin and Werner, 1990), can easily adjust a colour Received: 28 August 2009 so that it is neither red nor green, or neither blue nor Revised form: 28 January 2010 yellow (Valberg, 1971). Accepted: 13 February 2010 The four unique hues are the most overt and fundamental manifestation of the higher order organi- Correspondence and reprint requests to: Athanasios Panorgias, Faculty zation of colour processing (Mollon and Jordan, 1997). of Life Sciences, Moffat Building, University of Manchester, P.O. Box 88, Manchester, M60 1QD, UK. They represent the centres of the basic colour categories Tel.: +441613063878; Fax: +441613063887. (De Valois et al., 1997), in that red and green are the E-mail address: [email protected] colours seen when the yellow-blue mechanism is in

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Licensed content title Naming versus matching and the stability of unique hues Licensed content author A. Panorgias,J. J. Kulikowski,N. R. A. Parry,D. J. McKeefry,I. J. Murray Licensed content date Sep 1, 2010 Start page 553 End page 559 Type of use Dissertation/Thesis Requestor type Author of this Wiley article Format Print and electronic Portion Full article Will you be translating? No Order reference number Total 0.00 USD Terms and Conditions TERMS AND CONDITIONS

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