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On the Perceptual Identity of Depth Vision in the Owl On the Perceptual Identity of Depth Vision in the Owl Von der Fakult¨atf¨urMathematik,Informatik und Naturwissenschaften — Fachbereich 1 — der Rheinisch-Westf¨alischen Technischen Hochschule Aachen zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigte Dissertation vorgelegt von Doctorandus Robert Frans van der Willigen aus Goes, Niederlande Berichter: Universit¨atsprofessor Dr. H. Wagner Universit¨atsprofessor Dr. A.J. van Opstal Tag der m¨undlichen Pr¨ufung: 20. Oktober 2000 ”Diese Dissertation ist auf den Internetseiten der Hochschulbibliothek online verf¨ugbar” This work was supported by the Deutsche Forschungsgemeinschaft (Wa 606/6) and the Humboldt Foundation. All animals were cared for and treated under a permit from the Regierungsprsidium K¨oln (Germany) and according to ”Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health (NIH, http://www.nih.gov/). Publication Data: van der Willigen, R.F. Front Page: Owl standing on a perch RFvdW 1998. Title: On the Perceptual Identity of Depth Vision in the Owl Subtitle: A Neuroethological Approach Towards Avian Vision Key words: Depth vision / Discrimination-transfer / Stereopsis / Motion-parallax / Animal psychophysics / Neuroethology —To my parents, who taught me to seek the truth— —To my teachers, who showed me how— —To Mireille, who gave me new born life— CONTENTS 1 General introduction ............................. 1 1.1 Rationale . 1 1.2 Depth perception . 3 1.3 Stereopsis . 5 1.4 Functions and evidence for stereopsis in animals . 7 1.5 Binocular vision in the owl . 9 1.6 Outline . 12 2 Methods ................................... 15 2.1 Subjects and surgery . 15 2.2 Apparatus and Stimulus Presentation . 16 2.2.1 Experimental setup ....................... 16 2.2.2 Head-movement calibration ................... 18 2.2.3 Stereogram presentation .................... 19 2.3 Behavioural procedures . 22 2.3.1 Initial operant conditioning ................... 22 2.3.2 Discrimination training and testing ............... 24 2.3.3 Measurement of perceptual categorisation ........... 26 2.4 Discrimination paradigms and stimuli . 27 2.4.1 Basic discrimination paradigms ................. 27 2.4.2 Random-dot stereograms .................... 28 2.4.3 Monitor calibration ....................... 30 2.4.4 Stereoscopic motion ....................... 32 2.4.5 Kinematograms ......................... 32 2.4.6 Motion parallax stimuli ..................... 34 3 Discriminative learning and the specificity of visual perception ..... 38 3.1 Introduction . 40 3.2 Experiment I: Operant Conditioning . 41 3.2.1 Methods ............................. 41 3.2.2 Results and Discussion ..................... 41 vi On the Perceptual identity of Depth Vision in the Owl 3.3 Experiment II: Discrimination learning and transfer tests . 42 3.3.1 Methods ............................. 43 3.3.2 Results and Discussion ..................... 45 Discrimination paradigm I: Texture perception .. 45 Discrimination paradigm II: Motion perception .. 51 3.4 General discussion . 59 3.4.1 Discriminative learning ..................... 59 3.4.2 Signal-detection analysis and stimulus control ......... 60 4 Basic demonstration of functional stereopsis ............... 63 4.1 Introduction . 64 4.2 Methods . 65 4.2.1 Animals and behavioural apparatus ............... 65 4.2.2 Behavioural procedures and paradigms ............. 65 4.2.3 Discrimination tasks, stimuli and controls ........... 65 4.2.4 Data analysis .......................... 67 4.3 Results and Discussion . 67 4.3.1 Discrimination training ..................... 67 4.3.2 Transfer to stereoscopic stimuli ................. 69 4.3.3 Performance under monocular viewing conditions ....... 75 4.3.4 Methodological considerations ................. 76 5 The functional significance of owl stereoscopic vision .......... 79 5.1 Introduction . 80 5.2 Methods . 81 5.2.1 Subjects, Apparatus and Stimuli ................ 81 5.2.2 Behavioural procedures ..................... 81 5.2.3 Data analysis .......................... 84 5.3 Results . 84 5.3.1 Stereopsis and its dependence on contrast ........... 84 5.3.2 Stereo acuity .......................... 86 5.3.3 Stereo acuity as function of luminance ............. 88 5.3.4 Upper limit of stereopsis .................... 91 5.4 Discussion . 91 5.4.1 Methodological issues ...................... 91 5.4.2 The effect of contrast and stimulus illumination ........ 92 5.4.3 Stereoscopic resolution ..................... 94 Contents vii 6 Stereopsis and motion parallax produce similar depth impressions .. 96 6.1 Introduction . 98 6.2 Methods . 99 6.2.1 Animals and behavioural apparatus ............... 99 6.2.2 Stimulus configuration and parameters ............. 99 6.2.3 Behavioural procedures, tests and controls ........... 102 6.2.4 Data analysis and off-line analysis ............... 102 6.3 Results and Discussion . 104 6.3.1 Behavioural task ......................... 104 6.3.2 Transfer to motion parallax stimuli: .............. 104 6.3.3 Peering behaviour ........................ 108 6.3.4 No transfer during passive viewing ............... 110 6.4 General discussion . 112 7 General Discussion ............................. 115 7.1 Discrimination transfer as a tool to study vision . 115 7.2 Figure-ground perception . 116 7.3 Depth perception . 119 7.4 Final word . 128 Abbreviations & Symbols ........................... 131 References ................................... 134 Acknowledgements .............................. 151 Curriculum Vitae ................................ 152 viii On the Perceptual identity of Depth Vision in the Owl 1 GENERAL INTRODUCTION . Why cite me the examples of the ancient? It is no disgrace to pass on profound wisdom —Saint Ambose, answer to Symmachus 1.1 Rationale This thesis addresses a key issue in the psychophysical approach to vision—stereopsis— the perception of three-dimensional space achieved through binocular vision. Be- havioural experiments are described from which it is concluded that stereopsis is a robust and highly sensitive function of the owl visual system and its significance can be explained in terms of the camouflage-breaking hypothesis. An intriguing phenomenon of visual perception is the ability to determine the three-dimensional relationships of objects that constitute the visual scene from two- dimensional patterns of light that are projected onto the two retinae. One solution to this problem is binocular vision: viewing with two separated but frontally placed eyes as is the case in humans. Under binocular viewing conditions a common segment of visual space (binocular overlap) is viewed by the two eyes simultaneously which makes possible the perception of depth based on small variations (binocular disparity) between the monocular retinal images. This capacity is known as stereopsis and requires neural operations that combines the information from each eye’s sample. Despite the differences in the optics and the neural substrate, it has been sug- gested that there is a high degree of similarity between the avian and mammalian neural strategy that underlies stereopsis. However, unequivocal behavioural and neu- rophysiological evidence of stereopsis in vertebrate animals has so far been found in only two mammalian species: macaque monkey and domestic cat. Due to their frontally placed eyes, owls have binocular overlap, and neurons sen- sitive to binocular disparity have been described in the barn owl’s visual Wulst—the avian analogue of the mammalian visual cortex. Motivated by these data, I undertook a behavioural investigation of stereopsis in the barn owl. 2 On the Perceptual Identity of Depth Vision in the Owl Figure 1: Monocular pictorial depth cues: A. Side view of a scene. B. The tracing on the picture plane reveals the cues needed to perceive depth. Interposition: The fact that rectangle 4 interrupts the outline of 5 indicates which of the objects is in front, but not how much distance there is between them. Linear perspective: Although lines 6-7 and 8-9 are parallel in reality, they converge in the picture plane. Size perspective: The more distant boy (2) appears smaller than the closer boy (1) in the picture plane. Familiar size: The man (3) and the nearest boy are drawn to the same size in the picture. If one knows that the man is taller than the boy, it is possible to deduce on the basis of their sizes in the picture that the man is more distant than the boy. This type of cue is weaker than the others (Adapted from Hochberg, 1986). Chapter 1: General introduction 3 1.2 Depth perception The retina, the starting point of visual input in all vertebrate animals, such as mam- mals and birds, is a two-dimensional surface. This means the images formed on the retinae are flat and have no depth at all. The apparent missing third dimension (depth information), however, can still be appreciated from these two-dimensional represen- tations of visual space and is called space or depth perception (Collett and Harkness, 1982; Arditi, 1986). Thus, our eyes are the medium, and the visual cortex—the part of our brain dedicated to vision—is charged with making inferences about what we see. It is hypothesised that there is a direct relationship between seeing a stimulus in the visual field and associating it with depth. These “simple sensations” are the depth cues. They come in many different and diverse forms, but can be put into two major groups: monocular and binocular cues. Monocular cues are those which only need one eye (monocular vision) to
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