On the Perceptual Identity of Depth Vision in the Owl

Von der FakultätfürMathematik,Informatik und Naturwissenschaften — Fachbereich 1 — der Rheinisch-Westfälischen 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 suggested that there is a high degree of similarity between the avian and mammalian neural strategy that underlies stereopsis. However, unequivocal behavioural and neurophysiological 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 sensitive 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 mammals 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 representations 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 perceive depth. Pictorial cues are examples of these and there are many types of pictorial cues (Figure 1). An example of a non-pictorial monocular cue is accommodation. Accom- modation refers to the change in the lens shape (e.g., the lens will contract to look at something close up). The contribution of monocular cues to depth perception is likely to be quite important, but has only begun to be explored in higher animals (Collett and Harkness, 1982; Martinoya et al., 1988; Wagner and Schaeffel, 1991; Schaeffel 1994). In contrast, because of the salience of stereopsis for the appreciation of depth, and its applicability to human perception, binocular cues have dominated the literature on depth perception. Binocular cues require two eyes to be recognised (binocular vision), and are based on the premise that as our eyes are approximately six centimetres apart, they receive slightly different views of anything we look at. There are two exclusively binocular cues to depth: the vergence position of the eyes and binocular disparity (Howard and Rogers, 1995). Vergence is simply the angle of inclination of the eyes (see Figure 2). To extract distance information from this extra retinal cue the tension of the extra ocular muscles during fixation has to be measured. The resolution of such a mechanism, however, is limited (Foley, 1980; Collett and Harkness, 1982). Binocular disparity or binocular parallax, is a geometric fact—resulting from the difference in the relative position of images on the two eyes—and its sign and magnitude depends on viewing distance to a fixated target and the angle of vergence of the eyes (see Figure 2) (Arditi, 1986). Movement, of either the observer, “egocentric”, or the object, “exocentric”, brings in additional monocular and binocular cues that reveal depth information. For example, motion parallax is a monocular depth cue which refers to the fact that static objects at different distances from fixation move at different rates and directions on the retinae caused by motion of the observer (Rogers and Graham, 1979). 4 On the Perceptual Identity of Depth Vision in the Owl

A Far

Fixation g point a

Near D b

nodal point nodal point

B LEFT EYE VIEW RIGHT EYE VIEW

crossed

DISPARITY

un-crossed

Figure 2: Shown are eyes fixating a black dot at distance D. (A) Cues for stereoscopic depth are provided by points just proximal (grey dot) or distal (open dot) to the fixation point. These points produce binocular disparity by stimulating slightly different parts of the retina of each eye. (B) When this lack of correspondence is in the horizontal direction only, the disparity is perceived as a single solid dot. This phenomenon produces stereopsis, the perception of solid depth. Note also that the nearer an object is that is focused on, the more converged (crossed angle β) our eyes will be to each other. Conversely, the further away an object is, the eyes will be less converged (uncrossed angle γ). The angles subtended by the target points at the nodal points are called binocular parallax (angles: β, γ). The difference between binocular parallax and vergence angle (i.e., α - β or α - γ) directly measures absolute retinal disparity. The difference in absolute disparity of the far and near target forms relative retinal disparity which in turn is the stimulus for stereoscopic depth perception. Chapter 1: General introduction 5

Moreover, retinal disparity and motion parallax are closely related, since the successive viewings obtained by moving the head from side to side (through the interocular distance) provide the same information as the simultaneous views obtained by the two eyes with the head stationary. To summarise, in humans and animals the perception of three-dimensional visual space involves at least three interdependent mechanisms: (1) multiple sampling of the visual scene from either diﬀerent positions in space (binocular disparity) or time (motion parallax), (2) occulomotor adjustment of the optical system of each eye (accommodation) or both eyes (vergence) to maintain a sharp image (also known as extra ocular depth cues), and (3) exploitation of monocular cues such as occlusion, relative size, linear perspective, shading. It is also important to realise that binocular disparity and motion parallax (relative motion) are primary sources of visual information about the three-dimensional world. Their importance becomes apparent in the execution of visually guided tasks when subjects are free to move (Jones and Lee, 1981; Arditi, 1986).

1.3 Stereopsis

Stereopsis is the neural comparison of each eye’s image that allows binocular animals to extract information about relative depth of objects or surfaces. As a consequence this form of depth perception requires that each eye samples the same position in space (binocular vision) and enables the viewer to perceive a single image of solid three-dimensional space by integrating the information from the two separated eyes (binocular fusion). Essentially, stereopsis is based on the horizontal (not vertical; see Figure 2B) differences between the positions of similar image features of the retinal images to which I will refer to as binocular disparities. For stereopsis, as defined above, to be possible the brain has to pair features visible from the left eye with the corresponding feature as seen from the right eye’s vantage- point. Monocular features which project at the same perceived visual direction in the two eyes are called corresponding features or points (Tyler, 1993). In addition, the geometric information from the matched binocular features must be transformed into some estimate of binocular disparity. Thus disparity measurements inevitably require an animal to compare retinal images, and this means having binocular interactions at some level of the visual system. As a result, an animal with fixed eyes that wants to measure a wide range of disparities will need a substantial amount of its visual brain devoted to binocular interactions to cover even only a limited range of distances. Moreover, the lateral spread of binocular interactions emanating from a small area of the visual brain will be determined by both the animal’s spatial resolution and its disparity range. One means of limiting the necessary amount of binocular interaction 6 On the Perceptual Identity of Depth Vision in the Owl are convergent eye movements. With changing vergence, a relatively narrow band of disparities shifts in depth with the fixation point. In this case, binocular interactions can be limited to what are termed corresponding points on the two retinae. As can be appreciated from the section above, disparity in binocular animals can be computed under two different conditions (Collett and Harkness, 1982). In one, the eyes are fixed in the head and binocular disparity is calculated from the differences in horizontal position of the target images in the two retinae; in the other the eyes are converged to position the target onto a particular region of the retina, such as the fovea in human subjects and mammals such as cats and monkeys, then binocular disparity is given by the difference between binocular parallax and vergence angle. The geometry of the latter situation is shown in Figure 2. Thus an animal with fixed eyes needs a neural mechanism that only compares the two eye’s images, whereas an animal with vergence must agree to fixate the same target, which requires machinery for matching the images on the two retinae. Moreover, in humans and animals that can vary their angle of eye convergence, the retinal disparity values can be one of three classes (Richards, 1970): crossed (closer than fixation: negative disparity), uncrossed (farther than fixation: positive disparity), or zero disparity, depending on the position of the target with respect to the fixation plane. The detection of binocular disparity and its use in mediating depth perception requires not only binocular overlap but also the appropriate retinal specialisations and/or eye movements for binocular fusion (Schor, 1991). Binocular depth perception without fusion occurs in insects such as the praying mantis that have a fixed focal plane (i.e., their compound eyes lack accommodation) and cannot move their eyes relative to the head. Thus their prey striking behaviour is based on absolute depth perception (using the fixed vergence angle) rather than relative distance perception (using binocular parallax) (Rossel, 1983). Further, the magnitude and the sign of disparity between the images of an target signifies the absolute distance of that target from the animal. The ability to judge depth on this basis is referred to as range-finding, since it works like a range finder and does not require binocular fusion. A similar mechanism has been demonstrated to operate in toads (Collett, 1977; Collett and Harkness, 1982; Howard and Rogers, 1995). However, as I will emphasise throughout this thesis, stereopsis, is the percept of depth not depended on absolute disparities but rather on patterns of relative disparity over surfaces or between sets of objects as is described in Figure 2 (Howard and Rogers, 1995). The binocular combining of features in the images of the two retinae can involve two levels of processing called local and global stereopsis (Julesz, 1971; Richards and Kaye, 1974; de Valois and de Valois, 1980). In humans, these levels are dissociable since global stereopsis can be impaired while local stereopsis remains intact (Ptito et al., 1991). Local stereopsis refers to the assignment of a retinal disparity value to un- ambiguous matched corresponding points. Thus, some local (monocular detectable) Chapter 1: General introduction 7 pattern provides sufficient information so that there is no ambiguity which image of a single point in the left eye corresponds to an image in the right eye. Nevertheless, with more complex images, there may be ambiguity in determining which points in each eye’s image correspond to the same position in space. Resolving this ambiguity requires global stereopsis. A fairly effective method of testing global stereopsis is the use of Julesz random-dot stereograms (RDSs; Julesz, 1971). For those unfamiliar with stereograms, I include a method chapter, Chapter 2, describing this technique of creating stereoscopic depth. To summarise, stereopsis in humans and primates is an extremely acute mechanism for the detection of small differences in depth and requires a neural system that is sensitive to binocular information. In essence, for stereopsis to be possible, the visual nervous system in any frontal eyed binocular animal needs to perform two tasks with the information available from the left and right eyes. First, features visible from the left eye must be paired up with the corresponding feature in the right eye’s view. Second, the geometric information from the correct matched features must be transformed into some measure of binocular disparity.

1.4 Functions and evidence for stereopsis in animals

The recapturing of the third dimension through stereopsis assists in several types of spatial tasks: (1) stereopsis is very effective at revealing the presence of an object which are invisible to monocular inspection if its has a slightly different depth plane from the background (camouflage breaking) (Julesz, 1971; Pettigrew, 1990; Mckee et al., 1997), (2) the estimation of the relative position of surfaces with respect to some reference (usually the fixation point) which enables the detection of small relative disparities and hence 3-D shape (relative depth perception) (Collett and Harkness, 1982; Howard and Rogers, 1995), and (3) the estimation of absolute depth of a surface relative to the observer when combined with a fixed angle of vergence (by transformation of the convergence signal of the eyes) or motion parallax (Collett and Harkness, 1982; Richards, 1985; Howard and Rogers, 1995). Strong behavioural evidence of stereopsis comparable to that in humans has so far been found in only three mammalian species: macaque monkey (Bough, 1970; Sarmiento, 1974), domestic cat (Ptito et al., 1990) and Horse (Timney and Keil, 1999). Both local (Sarmiento, 1974; Harwerth et al., 1995) and global (Bough, 1970; Cowey et al., 1975; Harwerth and Boltz, 1979a,b) stereopsis have been demonstrated in monkeys, but stereo-thresholds in the range that are typical of normal human observers (Patterson, 1992) have been reported only by (Sarmiento, 1974). While there is behavioural evidence that falcons are able to use binocular cues to break camouflage (Fox et al., 1977), to date no study has demonstrated 8 On the Perceptual Identity of Depth Vision in the Owl relative depth perception by global stereopsis in birds. The probability of a local stereopsis mechanism in the frontal binocular field of the pigeon has been suggested by McFadden (McFadden, 1985; Mcfadden and Wild 1986), but requires experimental conformation (Martinoya et al., 1988). Finally, it is important to note that although stereopsis has been studied extensively in mammals such as cats and primates there is still no conclusive behavioural evidence that a non-mammalian species can use relative binocular disparity as the sole cue to detect differences in depth (Collett and Harkness, 1982; Howard and Rogers, 1995).

Figure 3: Schematic horizontal section (dorsal view) through the head of an great horned owl (Bubo virginianus). Redrawn from Erichsen, (1985). As a result of the frontal position of the eyes, binocular overlap is extensive. Binocular overlap permits a common segment of visual space to be viewed by the two eyes simultaneously. In the barn owl the optic axes diverges by approximately 62o (Martin, 1984). Chapter 1: General introduction 9

1.5 Binocular vision in the owl As noted in the previous section, the presence of binocular vision allows an animal to derive a three-dimensional visual world from distinct two-dimensional arrays. Because the presence of frontal eyes provides binocular overlap, binocular vision is probably most highly developed in frontal eyed birds which include falcons and owls (Casini, Fontanesi and Bagnoli, 1994). The large tubular-shaped eyes of adult barn owls have good optical quality (Scha- effel and Wagner, 1996) and are virtually fixed in the head in positions that are highly consistent from one individual to the next (Knudsen 1989). A schematic eye of the barn owl has been described (Schaeffel and Wagner, 1996) demonstrating an optical design that combines a low f/number (1.13) with large axial length (17.49 mm). Thus, despite their large size, the primary features of the barn owl’s eyes are image size and photoreceptor convergence to improve vision at dusk and dawn (Schaeffel and Wagner, 1996). Consequently, visual acuity can not reach the diffraction limit (Wagner and Schaeffel 1991) and data on retinal ganglion cell density predicted a moderate visual acuity of 7.9 cycles per degree (Whathey and Pettigrew, 1989). Moreover, the retinal topography showed a prominent temporal area centralis (located 24 deg temporal and 8 deg above the superior tip of the pecten; approximately 7 deg in diameter) and a moderate differentiated visual streak (Whathey and Pettigrew, 1989). Of all species for which comparable data are available, domestic cats seem most similar to barn owls with respect to visual acuity and retinal topography (Blake, Cool and Crawford, 1974; Hughes, 1975). The most apparent feature of the owls’ visual system is the frontal position of both eyes (Figure 3), which provides more binocular overlap than is usual in birds (Martin, 1984). Data on the actual shapes of uni-ocular and binocular retinal visual fields are available for only one owl species, the tawny owl (Strix aluco): the owls’ maximum binocular retinal field width (48o) is almost twice that of the pigeon (27o) (Martin, 1984). The owl’s binocular field is considerably smaller than that of man (120o) (Arditi, 1986). Maximum retinal binocularity occurs above the bill and the bill tip lies outside of the owl’s visual field (see Figure 3) (Martin, 1984). Barn owls have evolved an elaborate neural substrate (the visual Wulst) for binocular vision which is comparable with that found in mammals (the neocortex) (Medina and Reiner, 2000). Common features of these telencephalic regions include a high degree of binocular interaction, selectivity for stimulus orientation and direction of movement as well as binocular disparity (Pettigrew and Konishi, 1976a, Pettigrew, 1979). Binocular interaction refers to the phenomenon that single cells receive inputs from the same part of the binocular visual field of both eyes (Figure 4). Consequently, binocular cells form the neurophysiological basis for mechanisms that encode retinal disparity. Cells in the visual Wulst also appear to be arranged in ocular dominance columns, although these columns are seen only after monocular deprivation (Pettigrew, 10 On the Perceptual Identity of Depth Vision in the Owl

1986; Pettigrew and Gynther, 1989). The parallels in physiological functioning between the visual Wulst and visual cortex are quite striking when one considers that the anatomical organisation is very different, owls having a total decussation instead of the partial decussation of mammals at the level of the thalamic relay nucleus (Karten et al., 1973). Partial decussation allows information from each eye to be compared and is a prominent feature of binocular vision in mammals (Pettigrew, 1986). Nevertheless, partial decussation is also found in the owl and occurs at the level of the Wulst (Karten et al., 1973). Figure 4 shows a schematic representation of the anatomical organisation of the visual pathway that underlies binocular vision in owls (Pettigrew 1986). Functional parallels also extend to the phenomenon of plasticity, since binocular neurons in the Wulst are extremely sensitive to monocular deprivation (Pettigrew and Konishi, 1976b). In addition, when binocular vision is disrupted during a critical period of development the eyes fail to become properly aligned and monocular receptive fields of binocular cells in the optic tectum are misalignment (Knudsen, 1989). Thus, the neural development of binocular correspondence is innate and guides the alignment of the eyes in young owls. It has also been demonstrated that barn owls cannot accommodate independently in both eyes (coupled accommodation) and can use accommodation for near distance estimation (Schaeffel and Wagner, 1992; Wagner and Schaeffel, 1991). The near point of accommodation is variable dependent on the subspecies and ranges from 25 cm up to 10 cm (Howland et al., 1991; Schaeffel, 1994). Since the eyes of the owl are virtually locked in their orbits because of their size and move at most 1o it seems unlikely that owls converge to bring their fixation closer (Steinbach and Money, 1973; Knudsen 1989). Consequently, retinal disparity could code absolute depth as well as relative depth. In short, the visual system (i.e., eyes plus brain) of the barn owl could function as “model system” for avian stereopsis because of the following reasons: First, the retina of the barn owl possess a single and prominent area centralis (centred in the region of binocular overlap) together with a moderately differentiated visual streak, a situation comparable with domestic cats. Second, the pathways from the thalamic relay nucleus to the forebrain (”visual Wulst”) hemi-decussate so that corresponding inputs from the binocular visual field are brought to the same destination in the Wulst (Figure 4). Third, fused binocular vision is required for proper development of the owls’ visual system. Fourth, coupled accommodation indicates that information from the two eyes is not processed independently and may be linked to stereopsis. Fifth, much of the owls’ visual system is devoted to binocular visual processing. Moreover, the physiological properties of cells in the Wulst are very similar to those of cells in the striate visual cortex of mammals. Nevertheless, having stated all these features of the barn owls’ visual system, the final proof should come of course with the behavioural demonstration of stereoscopic abilities. Chapter 1: General introduction 11

Figure 4: Schematic representation of the organisation of forebrain visual pathways in the owl. Despite the total decussation of the optic nerve fibres, information from corresponding parts of the retina converge in the brain by means of a second decussation. Note that fibres projecting back to the opposite side of the brain arise from the representation in the thalamic relay nucleus of the retina temporal to the fovea (subserving the region of binocular overlap). This second crossing is partial and achieves a similar end result, at the final cortical destination (visual Wulst), to the hemi-decussation of optic nerve fibres as seen at the thalamic relay nucleus of mammals. The fovea for the frontal field is denoted by f, and limits of the binocular field by b (From Pettigrew, 1986). 12 On the Perceptual Identity of Depth Vision in the Owl

1.6 Outline

The key element to testing stereopsis in animals is a stereoscopic display that contains no monocular cues, even though an animal might try various strategies, such as closing one eye or making rapid head movements to obtain parallax information. A display devoid of these cues can be provided by Julesz random-dot stereograms (RDSs) in which the disparity information is camouflaged by a random matrix of thousands of minute dots (Julesz, 1971; Cobo-Lewis, 1996). Because of the complex nature of the method used to present the stereograms to the owls, a separate section of the method chapter (Chapter 2) is included— focusing on the generation and presentation of RDSs. In this chapter I also describe the techniques used to study depth perception from relative motion or motion parallax. Essentially, these techniques involved the use of a single random-dot pattern which was transformed either autonomously or with every movement of the animal’s head using a head tracking device. The experiments described in Chapter 3 have provided new information on the specificity of visual perception in the owl. First, an operant behaviour shaping technique was developed that prepared owls to be visually tested by images presented on a distant CRT monitor. Second, I found that owls can abstract the figure-ground organisation of computer generated random-dot images by testing two functions of vision that are thought to be involved in figure-ground segregation: (1) texture perception and (2) motion perception. Having established that random-dot patterns can be used to test visual capabilities in barn owls, I used the technique of time-multiplexed stereoscopic displaying to test whether binocular vision in owls enables stereopsis. Considerations about constrains imposed by sensory ecology have led to the claim, first made by Pettigrew (1986), that there is a high degree of similarity between the avian and mammalian neuronal algorithm that subserves stereopsis—the adopted computational strategy avoids feature extraction until information from both eyes has converged. The latter is known as global stereopsis and can be demonstrated by the use of random-dot stereograms (Julesz, 1971). While comparative psychology of sensory perception has incorporated behavioural measurements of global stereopsis in monkeys (see e.g., Harwerth and Boltz, 1979, Prince et al, 2000), cats (see e.g., Ptito et al., 1990), horses Timney and Keil, 1999) and falcons (Fox et al., 1977) it has failed to assess the perceptual judgement of relative depth through stereopsis. This basic function of stereopsis is investigated in Chapter 4 by examining discrimination-transfer performance—choosing between novel stimuli on the basis of a learned task in earlier discriminations—in barn owls trained to discriminate random-dot images. It is shown that the barn owl possesses stereopsis because this animal can determine directly the relative position of planar surfaces in space—relative depth perception—from disparity information alone and without recourse to egocentric translation of the head. Chapter 1: General introduction 13

In Chapter 5 it was hypothesised that when one specifically addresses those aspects of the owl visual system that set it apart from binocularity in primates, it is possible to determine the functional significance of stereopsis in the owl. By adopting this approach, I found that stereopsis is a robust and highly sensitive function of the owl visual system and I argue that its significance lies in the fact that the underlying neuronal algorithm enhances the discriminability of immobile targets (e.g., prey or tree branches) at low levels of illumination. While stereopsis has been found in a wide range of different vertebrate species, strong evidence of animals exploiting motion parallax as an independent monocular depth cue has been found only in insects (see for review Collett, 1996). There are, however, considerable similarities in the underlying computational theory of depth perception based on disparity and that based on motion parallax (see for review Howard and Rogers, 1995). Therefore, it seems likely that mechanisms, which have evolved to detect disparity and motion, have much in common, and this is likely to be reflected in the results of empirical studies of performance in the two cases. The discrimination- transfer experiments described in Chapter 6 clearly show that owls trained to categorise object and hole RDSs can perceive similar depth impressions from motion parallax displays (MPDs) without the need of additional training. This finding provides the most direct evidence in animals that perceptual knowledge derived through either stereopsis or motion parallax is closely related. Finally, Chapter 7, I will discuss the above described experiments by reviewing the main findings and their implications, and by proposing new experiments to further enhance our understanding of stereoscopic vision and cue interaction in the perception of depth. 14 On the Perceptual Identity of Depth Vision in the Owl 2 METHODS

. . . When the only tool one possesses is a hammer Every problem that one encounters tend to have the shape of a nail —Source unknown

2.1 Subjects and surgery

Four barn owls (Tyto alba): RG, JL, SL and VS, from the institute’s breeding stock, were cared for and treated according to the “NIH Guide for the care and use of laboratory animals” and were subject to regular inspections by the state veterinarian. Furthermore, all treatment was in agreement with the German laws on the protection of vertebrate animals. Birds were tamed by hand-rearing and could easily be handled. A T-stick, which also functioned as a perch, was used to transport the birds between the home cages (an indoor aviary) and the experimental chamber. Habituation to the apparatus took about 4 months for each owl. No attempt was made to reverse the owls’ nocturnal cycle. Training took place early in the morning or in the evening, 6 days each week. Normally, the owls were fed two to three 1-day-old domestic chick daily plus one mouse once a week to satisfy all the digestive and nutritive require- ments. During experimentation the birds were maintained at approximately 85% of their ad-libitum weight. The owls were rewarded with small pieces of chick muscle- tissue, approximately 2 grams in weight. Weighing of the owls took place daily. Under this procedure the owls were maintained in excellent health. All animals carried a head post on the head that had been fixed to the skull under anaesthesia (Ketamine, 20 mg/h/kg) at an earlier time. Surgery was performed aseptically and has been described in detail elsewhere (Wagner, 1993). During experimentation the birds always wore a spectacle frame that was attached to the head post (Wagner, 1991). Also attached was a small sensor when it was necessary to keep track of the owls’ head-movements. The spectacles had a velcro frame so that filters could easily be attached and exchanged. These filters were needed to correctly view the stereograms. 16 On the Perceptual Identity of Depth Vision in the Owl

2.2 Apparatus and Stimulus Presentation 2.2.1 Experimental setup The experiments were conducted in a specially designed experimental chamber with outer dimensions 230x120x220 cm, build of 20 mm ply-wood. The interior of the chamber was painted black and the front wall of the chamber was equipped

100cm

40cm infra red camera infra red infra red camera camera

STIMULUS viewing DISPLAY 35cm tunnel feeder feeder pecking bar left bar right bar perch perch slider

200cm slider 20

56 60 73

FRONT VIEW SIDE VIEW drawn to scale drawn to scale all dimensions all dimensions are in cm are in cm

Figure 5: Schematic front and side view of the experimental chamber showing the layout and dimensions of the manipulandum (left and right response-bar), feeder, perch and stimulus display (CRT monitor) for a viewing distance of 70 cm. Also shown are the positions of the two infrared cameras that allowed monitoring of the owls’ behaviour. with a single stimulus panel tangentially mounted onto one end of a 17 cm long viewing tunnel. This black tunnel minimised unwanted diffuse and specular screen Chapter 2: Methods 17 reflections. A diagram of the apparatus is shown in Figure 5. The manipulandum consisted out of two carbon response bars in combination with centrally placed carousel feeder (both custom made). The feeder contained one stepping motor that advanced a metal food dish (15x10x5 mm) with 12 oval shaped food cups. The access (triangle shaped; 2.5x3 cm) to the feeder was located in midway in the front part of the feeder. The stepping motor was controlled by an amplified audio signal (TTL-pulse) that originated from the audio-port output of a Silicon Graphics Inc. (SGI) workstation. Reinforcement delivery took max 400 msec. The two L-shaped response bars (2.5x3.5 cm) were horizontally separated by 14 cm. Their static mass, required to operate the micro switches of the response bars, approximated 30 gram. Correct pushing of the bars provided an audible click. The micro switches were connected to the serial mouse interface of a SGI-workstation via a small electronic circuit (LogiTech S/N: LI51400815). Algorithms were written to scan the mouse buffer and to generate a TTL-pulse. In this manner, the monitoring of the owl’s responses was fully automated and two infra-red cameras (one in front, and the other along side the perch) were used to observe the owls. During experimentation, the owls were placed on a T-shaped perch 12 cm in front of the feeder—both could be shifted along a 150 cm long horizontal optic-bench. The visual stimuli were computed with aid of an platform independent graphics library (OpenGL, version 2) on a fast SGI-workstation capable of rendering stereo displays. Used were either an SGI-Indy (100 MHz IP22 Processor; IRIX 5.2) or SGI-Octane workstation (175 MHz IP30 Processor, IRIX 6.4) depending on the amount of calculation required. A 17” cathode ray tube (CRT P22-phosphor colour monitor: ELSA 17H96; interlaced stereo mode resolution at 120 Hz: 1280x496 pixels) functioned as the stimulus presenting panel. By use of a time-multiplexed liquid crystal stereoscopic modulator (LCM: Tektronix SGS310), placed directly in front of the CRT, polarised stereograms could be created. For the measurements of head position a commercial real-time tracker was used, (miniBIRDTM : Ascension Technology Corporation), which contained a transmitter and, receiver. This system determined the head position by transmitting a pulsed DC magnetic field that was measured by its receiver (positional range:± 30 inch in X,Y and Z directions; positional accuracy: 0.18 mm) A small encapsulated sensor (1.8x0.8x0.8 mm) connected to a 25 cm long flexible cable (4 mm in diameter) functioned as the receiver. This sensor was marked with an orientation dimple and was fitted to the head post with the dimple pointing upwards. The transmitter (9.5 cm cube) was mounted onto the slide 10 cm behind the perch. Both the sensor and transmitter were connected to the miniBIRD electronics unit which made head position information from the receiver available (measurement rate 120 Hz) to a serial port (RS-232) of the Octane SGI workstation at a rate of 38400 Baud. An algorithm was written to read from and write to the serial buffer of the workstation. 18 On the Perceptual Identity of Depth Vision in the Owl

All algorithms were written in the C-programming language (ANSI-C) and were fully implemented in the OpenGL environment. To monitor the stimuli during experimenting, a second CRT was connected to the workstation via a video splitting system (RGB112, Extron Electronics). As a result, the stimulus sequences, reinforcing contingencies and data processing were controlled by a single workstation.

2.2.2 Head-movement calibration A complicating factor in head-tracking was the use of the head-tracking sensor because the animals were disturbed in their movements by the pull of the thick wire. For the owls, it took about one month of additional training to be completely comfortable with this device.

20 ] ] m c m [

c 6 B [

A n

16 o n i

t 4 o i i t s i o s 2

12 p o

p d 0 a d e a h

e 8 - 2 l h

a l t a

n - 4 c o i 4 t z r i

r - 6 e o V

0 H - 6 - 4 - 2 0 2 4 6 8 1 2 3 4 Horizontal head position [cm] Response time [sec] Figure 6: Typical head-movement trajectories (A) and head position traces (B) for one owl (SL) during a visual discrimination task. Recordings were made with the miniBIRD tracking system. The sensor was placed just above the owls beak (see Figure 10 on page 24). (A) Four two-dimensional trajectories (locus of movement on an Cartesian plot) of head-movements from viewing position to the response bars. (B) Head position traces as a function of time of the trajectories shown in A. Dotted line indicates time of stimulus onset. Note that there is a substantial variation in latency but there are no head-movements prior to the stimulus onset.

The tracking system was calibrated with a behavioural procedure. Azimuth, X, and Elevation, Y, and Distance, Z, of the target position relative to the null position—the centre of the perch—were related to the Cartesian position coordinates of the reference frame. The latter was defined by the physical orientation of the transmitter’s X,Y and Z axes. This introduced an ambiguity in determining the sign’s because the magnetic- field was symmetrical about each of the axes of the transmitter. The ambiguity in Chapter 2: Methods 19 position determination was eliminated through continuous tracking of the receiver position by the workstation. This required, however, resetting of the miniBIRD just before the workstation started to sample the position information. Calibration took place during the warm-up trials at the start of each experiment, and the output of the miniBIRD was recorded when the owl assumed stationary positions. These positions occurred when the owls: (1) attended to the observation stimulus, (2) pushed at the left bar, or alternatively, (3) pushed at the right bar. The vertical and horizontal component of each position was measured 10 times. The head position signals were re-adjusted off-line to the means of the above described stationary positions. The head-positions yielded by the calibration procedure provided a measure of the owls’ head movement relatively to the null position.

2.2.3 Stereogram presentation Used was the technique of time-multiplexed stereoscopic displaying to present stereograms to the animals (see also Hodges, 1992). Our time-multiplexed presenting

MONO MODE STEREO INTERLACED MODE

left image (uneven lines in stereo)

right image (even lines in stereo)

Figure 7: Generation of the stereo image using the time-multiplexed stereoscopic displaying technique. Mono mode: the left and right eye’s image are displayed in the upper and lower part of the CRT, respectively. Stereo interlaced mode: the left eye’s image is written to the odd scan lines and the right eye’s image to the even scan lines of the CRT monitor. system displayed left and right eye views of a stereogram simultaneously on a single CRT monitor run in stereo interlaced mode (Figure 7). Eﬀectively this means that one eye’s image is written to the even scan lines and the other eye’s image to the odd scan lines of the CRT monitor. During interlaced mode, the CRT was run at a 120 Hz refresh frame rate so that each eye’s image was refreshed at 60 Hz. However, in order for the animals to be stimulated dichoptically a special optical apparatus, to 20 On the Perceptual Identity of Depth Vision in the Owl deliver the correct image to each eye, is needed. Used were anaglyph and polarised displays (Hodges, 1992).

CRT monitor

RGB video OUT

LCM stereoscopic modulator SGI workstation

3W13 output

STEREOSCOPIC DRIVER driver output input output

vertical sync

composite sync horizontal sync front settings modulator

Figure 8: Connection diagram for the polarisation display system used to stimulate the animals dichoptically. When the time-multiplexed liquid crystal stereoscopic modulator (LCM) was placed in front of the CRT monitor and viewed in combination with a set of oppositely (left/right) circularly polarised ﬁlters the LCM transmitted and blocked the left and right eye’s images alternatively in synchrony with the refresh rate of the CRT. The vertical and horizontal synchronising output of the driver are only needed when the workstation is not capable to run the CRT monitor in stereo interlaced mode.

The polarising display system (dichoptic stimulation through polarisation separation), was based on a time-multiplexed liquid crystal stereoscopic modulator (LCM: Tektronix SGS310), mounted to the CRT monitor—run in interlaced mode. Figure 8 shows how the LCM was connected to the workstation. The LCM, that controlled the polarisation direction of any image passed through it, received input from a multi- function modulator driver (Tektronix SGS310) which in turn received the composite video signal of the SGI workstation as input. When viewed in combination with a set of oppositely (left/right) circularly polarised ﬁlters (OPF) the LCM transmitted and Chapter 2: Methods 21 blocked the left and right eye’s images alternatively in synchrony with the refresh rate of the CRT.

Table 1: Extinction Ratios Set1 Vertical Red Red White White Position [ratio] [%] [ratio] [%] Top 35 2.8 11.4 8.8 Middle 26 3.9 11.2 9 Bottom 24 4.2 10.6 9.4

A factor that affects the viewing of the polarised display is inter-ocular cross talk between the eyes. The amount of inter-ocular cross talk is determined by: (1) the amount light transmitted by the LC shutter in its off or closed state; (2) phosphor persistence; (3) and vertical screen position of the images. The correlation of cross talk with colour is derived from the fact that the P22 red, green, and blue phosphors used in the CRT monitor do not decay at the same rate. The effect of vertical screen position is caused by different phosphor decay residuals at different screen positions when the two fields are switched.

Table 2: Extinction Ratios Set2 Vertical Red Red White White Position [ratio] [%] [ratio] [%] Top 40 2.5 8.9 11.2 Middle 29 3.5 8.6 11.6 Bottom 21 4.6 7.9 12.6

Cross talk was measured by the extinction ratio (Yeh and Silverstein, 1990): the ratio of luminance of the correct eye image to the luminance of the unwanted ”ghost” from the image intended for the opposite eye. Tables 1 and 2 list the extinction ratios of red and white images at three vertical positions for two sets of polarised filters, respectively. The higher the extinction ratio, the less the degree of inter-ocular cross talk. Percentages indicate the amount of luminance that is captured by the blocked eye. This way of measuring cross-talk takes into account any contribution 22 On the Perceptual Identity of Depth Vision in the Owl by phosphor persistence, as well as leakage during the closed phase. The amount of cross-talk was even higher for the stimuli used in the owl experiments. For both sets each eye received approximately 17% of the others eye image. As can be seen from Table 1, the extinction ratio of a white stimulus presented in the centre of the CRT equalled maximally 11.4. The anaglyph display system (dichoptic stimulation through colour separation), presented the left- and right- eyes image with complementary colours (red/green, respectively) and then superimposes both eyes views on the CRT monitor—run in interlaced mode. When viewed in combination with a set of red and green filters that matches the colours on the CRT, the eye covered with the red filter will see only the red image while the eye covered with the green filter will see only the green image. However this is only the case when the coloured dots are projected onto a darker background. What is particularly useful about anaglyph stereograms is that dramatic changes in depth can be created by changing the background luminance. For example, by switching from a black to white background one can reverse the depth percept. Note γ-correction was applied to produce a linear relationship between luminance and the colour, or grey levels specified by the computer system (see section 2.4.3 on page 30). For a centred red or green stimulus, the extinction ratio equalled 1.5 and 6.2, respectively.

2.3 Behavioural procedures

2.3.1 Initial operant conditioning

After the owls learned to eat from the feeder (magazine training) they were auto- shaped to push the response bars. A single push on the correct bar (either left or right) was reinforced with one piece of meat. To avoid the occurrence of a preference toward a single bar (bias), they were rewarded only when emitting a bar push on the bar opposite to the last selected bar that led to the presentation of a reward (reciprocal operant conditioning). The more difficult aspect of operant conditioning was to teach the owls to first focus their attention to the distant stimulus panel before they were allowed to push one of the response bars. In order to let the pre-conditioned animals focus their attention towards a 70 cm distant computer monitor an “observation” stimulus, Sz, was used in the form of a dim rectangle Chapter 2: Methods 23 borderline (10 mm wide) covering the width of the screen and provided mesopic illumination of about 0.1 cd/m2 (measured at viewing distance). The sequence of events during reciprocal operant conditioning in combination with the observing response are illustrated by Figure 9. When the subjects were confronted with the observation stimulus, Sz, they were required to look in the direction of the monitor in a straight-upward position. Only when the screen was completely darkened a push response was allowed. When the animals responded during the Sz presentation the computer screen was blanked (2 cd/m2; measured at viewing distance) and the next Sz presentation was delayed for maximally 15 seconds. Only when Sz was removed, the animals were allowed to respond. If, however, the wrong key was selected Sz was displayed again (see Figure 9). After 1 rotation of the feeder, training was interrupted in order to refill the feeder. Such a confined sequence of trials represents one session. The refilling took usually 2-3 minutes, during which the owls were set aside. Normally, one training day consisted out of 4-8 sessions during which each animal received between 44-88 pieces of meat, because one slot was always kept empty.

Observation Stimulus off

Right Bar Push

Left Bar Push

Food Presentation TIME COURSE

Figure 9: Schematic representation of the initial operant conditioning procedure. Shown are traces of the “observation” stimulus onset, bar selections and reward presentations as function of time. Reciprocal reinforcement forced the animals to alternate between the left and right response bar. See main text for a more detailed explanation. 24 On the Perceptual Identity of Depth Vision in the Owl

2.3.2 Discrimination training and testing Subsequently, the birds were trained and tested in a two phase procedure described below. Prior to training or testing, each animal was placed on a perch in the experimental chamber for about 3-5 minutes under photopic illumination. All experiments were performed under dark room conditions.

itor mon ulus stim spectacle frame + wired sensor

nal latio ans t tr men li ove ne of sight d m hea

der y fee spla g di +Y rizin pola variable

h magnetic field perc standard transmitter

Figure 10: Illustrative drawing of the stimulus presenting system and head-tracking system. To control for stereopsis the owls wore spectacles and viewed the stimuli through a set of differently polarized filters. That is, a time-multiplexed polarising liquid crystal display modulator (LCM) in front of the stimulus monitor ensured dichoptic stimulation through polarization separation. To control for motion-parallax head movements were tracked in real-time by use of a small- wired sensor in combination with a magnetic-field generator; located just behind the perch. That is, the head-tracking sensor system measured the owl’s position and orientation on-line. Owls standing on a perch were trained to fixate the distant stimulus monitor and were required to reliably operate the response bars with their beak. A push on either the left response-bar (associated with the standard), or alternatively, the right response bar (associated with the non-standard ) could be reinforced with a reward made available from the feeder. Chapter 2: Methods 25

SCREEN BLANK2 SEC NO REWARD

left SCREENBLACKOUT NON STANDARD BAR TRIALABORTED < 100 msec STIMULUS PRESS S L right

OBSERVATION T1 STIMULUS T2 STIMULUS ON-SET 5-30 sec 1-30 sec

left STANDARD BAR STIMULUS PRESS S right R

SCREEN BLACKOUT + REWARD Figure 11: Flow diagram of the sequence of trial events during the training of the basic behavioural discrimination task: a two-alternative choice procedure. Each trial started with the onset of the observation stimulus. When the animal oriented itself in the direction of the screen, which otherwise was kept dark, it was presented with the observation stimulus and a randomly changed interval of maximal 30 sec in duration (interval T1) occurred before stimulus onset. The animals were allowed to respond as quickly as possible, but had to keep their head motionless just before stimulus onset. However, when the animals responded to quick (prior to, or just 100 msec after stimulus onset) or did not respond within 2 sec, after stimulus onset the trial was aborted by blacking-out the screen. Choosing the incorrect response bar after stimulus onset resulted in blanking the screen for 2 sec (negative reinforcement) followed by a delay of maximal 30 sec in duration (interval T2); a correct choice was rewarded with food access followed by a blackout (positive reinforcement).

In phase 1 (training of the discrimination task), the animals had to learn to correctly associate each image of a stimulus pair with one of the two response bars (SL or SR, see Figure 10) and were rewarded only for a correct response (100% reinforcement). The images of a single stimulus pair were of two types: a standard, and non-standard and had to be associated with the left and right response bar, respectively. The way in which the stimuli were configured has been described in section 2.4 on page 27. Data 26 On the Perceptual Identity of Depth Vision in the Owl were collected in a successive viewing of a balanced quasi-random sequence of images belonging to a single stimulus pair. Such a sequence was pre-determined and no more than three consecutive trials presented the same image. Consequently, the owls had to compare each image to their memory of the standard and then had to decide if they were looking at the standard or non-standard image. With the stimuli presented in this manner, 100% correct represents perfect discrimination and 50% chance responding. The sequence of trial events during discrimination training are described in Fig- ure 11. To avoid the development of side preferences during training (due to the high probability of getting a reward just by chance) a correction procedure was employed. Two consecutive incorrect responses were followed by repeating the presentation of the same stimulus until the owls responded correctly. However, only the response to the presentation prior to the correction procedure was considered in the data analysis. In phase 2 (psychophysical analysis), psychophysical testing began after each bird had reached criterion—reliable performance: 85% correct for 70 consecutive trials; P (X ≥ 85%) .0001 independent binomial probability— and rewards were given in only 70% of the trials; independent of whether the response was correct or not (un- differential reinforcement). Both (1) the method of constant stimuli and, (2) adaptive tracking (the method of limits) were applied to measure the animals sensitivity to a specific visual cue (Niemiec and Moody, 1995).

2.3.3 Measurement of perceptual categorisation Whereas the method of constant stimuli and the method of limits provide information about sensory acuity and the limits of resolution of the tested sensory system, they stop short to assess perceptual judgement (Stebbins, 1995). To overcome this problem, I used tests of discrimination transfer—choosing between novel stimuli on the basis of a learned task in earlier discriminations. In this way one can address questions such as: Can owls make judgements about relative depth when presented with RDS?, Can owls categorise RDSs stimuli? etc. The proper asking of the question (that is, the proper reinforcement contingency to stimuli that differ) in combination with the appropriate design of the discrimination transfer will give us some better understanding of animal perception. In these kinds of experiments it is important not to lead or confuse the animals. To avoid leading, the animals were un-differentially reinforced during transfer tests. In addition, to avoid confusion, the judgements that the animals had to make about visually stimuli have to be well within the limits imposed to their sensory systems that can only be defined by threshold measures using the method of constant stimuli or the method of limits. Chapter 2: Methods 27

2.4 Discrimination paradigms and stimuli

2.4.1 Basic discrimination paradigms The two employed discrimination paradigms, paradigm I and II, were based on the phenomenon that perceptual groupings help to segregate objects and their surrounds in response to diﬀerences in texture and/or luminance, motion and, depth cues into “ﬁgure” and “ground” (Nakayama et al., 1989). An illustrative example of stimuli used in paradigm I and II is shown in Figure 12.

Stimulus S Stimulus S L R

Paradigm I

standard non-standard

Paradigm II

standard non-standard

Figure 12: Shown are two pictorial drawings of stimulus pairs used in discrimination paradigm I and II, respectively. The images of each stimulus pair are of two types: a standard image (associated with SL) and a variable non-standard image (associated with SR). In I the ground- only image was used as the standard and the figure-ground image could be varied by changing the amount of grey dots in the figure region. In II the hole configured image functioned as the standard and the object images could be varied by changing the visual cue that signalled the difference between figure and ground. 28 On the Perceptual Identity of Depth Vision in the Owl

In paradigm I, one image of each pair was composed of two distinct areas, a surround (“ground”) and a smaller inner region (“figure”) visible through either monocular or binocular discriminative cues, while the other stimulus consisted of a homogeneous random-dot pattern (“ground” only); viewing distance: 70 cm, dot size: 8.8x6.3 arcmin; ground size: 120x125 dots; figure size: 50x115 dots; luminance grey/black dots: 1.6 cd/m2 / 0.0 cd/m2; percentage of grey (and black) dots: variable in figure, and 50% in ground region. In paradigm II, the two RDSs of each pair were composed of two distinct areas and were viewed at a distance of 150 cm. However, the depth relationship between figure (150x150 dots) and ground (450x450 dots) regions differed between the two stimuli. The size of a single dot subtended 1.0x1.0 arcmin. The RDSs are described in more detail in section 2.4.2 of this chapter. The conceptual difference between the two paradigms lies herein that in paradigm I the owls had to discriminate pure random-dot patterns (ground-only) from random-dot patterns that contained both a figure and a ground region (figure-ground stimuli)— signal versus no-signal discrimination—, whereas with paradigm II every pattern was a figure-ground stimulus—signal versus different-signal discrimination. Thus, the discrimination in paradigm II has to become even more specific than in paradigm I because the differences between the images are not found in the presence or absence of a visual cue. Instead the animals have to categorise between different configurations of the same visual cue.

2.4.2 Random-dot stereograms The key element to testing stereopsis in animals is a stereoscopic display that contains no monocular cues, even though an animal might try various strategies, such as closing one eye or making rapid head movements to obtain parallax information. A display devoid of these cues is provided by Julesz random-dot stereograms (RDSs) (Julesz, 1961) in which the disparity information is camouflaged by a random matrix of thousands of minute dots. For those unfamiliar with random-dot stereograms, I have included a schematic drawing (Figure 13), describing this technique of creating depth as it was first introduced by Julesz (1971). Note, however, that the manner in which Julesz constructed his RDS slightly differs from the construction I used, as described below. Retinal disparity, r —induced by a horizontal shift of the figure relative to the ground in one eye’s image (half-image), combined with an identical shift (but in the opposite direction) of the corresponding elements in the other eye’s image—was calculated according to Cormack and Fox (1985) using an interpupillary distance of 45 mm. The reader should note, however, since r is a relative measure the shifted inner region of the RDS may be seen as an “object” that lies in front of the surrounding Chapter 2: Methods 29 background or is seen as a ”hole” revealing a surface that lies behind it. The direction of displacement relative to the surrounding plane (i.e., sign of disparity) was taken to be negative in case of a hole RDS and positive in case of a object RDS. Note also, the depth plane of the stimulus displaying panel (i.e., the mask of the CRT screen) was arbitrary taken to be zero retinal disparity. Also the dots were anti-aliased by applying an in-build algorithm of the OpenGL library. Thus in principle, the change in disparity could be smaller than the dot size without causing de-correlation disturbances (see also Cobo-Lewis, 1994). Thus, the induced retinal disparity could be varied in steps smaller or related to the dot size and ranged from zero up-to ±120 arcmin.

LEFT EYE HALF-IMAGE RIGHT EYE HALF-IMAGE

Figure 13: A random-dot stereogram (RDS) and its structure. The lower part schematises the construction of the RDS shown in the upper part. Both half-images of a RDS consist of a uniform, randomly generated texture of equal amounts of black and grey dots. The enclosed area by the white square in the left eyes half-image is displaced to the left creating the right eyes half-image. The gap left at the right side of the enclosed area is ﬁlled with random dots. When each half-image is presented to the correct eye, the shifted square would be seen ﬂoating above the background (adapted from Julesz, 1971).

Two types of stereograms were used, dynamic and static RDSs, and both were presented using the technique of dichoptic stimulation through either polarisation or colour separation, as described above, and are referred to as polarised and anaglyph RDSs, respectively. With the computer in stereo interlaced mode, half-images were 30 On the Perceptual Identity of Depth Vision in the Owl presented at 120 Hz, alternating in the odd and even scan lines; mounting to a half-image frame rate of 60 Hz. At the viewing distance of 1.5 m, each random-dot subtended 1x1 arcmin irrespective of the displaying technique and all RDSs were segmented into two distinct areas a large ground and a smaller inner figure region. The polarised RDSs consisted of two half-images each containing a random-dot matrix of equal amounts (50%) of grey and black dots with a luminance of 0.36 cd/m2 and 0.0 cd/m2, respectively. Anaglyph RDSs consisted of two half-images: one contained a random-dot matrix of equal amounts (50%) of red and black dots the other equal amounts (50%) of green and black dots. Luminance of the red and green dots equalled 0.15 and 0.67 cd/m2, respectively. Luminance of the non-coloured black dots was set .00 cd/m2. Luminance was measured at the viewing distance through the LCM plus the polarised filter or through the coloured filters by averaging over at least 70 dots, using a Minolta luminance meter (LS-100). During the presentation of static RDSs, the ground of each half-image filled a region of 450 x 450 dots; containing 202,500 dots during each half-image frame with a dot density of 3600 dots/deg2. Owing to technical limitation, the dynamic RDS dots subtended 1x2 arcmin and builded a ground of 450x225 dots; containing 101,250 dots during each half-image frame with a dot density of 1800 dots/deg2. In dynamic RDSs, the computer updated each half-image every 30 msec. The figure region of static and dynamic RDSs comprised of: 150x150 and 150x75 dots, respectively.

2.4.3 Monitor calibration Gamma correction was applied to produce a linear relationship between luminance and the colour level specified by the computer. During this procedure, the luminance of the CRT monitor was calibrated at 70 equally spaced slots out of the 256 slots of the colour map with a Minolta luminance (LS-100) meter positioned at the viewing distance. The resulting calibration curve reflected the γ-correction of the used CRT monitor. For a desired intensity value, the interpolated calibration curve was evaluated inversely and the closest colour-map slot was used. A high level of spatial precision was achieved by use of two procedures: anti-aliasing (see section 2.4.2) and spatial calibration. Spatial calibration involved the creation of a look-up table that converted desired visual directions into screen coordinates. During the spatial calibration procedure, a translucent 25-by-25cm grid—filled with 625 squares created by 1 mm thick black lines—was mounted 4 mm in front of the CRT mask. An observer positioned a bright white dot to be coincident with specified Chapter 2: Methods 31 intersections in the grid while viewing through the luminance meter at the viewing distance. A dot was considered to be aligned when the measured luminance level was lower than .00 cd/m2. When a dot was aligned, its coordinates were recorded. The procedure was repeated for misaligned dots until interpolated positions of all dots were correct (about 200 explicit settings). During experimenting the translucent grid was removed and its former location defined a virtual plane onto which stimuli were projected. The calibrated area was 9.5x9.5o

COMPUTER SCREEN

Figure 14: Illustrative drawing of the stimulus display presenting the motion-in-depth stimuli. An owl wearing spectacles is drawn viewing the stimulus display. Shown are two classes of stereoscopic motion stimuli: hole (A) and object (B) motion display. Note the stereoscopic images of the object and hole stimuli moved along a diagonal line relative to the owls midline, and in opposite directions (see Regan, 1993). 32 On the Perceptual Identity of Depth Vision in the Owl

2.4.4 Stereoscopic motion

To facilitate discriminative learning during the training of paradigm II a monocular discernible cue “structure from motion” (Regan and Beverley, 1984) was used in addition to the binocular disparity cue of the static RDSs. This was achieved by inducing translational motion of the boundaries of figure relative to the ground in one eye’s image, while leaving unaltered the corresponding elements in the other eye’s image. As a result, the translational motion of the figure boundaries were defined by changes in binocular disparity over time. This type of motion display is called stereoscopic motion or motion-in-depth (Julesz, 1971; Cumming and Parker, 1997; Regan, 1993). In this way the owls were taught to detect a stereoscopic form moving in front of (object configuration, motion only in the left eye), or alternatively, behind (hole configuration, motion only in the right eye) a non-disparate static background. For all motion displays the coherent motion consisted of a sequence of discrete horizontal displacements of the figure region dots at a frame-rate of 60 Hz. The displacements had a step size of 3 dots per frame (equal to a speed of 4 deg/sec) and oscillated between 9 and 27 dots; representing a retinal disparity of ±18.6, and ±35.2 arcmin, respectively. Consequently, depending in which eye the motion occurred, the owls were presented with either an object that moved back and forward, or alternatively, a hole that decreased and increased over time. Also, the absolute direction of the stereoscopic figure region deviated from the owls midline and followed opposite directions when compared between the two stimulus classes—object versus hole—as is illustrated in Figure 14 (see also Regan, 1993). Note however, as opposed to the motion-in-depth stimuli used by Julesz (1971) for each new disparity the same set of random-dot patterns were used. In this case there existed a correlation between successive patterns presented to either eye that induced structure-from-motion. The latter is a monocular detectable cue, as was outlined above.

2.4.5 Kinematograms

Two factors that have the most utility in specifying surfaces are motion (or common fate) and global stereopsis (binocular disparity) (Nakayama et al., 1995). In humans, regions of common motion in random-dot patterns lead to the vivid emergence of surfaces and these random-dot kinematograms (RDKs) can be regarded as the motion domain counterparts of RDSs (Frost et al., 1994). The compelling visual percept induced by RDSs and RDKs are tightly linked to depth vision because it is thought that surface representation forms a critical stage between the earliest pickup of visual information and later stages, such as object recognition (Nakayama et al., 1995). Chapter 2: Methods 33

To produce kinematograms, typically a small circumscribed region of dots in the centre of a field of random-dots—figure—is moved coherently in one direction while keeping the surrounding region of dots perfectly still—ground. It is thought that the perception of these pure motion stimuli is based on the ability of the visual system to integrate a set of seemingly independent motions into a single coherent percept— structure-from-motion; Regan and Beverley (1984). Moreover, RDKs can be configured in two basic ways that are differentiated through either a dynamic boundary (separating the moving from the non-moving dots) that moves coherently with the figure, or alternatively, a boundary that remains at the same position relative to the ground (see Figure 15 for explanation). These different configurations of RDKs reveal an important aspect of the visual world: surfaces can occlude other surfaces. At the leading edge of the moving object there is occlusion of the ground, while at the trailing edge there is dis-occlusion. Conversely, at the leading edge of the hole there is dis-occlusion while at the trailing edge there is occlusion. Furthermore, the remarkable unimpaired percept of hole and object RDKs reveal that the visual system has adopted strategies to deal with this real world constraint (occlusion) because the amount of occlusion in these RDKs varies greatly.

A B

Figure 15: Shown are two basic patterns of kinematogram images configured either as “object” (A) or “hole” (B). When the object configuration is shown to human observers they invariably report seeing an object move over a more distant background pattern. The hole configuration is being seen as a plane surface with a window revealing a more distant surface. Note that kinematogram A and B are essentially equivalent to the object and hole RDSs, respectively. The white arrows indicate the direction of movement of the small circumscribed region in the centre of image (After Frost et al., 1994). 34 On the Perceptual Identity of Depth Vision in the Owl

In all experiments the RDKs employed consisted of an image sequence in which each individual frame was a random-dot pattern with equal amounts (50%) of grey and black dots. Figure and ground were made visible by changing, frame for frame, the horizontal position of the dots of a small circumscribed region (ﬁgure: 150x150 dots) in the centre of a larger ﬁeld (ground: 450x450 dots). At the viewing distance, 1.5 m, the grey and black dots subtended 1x1 arcmin, with a luminance of 0.36 cd/m2 and 0.0 cd/m2, respectively. For all moving stimuli the coherent motion consisted of a sequence of discrete displacements. The leading edge of the dot displacement was always initiated at the same position near the centre of the screen. The dots were shifted rightwards by 3 dots each frame. The number of frames per second was varied from 10 - 60 in steps of 10, giving rise to a maximal horizontal velocity of 3 deg/s.

2.4.6 Motion parallax stimuli To study the perception of depth from motion parallax a similar random-dot technique was used as described by Rogers and Graham (1979) with human subjects. Essentially their technique involved the use of a single random-dot pattern, viewed monocularly, which was transformed—thereby generating relative motion on the retina—with every movement of the observer’s head. When the observer’s head is stationary, there are no cues available in these kind of interactive motion displays that allow depth judgements. I have used Rogers and Graham’s (1979) motion parallax displaying technique to simulate the random-dot patterns of relative motion that would be produced by a real three dimensional surface during active movements of the subject’s head. In this sense motion parallax displays are interactive stimuli as opposed to the kinematogram displays (described above) which do not require active movement of the subject. To do this, a single, random-dot pattern of equal amounts of black and grey dots 450x450 dots, was systematically transformed (in two dimensions: vertical and horizontal) with each movement of the owl’s head. This was accomplished by tracking the movement of the owl’s head by use of a head-tracking device as described on page 18. Because the head-tracker continuously provided the pattern generating workstation with the horizontal and vertical head position coordinates, parallax motion was continuous and exactly in step which each movement of the animal’s head. For example, as the owl moved its head from left to right and back, a single horizontal band of dots would move in the same direction across the stimulus display to simulate a surface that is further from the owl than the non-moving parts of the display (Figure 16). The opposite situation exists—the dots move in the opposite direction relative to the owls’ Chapter 2: Methods 35 head movement—when a surface is simulated that is further from the owl than the non-moving parts of the display. However, to create motion parallax displays that resembled “object” or “hole” depth conﬁgurations, the edges of the transformed region were made visible by making use of occlusion in the same way as it was applied in the RDKs stimuli. Therefore, the transformed region only contained 150x150 dots. In case of a parallax motion display simulating a object the transformed region of dots moved in the opposite direction relative to the head motion, whereas the window conﬁguration was created by a parallax motion display that moved in the same direction as the observer.

Figure 16: Horizontal motion parallax transformations. When the square-wave surface depicted by A (shown under a viewing angle such that its three-dimensional structure can be appreciated) is viewed by an owl that moved his head side-to-side, relative motion—measured by a head tracking device—is created between the surface features at diﬀerent distances. This is motion parallax. The lower part B displays how the random-dot pattern on the stimulus display was transformed in synchrony with the head movement. In order to simulate a plane going into the stimulus display the direction of pattern transformation (white arrows) was made identical to the movement of the head (black arrows). The ratio between the size of the white and black arrows is a direct measure for the gain used, here 1/10. Note that only the area between the two stippled vertical lines was made visible to the observer by superimposing a random-dot pattern that occluded the leading and trailing edge of the moved horizontal band of dots (after Rogers and Graham, 1979). 36 On the Perceptual Identity of Depth Vision in the Owl

In a real three dimensional surface, the amount of parallax of the surface relative to its background is directly proportional to the amount of relative depth in that surface. Hence by modulating the gain of the amplitude modulation, more or less relative motion could be introduced into the display for the same extend of head movement. In all experiments the animals viewed the stimuli at a distance of 1.5 m and were allowed to move their heads freely. At viewing distance the grey and black random-dots subtended 1x1 arcmin, with a luminance of 0.36 cd/m2 and .00 cd/m2, respectively. The gain was set at 1/10, thus a head movement of 25 mm resulted in a random-dot pattern transformation of 2.5 mm. Chapter 2: Methods 37 38 On the Perceptual Identity of Depth Vision in the owl 3 DISCRIMINATIVE LEARNING AND THE SPECIFICITY OF VISUAL PERCEPTION

. . . Nothing is greater or little otherwise than by comparison. —Johnathan Swift, Gulliver’s Travels

Abstract Whether owls can be trained to discriminate computer generated random-dot patterns purely on the basis of their figure-ground organisation is an open question. Here I investigate this question by (A) providing an operant shaping technique that prepared four barn owls for behavioural measurements employing a remote computer display (Experiment I) and (B) using the random-dot technique together with tests of discrimination-transfer (Experiment II). Tested were two functions of vision that are thought to be involved in figure-ground segregation: (1) texture perception and (2) motion perception. The computer displays consisted of patterns of randomly positioned black and grey dots, that differed either in their position, textural organisation, or common fate (motion). The rapidness with which the owls learned to discriminate varied between the different individuals and depended heavily on the visual function tested. The here described experiments have been instructive in four ways. First, Ex- periment I has provided an adequate operant shaping method that prepared barn owls to be behaviourally tested with random-dot patterns that were displayed on a CRT screen. Second, Experiment II provided behavioural data that clearly demonstrated that owls can abstract figure from ground in computer displays of random-dot patterns. Third, signal detection analysis of the measured psychometric curves revealed a consistent response criterion for stimuli above or near threshold level, indicating a high degree of stimulus control. Fourth, the transfer tests provided evidence for generalisation discrimination in owls. 40 On the Perceptual Identity of Depth Vision in the owl

3.1 Introduction In vertebrate animals one of the primary functions of vision is to provide information about the three-dimensional relationships of objects in their natural settings. To obtain this spatial information, however, these animals have to rely on the two-dimensional images projected on the retinae. In turn retinal images arise from the light reflected by the surfaces of the objects that constitute the visual scene (e.g., Gibson, 1979). Thus, a process that must occur in any visual system to appreciate the depth relationships of objects is the segmentation of the visual scene into distinct surfaces. This process has been termed “figure-ground” segregation and many factors can contribute in specifying a surface, including differences in texture, depth, and motion between an object and its surround (Julesz, 1971; Regan and Beverley 1984; Nakayama et al., 1989). The experiments described in this paper were designed to answer two questions. First, can owls be trained to discriminate images that are presented on a remote computer display. Second, what kind of visual cues can be used to serve as useful inputs to figure-ground segregation. The rationale behind these two questions is based on two observations. First, the majority of studies focusing on visual discrimination in behaving owls have measured only visual thresholds and thus tell us merely about the limits of visual sensitivity (for review see Martin, 1990). Consequently, little is known about how owls classify and structure their visual world. Second, electrophysiological studies have revealed that there is a close parallel between functional attributes (e.g., disparity, motion, spatial frequency) of neurons in the visual Wulst of the barn owl and those described in the striate cortex of mammals (Pettigrew and Konishi, 1976a,b; Pettigrew, 1979; Cooper and Pettigrew, 1979; Wagner and Frost, 1994; Nieder and Wagner, 1999). Common features of these telencephalic regions include a high degree of binocular interaction, selectivity for stimulus orientation and direction of movement, as well as binocular disparity. These findings suggest that the barn owl’s visual processing capabilities provide them with excellent information for segmenting surfaces from a background of similar textures and patterns. The random-dot technique, as it was introduced by Julesz (1971), has been instrumental in showing that human and, animal vision does in fact exploit texture, depth, and motion cues to convey surface information (see e.g., Frost et al., 1988; Nakayama et al., 1995). For example, regions of coherent motion in random-dot patterns lead to the sudden emergence of surfaces from these kinematograms (RDKs). To produce kinematograms, typically a small circumscribed region of dots in the centre of a field of random-dots (figure) is moved coherently in one direction while keeping the surrounding region of dots perfectly still (ground). It is thought that the perception of these pure motion stimuli is based on the ability of the visual system to integrate a set of seemingly independent motions into a single coherent percept (structure-from-motion; Regan and Beverley, 1984). Moreover, RDKs can be configured in two basic ways that are differentiated through either a dynamic boundary (separating the moving from the Chapter 3: Discriminative learning & visual perception 41 non-moving dots) that moves coherently with the figure, or alternatively, a boundary that remains at the same position relative to the ground. When presented to human subjects they invariably report seeing a surface moving over a more distant background texture in the former case (object RDK), and a plane surface with a hole revealing a more distant surface in the latter case (hole RDK) (Frost et al., 1994). These different configurations of RDKs reveal an important aspect of the visual world: surfaces can occlude other surfaces. In turn, the remarkable unimpaired precepts of hole and object RDKs reveal that the visual system has adopted strategies to deal with this real world constraint because the amount of occlusion in these RDKs varies greatly (Frost et al., 1994; Anderson and Nakayama, 1994). To study visual perception in the owl, I assessed the usefulness of texture and motion cues in specifying visible surfaces. For this purpose four owls were presented with a succession of different random-dot patterns including RDKs that remained constant only in their figure-ground organisation. To test whether the owls were capable of extracting this feature on the basis of visual texture perception or visual motion perception, they were presented with novel patterns that could be distinguished only on the basis of their figure-ground organisation. The described behavioural procedures and discrimination paradigms provided the necessary background for studies with the specific aim of obtaining psychophysical measurements of visual capacities in the barn owl and of determining the nature of the visual cues involved—parts of which already have been published (van der Willigen et al., 1997, van der Willigen, Frost and Wagner 1998).

Experiment I: Operant Conditioning

This experiment was undertaken to provide an operant shaping technique that would prepare owls for behavioural measurements of visual perception using a CRT screen.

3.2.1 Methods Animals, apparatus and procedures: A detailed description of animal treatment, the behavioural apparatus and procedures is given in Chapter 2.

3.2.2 Results and Discussion During the auto-shaping of the bar-pushing operant response, data were collected from all four owls. Normally, one training day (i.e., a single experiment) consisted out of 4-6 sessions. A session commenced until the feeder that could deliver a maximum of 12 rewards, was empty. The average duration of a session ranged from 2.5 to 4 42 On the Perceptual Identity of Depth Vision in the owl min. The number of recorded pushing responses per session ranged from 20 up to 40. All animals developed stable patterns of responding after 12-20 sessions. t f

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10 10 m20in 30 40 50 The more difficult aspect of operant conditioning was to teach the owls to first focus their attention to the distant stimulus panel before they were allowed to emit a response. The probability of getting rewarded just by chance (50%) turned out to be high enough to let the birds match their response bar choice after having been cued by the observation stimulus. Within 60-100 sessions, the owls learned to be cued and to manipulate the response bars without the occurrence of a preference. Reciprocal operant conditioning was stopped when the number of responses to either response bar were equal within a single experiment for three successive days. Examples of the final response traces are shown in Figure 17. Note the birds were only “timed-out” when they emitted a response while being presented with observation stimulus (see Figure 9 on page 23). The use of timeouts, after the wrong response bar had been selected, turned out to be counter productive. The signal that indicated an incorrect response was the omission of a reward combined with a screen blank. In contrast to other studies of operant responding in birds (Martin, 1974; Witoslawski, 1963; Whitt and Crawford, 1967), the owls used here were not sensitive to variations in the experimental procedure. These variations included the spatial separation of the response bars, distance to the stimulus panel and level of food deprivation. Thus, the discrimination apparatus and operant shaping procedure—employing reciprocal reinforcement—in combination with a visual cueing signal proved to be suitable to produce unbiased responding behaviour. Chapter 3: Discriminative learning & visual perception 43

Experiment II: Discrimination learning and transfer tests

The fact that owls can be operantly conditioned to attend to a distant CRT screen raised the question whether the pre-conditioned animals of experiment I could be trained on fairly simple visual tasks such as visual search, texture and, motion perception. The behavioural procedures and discrimination paradigms described in this second experiment were designed to address this question. 3.3.1 Methods Discrimination paradigms and behavioural procedures: All birds were trained and tested in a two phase procedure (see section 2.3 of chapter 2). The employed discrimination paradigms I and II are described in chapter 2. The conceptual difference between the two paradigms lies herein that I provided a signal versus no-signal discrimination, whereas II provided a signal versus different-signal discrimination. Thus, the discrimination in II has to become even more specific than in I because the differences between the images are not found in the presence or absence of a visual cue. Instead the animals have to categorise between different configurations of the same visual cue. Prior to testing, the animals were reminded of their task by rewarding them only for correct choices and testing began only after each bird had reached criterion— reliable performance: 83% correct for 12 consecutive trials; P (X ≥ 83%) < .001 independent binomial probability. During psychometric testing rewards were given in only 70% of the trials; irrespective of the correctness of the choice—nondifferential reinforcement—to maintain discriminative behaviour. To avoid feedback during the transfer sessions, the birds were nondifferentially reinforced in all trials. In a single transfer test experiment the owls were subjected to a total of 24 sessions. A session was terminated when the owls had received 10 reinforcements. On a daily basis, the birds had to undergo four sessions. In the first two “training” sessions the training stimuli appeared, with being switched to the modified transfer stimuli in the second two “transfer” sessions.

Discrimination tasks, stimuli and tests of transfer: In total, three tasks were trained. In the visual search task (1) and the texture perception task (2) the stimuli were identical to those described for paradigm I and could appear in any of three locations on the screen i.e., either at the centre, the left, or the right side. In the motion perception task (3), the stimulus conﬁguration were identical to those described for paradigm II and the motion contrast between ﬁgure and ground was either “high” (216,000 dots/deg2/sec) or “low” (36,000 dots/deg2/sec). The owls were divided into two groups of two subjects, the paradigm I group and the paradigm II group. Owls, JL and RG, of the paradigm I group were trained in the visual search task using asymmetric positioned images. The same owls were also trained in texture perception 44 On the Perceptual Identity of Depth Vision in the owl task using symmetric positioned images. Owls, SL and VS, of the paradigm II group were trained in the visual motion task using either the unequal motion stimulus pair (low hole versus high object) or the equi-motion stimulus pair (low versus low).

Data analysis: Data were collected in a successive viewing of a balanced quasi- random sequence of images belonging to a single stimulus pair. With the stimuli presented in this manner, 100% correct represents perfect discrimination and 50% chance responding. Performance on the test and training stimulus pairs was calculated from the mean of the individual sessions (N=12). The subjects trained with the texture perception task, using displays of asymmetrical positioned images, were transfered to discriminate symmetrical displays of the same images. The subjects trained with the motion perception task, using RDKs that contained unequal amounts of motion, were transfered to discriminate RDKs that contained the same amount of motion. Psychometric functions were constructed for the texture, and motion perception tasks to assess the degree of stimulus control. Used was a non-parametric index of response bias (Hodos, 1970). This index of stimulus control was determined through a signal-detection analysis of the psychophysical data (Green and Swets, 1966). The psychophysical data were obtained by employing the above described two-alternative choice procedure combined with the method of constant stimuli. The stimulus levels spanning the psychometric function were presented in a randomly intermixed sequence of separate blocks to form a daily session. In turn, each block contained a balanced quasi-random sequence of 10 images belonging to a single stimulus pair. Thus for any given block only one difference in stimulus level between the standard and non-standard image was used. The data of a particular daily session was omitted when the birds failed to report the standard image with a probability of more then 80% in the trials presenting the two highest stimulus levels. A psychometric function—representing the probability that the owl’s response correctly indicated the presence of either the standard or the non-standard image as function of stimulus level—was fitted to the data that combined 5 successive sessions by use of the bootstrap method (Foster and Bischof, 1991). Threshold was defined as the stimulus value yielding a performance of 75% correct, that was derived by interpolation. The absolute difference in the stimulus value between standard and threshold was taken to be the difference threshold. The psychometric data on the texture perception task was obtained by gradually reducing the texture and/or luminance cue in the figure-ground image employing 8 levels of grey-dot percentage i.e. 100, 95, 90, 85, 80, 75, 70, and 50%. The standard image (ground-only) contained 50% grey dots. By reducing the amount of motion in the object RDK, using 6 levels of velocity i.e. 3.0, 2.5, 2.0, 1.5, 1.0 and 0.5 [deg/s], psychometric data on the motion task was acquired. The velocity in the standard image(hole RDK) was kept at 0.5 [deg/s]. Chapter 3: Discriminative learning & visual perception 45

3.3.2 Results and Discussion Discrimination paradigm I: Texture perception Visual search training: Owls JL and RG, were trained with paradigm I to test texture perception. Figure 18 shows the individual learning curves of these owls when they were trained to indicate whether an image was presented on the left side, or alternatively, the right side of the monitor. The design of the experiment was such that the ﬁgure-ground image was always assigned to the left side and the ground-only always to the right side. Both animals learned the task and showed only a small difference in acquisition of the discrimination (18 sessions in JL versus 13 sessions in RG).

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Figure 18: Paradigm I: Individual learning curves of owls JL and RG on the visual search task with the asymmetric positioned stimuli (training stimuli of Figure 19). Shown is the percentage of correct responses per training session. JL reached baseline performance after 18 sessions (300 trials), and RG after 13 sessions (219 trials). 46 On the Perceptual Identity of Depth Vision in the owl

Transfer from asymmetric to symmetric positioned stimuli: To determine whether the difference in textural organisation of the images guided the owl’s responses the same animals were tested with symmetrical displays of the paradigm I images. This was done by displaying all the images in the centre of the monitor. Figure 19 shows the disruptive effect of the symmetrical positioning of the images on the learned discrimination. The difference in performance to the new symmetrical stimuli (after the ground-only image left versus figure-ground image right discrimination) was highly significant in both owls [Wilcoxon rank-sum test, JL: t(22)= 8.3, p<.001, RG:t(22)= 8.2, p<.001]. Between the individuals, however, there was no significant difference in the mean performance [Wilcoxon

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Figure 19: Paradigm I: Effect of stimulus position on the learned visual search task with owls JL and RG (A) and two sets of figure-ground versus ground-only stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 12 sessions with the training pair (shaded bars, JL: 86±8; RG: 90±10) and the test pair (open bars, JL: 52±7; RG: 52±6) stimuli. The error bars indicate standard deviation. B: Shown are scaled versions of the used training and testing patterns. Chapter 3: Discriminative learning & visual perception 47 rank-sum test, visual search: t(22)= 1.0; texture perception: t(22)= 0.3]. In addition, both owls did not treat the figure-ground images different from the ground-only images when they were presented symmetrically [Pearson chi-square test, JL: χ2(1) = 0.15; and RG: χ2(1) = 0.14].

Texture perception training: To force the animals to use the local features (i.e., diﬀerences in texture and/or overall luminance) that existed between the images of paradigm I the same subjects were trained to discriminate the symmetrically positioned images. In other words, the owls were now required to report the presence (standard image: 100%) or, alternatively the absence (non-standard image: 50%) of a rectangle (Figure 21A).

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Figure 20: Paradigm I: Individual learning curves of owls JL and RG on the texture perception task with the symmetric positioned stimuli (training stimuli of Figure 21B). Shown are the percentage of correct responses per training session. JL reached base line performance after 54 sessions (929 trials), and RG after 35 sessions (605 trials). 48 On the Perceptual Identity of Depth Vision in the owl

As can be seen from the learning curves in Figure 20 owls JL and RG learned the task but showed a marked individual difference in number of sessions to reach criterion (54 versus 35, respectively). Moreover, the owls attended more easily to the image-monitor spatial relationship than to the figure-ground organisation of the displayed images since it took them much longer to reach criterion (on average 29 sessions) when only textural and luminance differences could be used as the cues to discriminate. This marked difference in acquisition speed, however, could have been enhanced because the owls had first to unlearn the visual search task.

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Figure 21: Paradigm I: Successful transfer of the texture perception task with owls JL and RG after inverting the luminance cue (A) and two sets stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 12 sessions with the training pair (shaded bars, JL: 87±8 RG: 90±7) and test pair (open bars, JL: 83±11; RG: 86±11). The error bars indicate standard deviation. B: Shown are two sets of ﬁgure-ground versus ground-only texture stimuli pairs Chapter 3: Discriminative learning & visual perception 49

Texture perception transfer with inverted luminance stimuli: After having established that the owls could discriminate the paradigm I patterns, I performed a transfer test to rule out the possibility of discriminative behaviour based on the difference in average luminance between ﬁgure and ground. When tested with patterns containing a black rectangle high performance levels were observed [independent binomial probability, JL: P (X = 83%) .0001; RG: P (X = 86%) .0001] (open bars in Figure 21). Inversion of the luminance cue did not disrupt performance signiﬁcantly [Wilcoxon rank-sum test, JL: t(22) = 1.2; RG: t(22) = 1.0] (Figure 21).

Texture perception signal detection analysis : To obtain a measure of response bias in the texture perception task a signal-detection analysis was carried out. For this purpose, measured was the change in performance when figure-ground organisation of the image that contained the rectangle was faded by adding black dots to the figure region (Figure 22B). From these data the texture difference threshold was calculated as 31% for owl JL and 20% for RG (Figure 22A), representing a threshold value of 81% and 80%, respectively. Subsequently, the psychometric data of Figure 22A was plotted in the form of a signal-detection unit-square. In the squares of Figure 23 the conditional probability of a correct acceptance is plotted as a function of an incorrect acceptance. Here correct acceptance was defined as: the probability of reporting the presence of a figure when a figure-ground image was actually displayed, and incorrect acceptance as: the probability of reporting the presence of a figure when in fact a ground-only stimulus was shown. The number at each data point within the squares denotes the stimulus level of the data shown in the psychometric functions of Figure 22A for owl JL and RG, respectively. Consequently, each point represents 50 trials. Both subjects maintained a small but fairly consistent response bias to the ground-only image, except for the smallest stimulus levels. The response bias in owl JL approximated 10% and was somewhat less than that found in owl VS that approximated 25%. When focusing on the sensory capability of the owls, the areas under the dotted contours (receiver operating characteristic, ROC; Green and Swets, 1966) in the plots of Figure 23 provide a useful measure of sensitivity. Sensitivity can range from .5 (no figure-ground detection) to 1.0 (perfect figure-ground detection). In both unit squares, the points representing the highest stimulus levels (90-100%) are clustered in the upper left corner above the .9 iso-sensitivity contour, indicating that these stimulus pairs were easy to discriminate. Moreover, points depicting stimulus levels closer to the value of the ground-only stimulus (50%) move progressively nearer to positive diagonal. Thus, for both owls the relationship between sensitivity and the magnitude of difference in grey-dot percentage between the images of a particular stimulus pair is preserved. Stimulus control in owl RG, however, was completely lost in blocks that contained stimulus levels well below stimulus threshold (80% black dots). 50 On the Perceptual Identity of Depth Vision in the owl

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Figure 22: Paradigm I: Psychometric functions obtained for owls JL and RG, respectively, in determining the detection threshold for the figure-ground stimulus (A) by eliminating the textural cue (B). A: The functions represent the probability that the owl’s response correctly indicated the presence of either the standard (ground-only) image or the variable non-standard (figure-ground) image as function of the percentage grey dots in the figure region. The grey bars depict the 95% confidence interval at each data point. B: Figure-ground fading by adding black dots to the figure region of the trained 100% grey dot stimulus. Chapter 3: Discriminative learning & visual perception 51

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Y RG ( 0 P 0 .2 .4 .6 .8 1.0 P(YES | GROUND-ONLY) Figure 23: Paradigm I: Signal-detection analysis of texture perception psychometric data obtained for owls JL and RG. The curved grey lines are non-parametric iso-bias curves, depicting (going from left to right) 50%, 25% and 10% response bias toward the ground-only image, respectively. The negative diagonal represents the locus of points having zero-bias. The areas under the dotted iso-sensitivity contours equal (going away from the positive diagonal along the negative diagonal) .6, .7, .8 and .9, respectively, and is a measure for the sensitivity of the animals. The area under the positive diagonal measures .5 and represents the locus of points indicating no-detection of the diﬀerence in texture between ﬁgure and ground. The numbers indicate the stimulus level [% grey-dots]. 52 On the Perceptual Identity of Depth Vision in the owl

Discrimination paradigm II: Motion perception Training with unequal motion contrast stimuli: Owls SL and VS, were trained with paradigm II to test motion perception. Figure 24 shows the individual learning curves of these owls when trained with the unequal motion stimuli. The owls were required to indicate whether the amount of motion contrast was low or, alternatively, high. The design of the experiment was such that the hole RDK was always assigned to be low, and the object RDK always high. Both animals learned the task and showed only a small diﬀerence in the number of sessions to reach criterion of the discrimination (28 sessions in SL versus 26 sessions in VS). Although, it took owl VS two sessions less to reach baseline performance than owl SL, the amount of trials that these 26 sessions contained was much higher i.e., 414 trials in SL versus 666 trials in VS.

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Figure 24: Paradigm II: Individual learning curves of owls SL and VS on the motion perception task with the unequal-motion stimuli (see training stimuli of Figure 25B). Shown are the percentage of correct ﬁrst responses per session. SL reached baseline performance after 28 sessions (414 trials), and VS after 26 sessions (666 trials). Note that the motion contrast level in the hole RDKs was 6 times lower than that in the object RDKs. Chapter 3: Discriminative learning & visual perception 53

Motion perception transfer with equi-motion stimuli: In principle, the owls could have based their judgements on the patterns of occlusion and dis-occlusion in addition to the motion contrast (or velocity) cue, because the former diﬀer between object and hole RDKs. At the leading edge of the moving object there is occlusion of the ground, while at the trailing edge there is dis-occlusion. Conversely, at the leading edge of the hole there is dis-occlusion while at the trailing edge there is occlusion. To determine whether occlusion was guiding the owl’s responses the same animals were tested with the equi-motion RDKs.

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Figure 25: Paradigm II: Test of transfer on the learned motion perception task after removal of the motion contrast cue with owls SL and VS (A) and two sets stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 12 sessions with the training pair (shaded bars, SL: 90±6; VS: 90±4) and the test pair (open bars, SL: 60±4; VS: 55±6). The error bars indicate standard deviation. B: Shown are two sets of hole versus object RDK stimulus pairs. The size of the black arrows are a measure for the amount of motion contrast.

Figure 25 shows that the discrimination of RDKs containing the same level of motion contrast was significant more difficult than discrimination of RDKs containing 54 On the Perceptual Identity of Depth Vision in the owl different levels of motion contrast [Wilcoxon rank-sum test, SL: t(22)= 8.3, p<.001, VS: t(22)= 8.2, p<.001]. Closer inspection of the stimulus response relationship on the test trials (Figure 25 open bars) revealed that performance levels on the hole RDK trials differed significantly from chance (Figure 26) [independent binomial probability, SL: P(X ≥ 74%) = .0000007; RG: P(X ≥ 65%) = .00005]. It turned out that at least one owl, SL, treated the equi-motion object and hole RDKs as different stimuli [Pearson chi-square test, SL: χ2(1) = 10, p<.005; VS: χ2(1) = 2.1, p<.25].

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Figure 26: Paradigm II: Transfer performance in owls SL and VS on the motion perception task with object and hole RDKs containing the same amount of motion contrast (A) after prior training on RDKs diﬀering in motion contrast and their respective stimulus-response matrices (B). A: The histograms depict the mean percentage correct performance from 12 sessions on the hole (shaded bars, SL: 73±8; VS: 65±10), and the object RDK trials (open bars, SL: 49±5; VS: 44±6). The error bars indicate standard deviation. B: Shown are the absolute number of outcomes on the hole and object trials. Numbers outside the cells indicate the sum of the respective rows and columns.

The data of Figure 26 indicated that the subjects were applying some generic rules for grouping the RDKs into objects and holes. Thus, it should be possible to determine the features that are used for such a classification. One feature that sets the objects apart from holes is the change in position of the figure relative to the ground over time. In the hole RDKs the figure always remained at the centre of the display. Chapter 3: Discriminative learning & visual perception 55

Motion perception transfer with reversed-motion stimuli: To rule out the possibility that object position was used as the critical cue to discriminate the unequal motion RDKs the animals were tested with a stimulus pair in which the motion contrast levels were reversed (Figure 27B). If object position was guiding the owls’ responses than one would expect that discrimination of objects should be confounded because initially a slow moving object does not deviate much from the centre of the stimulus.

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P 40 hole slow object slow object fast hole fast Figure 27: Paradigm II: Successful transfer of the motion perception task in owls SL and VS after reversing motion contrast cue (A) and two sets of stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 12 sessions with the training pair (shaded bars, SL: 91±6; VS: 87±3) and the test pair (open bars, SL: 78±4; VS: 79±7). The error bars indicate standard deviation. B: Shown are two sets of hole versus object RDK stimulus pairs. The size of the black arrows are a relative measure for the amount of motion contrast.

The results shown in Figure 27, that provide an example of successful transfer [Wilcoxon rank-sum test, SL: t(22)= 6.8, VS:t(22)= 3.2], were not consistent with this expectation. And, more important, both owls treated the high motion contrast object, and the low motion contrast hole RDK as perceptually diﬀerent [Pearson chi- square test, SL: χ2(1) = 70, p.001; and VS: χ2(1) = 62, p.001]. 56 On the Perceptual Identity of Depth Vision in the owl

Motion perception signal detection analysis: To get a more detailed view of the role that the motion cue played in the owls’ discriminative behaviour a signal-detection analysis was carried out. The data for this analysis were obtained by measuring the change in performance when the motion cue was faded by reducing the amount of motion in the object RDK. Note that stimulus level—motion contrast ratio—is given by the ratio: object velocity / hole velocity. For each testing condition (Figure 28), performance decreased as the motion contrast ratio decreased. In both owls, this dependency tended to be linear. The diﬀerence in motion needed to discriminate reliably varied amongst the individuals. The motion contrast ratio threshold was measured to be 2.9 and 4.3 for owls SL and VS, respectively. T

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| o r e S .2 z E Y ( VS P 0 0 .2 .4 .6 .8 1.0 P(YES | HOLE-RDK) Figure 29: Paradigm II: Signal-detection analysis of motion perception psychometric data obtained for owls SL and VS. The curved grey lines are non-parametric iso-bias curves, depicting (going from left to right) 50%, 25% and 10% response bias toward the Hole RDK, respectively. The negative diagonal represents the locus of points having zero-bias. The areas under the dotted iso-sensitivity contours equal (going away from the positive diagonal along the negative diagonal) .6, .7, .8 and .9, respectively, and is are measure for the sensitivity of the animals. The area under the positive diagonal measures .5 and represents the locus of points indicating no-detection of the diﬀerence in motion contrast between hole and object RDK. Numbers indicate the motion contrast ratio. 58 On the Perceptual Identity of Depth Vision in the owl

The psychometric data of Figure 28 was plotted in the form of a signal-detection unit-square. Here (Figure 29) the conditional probability of a correct acceptance of the object RDK was plotted as a function of an incorrect acceptance of the hole RDK. The number at each data point, which represents 50 trials, denotes the motion contrast ratio of the tested stimulus pair. The response bias in owl SL remained at a moderate level of 25%. Owl VS showed also a consistent response bias, but at a lower level (10%) than was the case for SL. Thus, both subjects showed a remarkable consistent response bias to the hole RDK at all measured motion ratios.

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When focusing on the sensory capability of the owls, in both unit squares the points representing the three highest motion ratio values are located above the .8 iso- sensitivity contour. And points depicting stimulus levels closer to a motion contrast ratio of 1 move progressively nearer to positive diagonal. Thus, for both owls the Chapter 3: Discriminative learning & visual perception 59 relationship between sensitivity and the motion ratio value of a particular stimulus pair is preserved. Note however, stimulus control in these animals was never lost.

Training with unequal motion contrast stimuli: After having demonstrated that the owls could discriminate between RDKs that differed in their motion content. And that this discrimination is, at least in part, dependent on the occlusion pattern of the motion display and not the location of motion, it should be possible to train owls to discriminate between object and hole RDKs contain the same amount of motion. Consequently, owls SL and RG, were trained with such an equi-motion stimulus pair. As can be seen from the learning curves in Figure 30, owls SL and VS learned the task with only a small difference in training sessions (31 in SL versus 34 in VS). The amount of trails needed to reach baseline discrimination, however, differed greatly (504 in JL versus 698 in VS). When compared with the learning curves of Figure 24 it appears that the pre-trained owls attended more easily to the motion content of the random-dot displays than to the patterns of occlusion and dis-occlusion.

3.4 General discussion

3.4.1 Discriminative learning The difference in acquisition speed of owls JL and RG on the visual search (Figure 18) and texture perception (Figure 20) task can tentatively be explained in terms of a predisposition to spatial position rather than figure-ground perception. But it could also be possible that it took the owls longer to learn the texture perception task because they first had to un-learn the visual search task. The latter interpretation, however, fails to account for the fact that during the visual search training the spatial position appeared to be dominant over the textural organisation of the presented images. Moreover, if the owls were more prone to pick up differences in spatial position rather than textural differences then one would expect that the unequal motion task is learned equally fast as the visual search task because both tasks can be solved by determining the position of the figure region. Although, owls SL and VS mastered the (unequal) motion perception task (Figure 24) not as fast as owls JL and RG mastered the visual search task, acquisition on the motion perception tasks (Figure 24 and 30: owls SL and VS) was substantially faster when compared to acquisition on texture perception task (Figure 20: owls SL and RG). Even when there existed some individual differences in the learning ability amongst the tested owls (SL and RG versus JL and RG), and some un-learning had to take place in owls JL and RG, this cannot logically explain the large difference in acquisition speeds between the texture perception and 60 On the Perceptual Identity of Depth Vision in the owl the motion perception task. In my view, it is more likely that the difference in positional information between the standard and non-standard images of the visual search and motion perception task helped the owls to learn much faster.

3.4.2 Signal-detection analysis and stimulus control The observation common to both the texture and motion perception experiments was that the bias was always projected towards the standard stimulus i.e., the constant stimulus. Probably the owls attended more easily to the standard simply because of the difference in exposure. In other words, the owls were more used to detect the standard and as a result were more prone to indicate its presence. However, another interpretation would be that owls may have some neglect to the right side of their bodies, since the standard stimulus was always coupled to the left key. An observation confined to the signal-detection analysis of the motion perception task was that both owls, SL and VS, were still under stimulus control even when the motion content in the object RDK was well below the motion contrast ratio threshold (see also Figure 26). Stimulus control is here defined as the ability of the subjects to reliably detect the standard stimulus, i.e., hole RDK. Thus, there is some evidence to suggest that the discriminative behaviour of the owls during the motion perception task was not only based on the motion content. In the texture perception task, however, stimulus control was completely lost in both owls (see Figure 23); even when the textural cue was not completely eliminated. It seems therefore that in this case differences in texture density was the most prominent visual feature to the owls which guided their level of performance. Chapter 3: Discriminative learning & visual perception 61 62 On the Perceptual Identity of Depth Vision in the owl 4 BASIC DEMONSTRATION OF FUNCTIONAL STEREOPSIS

. . . He that thinks with more subtlety will seek for terms of more nice discrimination —Samuel Johnson, The Idler

Abstract This chapter presents behavioural data1 of a series of experiments for demonstrating stereopsis in operant conditioned owls. First, an initial base line discrimination between distinct types of random-dot patterns was established in three barn owls. Then, I describe discrimination-transfer procedures and control experiments used to test for stereopsis with random-dot stereograms. These behavioural tests clearly showed that avian stereopsis underlies (1) the capacity to detect monocular camouflaged objects, (2) the ability to immediately transfer from non-stereoscopic to stereoscopic “figure- ground” perception and, (3) the ability to determine relative depth, using retinal disparity as the sole cue for discrimination. In addition, head position monitoring, by means of a real-time tracking device, revealed that the owls did not need to move or reposition their head relative to the stereoscopic figure to perform reliably.

1 Adapted from: van der Willigen, Frost and Wagner 1998. In: NeuroReport Vol.: 09, no. 06, pp: 1233-1237. 64 On the Perceptual identity of Depth Vision in the Owl

4.1 Introduction

Considerations about constraints imposed by sensory ecology have led to the claim, first made by Pettigrew (Pettigrew, 1986), that there is a high degree of similarity between the avian and mammalian neural algorithm for stereovision—the adopted computational strategy avoids feature extraction until information from both eyes has converged. The latter is known as global stereopsis and can be demonstrated by the use of random-dot stereograms (RDSs) (Julesz, 1971). To test Pettigrew’s ”unitary” hypothesis of stereopsis (Pettigrew, 1990) I employed the barn owl as a “model system” and searched for behavioural evidence of stereopsis in this avian species. The rationale behind using the barn owl as a “model system” is based on the fact that this nocturnal animal has evolved an elaborate neural substrate (the visual Wulst) for binocular vision which is comparable with that found in mammals (the striate cortex) (Pettigrew, 1986; Nieder, 1999). Common features of these telencephalic regions include a high degree of binocular interaction, selectivity for stimulus orientation, direction of movement and spatial frequency as well as binocular disparity (Pettigrew and Konishi, 1976a, Pettigrew, 1979; Wagner and Frost 1994). Binocular interaction refers to the phenomenon that single cells receive inputs from the same part of the binocular visual field of both eyes. Consequently, binocular cells form the neurophysiological basis for mechanisms that encode retinal disparity. And in turn, binocular retinal disparity is thought to form the neural basis of binocular stereoscopic depth perception. While comparative psychology of sensory perception has incorporated measurements of global stereopsis in monkeys (see e.g., Harwerth and Boltz, 1979), cats (see e.g., Ptito et al., 1990), horses Timney and Keil, 1999) and falcons (Fox et al., 1977) it has failed to assess the perceptual judgement of relative depth through stereopsis. And although a study by Bough (1970) has shown that monkeys can differentiate between different classes of RDSs—one revealed an object in front of a more distant background pattern (“object” RDS) the other, however, displayed a background pattern that contained a hole revealing a more distant surface (“hole” RDS)—it is not clear if animals are able to generalise to differences in absolute depth within these classes of RDSs. To resolve this lack of knowledge, I used tests of discrimination transfer— choosing between novel stimuli on the basis of cues learned in earlier discriminations. The primary goal of this study was to demonstrate stereopsis in the owl at the behavioural level. To achieve this aim I adopted the following criteria: (I) the power to break camouflage and, (II) the ability to determine relative depth based on the inspection of static RDSs. Chapter 4: Basic demonstration of functional stereopsis 65

4.2 Methods

4.2.1 Animals and behavioural apparatus Three barn owls (Tyto alba), JL, SL and, VS were cared for and treated according to the “NIH Guide for the care and use of laboratory animals” and were subject to regular inspections by the state veterinarian (see also section 2.1 on page 15). For a detailed description of the apparatus see Chapter 2 (page 16). The tracking system was calibrated with a behavioural procedure as described in Chapter 2 (page 18).

4.2.2 Behavioural procedures and paradigms The owls were trained and tested in a two phase procedure as is described in section 2.3 of chapter 2. The employed discrimination paradigms I and II are described in section 2.4. A detailed description of the reinforcement contingencies and the behavioural procedures are given in section 3.3.1 of Chapter 3.

4.2.3 Discrimination tasks, stimuli and controls One approach to demonstrate stereopsis was testing whether purely monocular induced figure-ground segregation is perceptually preserved in novel binocular stimuli—devoid of the pre-learned monocular cue. For this purpose owl SL was trained with the paradigm I stimulus pair and subsequently tested with RDSs. In this novel stereoscopic testing pair, one RDS was identical to the ground-only stimulus, and the other contained a stereoscopic rectangle that appeared to lie behind a similarly textured background (un-crossed r= 26 arcmin). Both the rectangle and background contained equal amounts (50%) of grey and black dots. However, before stereoscopic testing took place measured was a psychometric function to determine the monocular cues that guided the owls’ responses. The psychometric data were obtained by gradually reducing the texture and/or luminance cue in the figure-ground image employing 8 levels of grey-dot percentage i.e. 100, 95, 90, 85, and 50%. The standard image (ground-only) contained 50% grey dots. An alternative approach to demonstrate stereopsis was testing for the animals’ ability to differentiate between different classes of RDSs using retinal disparity as the sole cue for discrimination. For this purpose two owls, SL and VS, were trained with the paradigm II using the motion-in-depth RDSs. Hereafter, the monocular detectable cue (apparent motion) was removed. Thus, an interpretation in terms of stereoscopic depth perception makes a clear prediction about the owls’ discriminative performance: removal of the motion cue would necessarily affect performance when the owl visual system is not capable of stereopsis. 66 On the Perceptual identity of Depth Vision in the Owl

The next step was to determine what kind of binocular information was used: relative or absolute disparity. If relative depth perception was guiding the depth judgements, one would expect that the owls could generalise to a wide range of disparity values irrespective of the used RDS class (objects versus holes). To address this hypothesis a generalisation experiment was conducted referred to as the depth ordering test, used was the paradigm II RDS stimulus pair. For this purpose the sign of the figure disparity in the learned RDSs was systematically changed while keeping unchanged the depth ordering between figure and ground. As a result to novel RDSs pairs were constructed. In one pair, figure disparity of the object and hole RDS equalled 16 and -16 arcmin, respectively, and that of the ground 32 and -32 arcmin, respectively. In the other pair the figure was always non-disparate (zero disparity), whereas the ground disparity in the object and hole RDS equalled 16 and -16 arcmin, respectively. The concept behind this change in disparity content of the RDSs lies herein that an animal sensitive to the relative depth cue should be able to classify the novel RDS into object and hole irrespective of the absolute values of the disparity that made up the figure- ground segregation. In addition, measured were the head movements of the owls while performing the depth ordering task. To determine whether the owls needed to assume a fixed relationship between stereoscopic figure and its position in the visual field I also misaligned the location of the stereoscopic figure relative to the owls’ midline. As a result, 20% of the stereoscopic squares in the depth ordering test could occupy one of four possible locations that were specified by the centre coordinates of the backgrounds’ quadrants. To create an even distribution of the target locations, I made sure that they appeared in each of the quadrants with the same probability. Furthermore, the visual angle of the stimulus was increased by decreasing the viewing distance to 70 cm as opposed to the standard 150 cm. Note retinal disparity was corrected for this novel viewing distance. Finally, a standard control of stereopsis was to measure performance under monocular viewing conditions. I carried out the equivalent of monocular occlusion by placing filters of the same polarisation or colour in front of the eyes (Fox et al., 1977). This procedure permits only one half-image to stimulate both eyes. As a result, the monocular control sessions were of two types: in one only the left, and in the other only the right half-image was made visible. Used were crossed and un-crossed RDSs that contained a figure disparity of -18 or, 18 arcmin, respectively. Within a single session these test stimuli were presented intermixed using a balanced quasi-random list that was predetermined. This control was performed on both static polarised and, static anaglyph RDSs. A single control experiment existed of a sequence of five session that alternated between stereo and mono viewing conditions i.e., stereo, mono left, stereo, mono right, stereo. All animals were subjected to this type of control and tested were both polarised and anaglyph RDSs. Chapter 4: Basic demonstration of functional stereopsis 67

4.2.4 Data analysis Data were collected in a successive viewing of a balanced quasi-random sequence of images belonging to a single stimulus pair. With the stimuli presented in this manner, 100% correct represents perfect discrimination and 50% chance responding. Performance on the test and training stimulus pairs was calculated from the mean of the individual sessions (N=12). In all plots the numbers at each data point indicate number of trials and the vertical bars display 95% conﬁdence intervals. For the purpose of graphical display, it was assumed that the errors were normally distributed, and the 95% conﬁdence intervals were calculated using the method described Watson and Peli (1997). The variable number of trials at each data point is a by-product of the followed behavioural procedures as described in section 2.3.2 of chapter 2.

4.3 Results and Discussion

4.3.1 Discrimination training Non-stereoscopic texture discrimination: Owl JL was trained with paradigm I and learned to report the presence, or alternatively, the absence of a grey rectangle (Figure 12 on page 27). JL reached criterion after 54 sessions (Figure 31). t

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Figure 31: Paradigm I: Learning curve of owl JL showing percentage of correct choices over 54 training sessions for discrimination of ground-only versus ﬁgure-ground random-dot stimulus pair. Shown are the percentage of correct responses per training session. JL reached base line performance after 54 sessions (929 trials). 68 On the Perceptual identity of Depth Vision in the Owl

Stereoscopic motion discrimination: Owls SL and VS were trained with paradigm II and learned to detect a stereoscopic form that oscillated either in front (object), or alternatively, behind (hole) a non-disparate background (see Figure 14 on page 31).

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Figure 32: Paradigm II: Learning curves of owls SL and VS, showing percentage of correct choices over sessions for one pair of stereograms: object versus hole RDSs. Shown are the percentage of correct responses per training session. SL reached base line performance after 33 sessions, and VS after 36 sessions.

Figure 32 shows that SL mastered this task within 33 sessions (558 trials), whereas VS reached criterion after 36 sessions (639 trials). Chapter 4: Basic demonstration of functional stereopsis 69

4.3.2 Transfer to stereoscopic stimuli Transfer from non-stereoscopic to stereoscopic figure-ground stimuli: With paradigm I, I was able to demonstrate transitive inference of the learned figure- ground segregation task in JL by replacing the learned monocular cue (difference in luminance and/or texture) through a novel, binocular, cue (horizontal retinal

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Figure 33: Paradigm I: Transfer from monocular to binocular discrimination with JL. A: Per- centage of correct responses to monocular (MONO: dots) and binocular (STEREO: squares; r= 26 arcmin) discriminative stimuli. Goodness of fit stereo data: χ2(3) = 9.9,P<.005. B: Figure-ground fading of the stimulus that contained the rectangle, by randomly adding black dots to the figure region. Shown are scaled versions of the monocular discernible test figure- ground patterns representing four different stimulus levels: 50, 65, 75 and 100% grey dots in the figure region. Note only 100% and 50% grey dot patterns were used during the training phase. The 50% grey dot patterns were invariant and function as the standard stimulus during the test phase. 70 On the Perceptual identity of Depth Vision in the Owl disparity). In non-stereoscopic testing JL only responded reliably when there existed a substantial overall luminance difference between figure and ground (MONO: 85%- 100% grey dots, Figure 33). A difference in texture was not enough since performance was at chance level if figure and ground had the same number of randomly distributed black and grey dots (MONO: 50% grey dots, Figure 33A). When tested with stereoscopic stimuli (STEREO, Figure 33A), however, JL exhibited high performance levels, even in the absence of any difference in luminance (STEREO: 50% grey dots, Fig- ure 33A).

Depth ordering test and generalisation of relative depth: To distinguish between relative and absolute depth perception, I devised a depth ordering task (paradigm II) similar to that used by Bough (1970). In the training phase of this “depth ordering” experiment, a monocular discernible cue—structure from motion—was used in addition to the binocular cue to facilitate discriminative learning (open area in Figure 34). s

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Hereafter, I removed the non-stereopsis information and allowed sharpening of the initial generalisation tendencies through differential reinforcement. Acquisition was quite rapid. Within 4 sessions the animals reached the pre-change level (shaded area in Figure 34). Despite this positive transfer, it should be cautioned that perception of the “figure-ground” depth configuration may be possible simply by detecting the absolute depth of the stereoscopic form, since the eyes of the barn owl are locked in a more or less fixed position of vergence (Knudsen, 1989). Consequently,

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Figure 35: Paradigm II: Successful transfer to the β and γ RDSs of the depth ordering test with owls SL and VS (A) and three sets stimulus pairs: α, β and γ (B). A: The histograms depict the mean percentage correct performance of 12 sessions with the training pair α (SL: 92±6; VS: 91±5) and the two test pairs β +γ (JL: 87±7; RG: 88±7). The error bars indicate standard deviation and N denotes the number of sessions. B: Shown are the depth contours of three sets of RDSs. The dotted line indicates the depth plane of the stimulus display. The open and closed black rectangles depict the ﬁgure, and the grey rectangles depict the ground region. Note the closed black rectangles are in the object, and the open black rectangles are in the hole conﬁguration. 72 On the Perceptual identity of Depth Vision in the Owl ] N=12 SL ] N=12 VS % 100 % 100 [ [

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t 60 t 60 c c e e r r r r o o C 40 C 40 β β γ γ β β γ γ Object Hole Object Hole Object Hole Object Hole

Figure 36: Paradigm II: Transfer performance in owls SL and VS on the depth ordering task (A) and two sets of stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 12 sessions on the object and hole RDSs of stimulus pair β (SL: object 89±7, hole 85±11; VS: object 89±8, hole 89±9) , and stimulus pair γ (SL: object 82±11, hole 86±11; VS: object 87±13, hole 87±8), respectively. The error bars indicate standard deviation. to demonstrate relative depth perception unambiguously, one must test the animals whether the stereoscopic form appears in front or behind the background for a series of different organised RDSs irrespective of the used disparities. This was accomplished by changing both the sign and magnitude of the figure disparity in both α RDSs to respectively the opposite sign (β in Figure 35B) and zero arcmin (γ in Figure 35B) while leaving the difference in disparity between figure and ground unchanged. The transfer to pairs β and γ happened without differential reinforcement and all stimuli were presented intermixed with equal probability. Nevertheless, the performance of the owls remained unchanged (Figure 35A). Closer inspection of the data shown in Figure 35 revealed that the owls’ performance on the object and hole RDSs trials during testing with stimulus pairs β and γ did not differ significantly (Figure 36).

Monitoring of head motion: So far, the interpretation of the data has assumed that the owls viewed the RDS motionless and from the same position in space. Barn owls, however, make head movements that resemble side-to-side “peering” Chapter 4: Basic demonstration of functional stereopsis 73 4 4

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8 6 4 2 0 2 4 6 8 8 6 4 2 0 2 4 6 8 ] m c [ n o i t i s o p - X d a e H ] m c [ n o i t i s o p - X d a e H Head-position traces of owls VS and SL measured when tested with the Figure 37: vertical (Y) and distancethe (Z) perch). component of The theright coordinates owls’ bar: head-position of (-8,0,2). measured thewas in stationary Measurements correctly [cm] positions operated. started relative approximated: 200 The toclarity msec traces the (1) traces were primary prior fixation of recorded position to position: incorrect during (the stimulus response a centre (0,9,0), onset single bar of (2) session selections (dashed while were left lines) the omitted. bar: and owls were were (8,0,2) performing stopped and on when (3) depth a ordering response task. bar For 74 On the Perceptual identity of Depth Vision in the Owl as also seen in insects that are sensitive to motion parallax (Collett and Harkness, 1982; Wagner, 1989). This peering behaviour raises a potential complicating factor because in combination with a stereoscopic display it can induce “compensatory motion parallax”. Compensatory motion parallax refers to the situation in which apparent motion of the stereoscopic figure relative to its background is not real, but due to the fact that the visual system compensates for the lack of motion parallax that a surface under natural viewing conditions would evoke. As a result, the stereoscopic figure shifts its position relative to the direction of the head motion and reverses when sign of disparity of the stereoscopic figure changes. Thus, peering could have been used to discriminate between hole and object RDSs. In this case the direction of motion of the stereoscopic form would be the critical cue on which the owls based their discriminative behaviour. Note however, for the owls to use peering as a strategy to discriminate RDSs, they clearly have to possess stereopsis but the appreciation of the difference in depth between figure and ground is not critical. For this reason, head position was monitored while the owls were performing on the depth ordering task. As will become apparent, however, head position monitoring was not only aimed to detect peering movements. In primates and humans, convergent eye movements provide a powerful mechanism to limit the disparity range that has to be monitored in order to determine relative depth over a wide range of distances. If an animal with fixed eyes, however, would turn its head to face the stereoscopic target squarely and only attempts to measure relative depth at distances straight ahead, than this would limit also the horizontal extend on the retina that has to be devoted to the detection of binocular disparity—as argued by Collett and Harkness, 1982. To evaluate this possibility, I misaligned the location of the stereoscopic figure relative to the owl’s midline in four sessions of the above described depth ordering experiment. For the owl to be able to discriminate relative depth of the shifted stereoscopic region from a distance straight ahead, it had to deviate 5 cm to the left or right side from its initial “fixation” position. It turned out that performance was not affected by the misalignment of the stereoscopic region, both owls made less than 6 mistakes on a total of 48 trials. Thus, to determine whether this was due to the use of head-movements I needed to examine the individual head movement traces. However, I did not observe any systematic change in head position just after stimulus onset, as can be seen from the individual head movement traces shown in Figure 37. Inspection of all measured traces indicate that head movements were only involved to operate the response keys. In only one case (arrow, upper left plot of Figure 37), owl VS moved his head from side-to-side before selecting a response key. I also determined the scatter of the position of the owl’s head at the time of stimulus onset. The horizontal and vertical (X,Y) component varied within ±1 cm and distance (Z) varied within ±1.5 cm. Chapter 4: Basic demonstration of functional stereopsis 75

4.3.3 Performance under monocular viewing conditions In order to verify whether the used RDSs did or did not contain monocular detectable cues the owls were tested under monocular viewing conditions. It can be seen from Figure 38 that performance fell to chance when the eye ﬁlters were of the same

A Polarized static RDSs 56 82 91 90 54 68 98 70 94 54 t t c 100 c 100 e e r r r r o 80 o 80 c c

e 60 e 60 g g a a t t n 40 n 40 e e c c r JL r VS e 20 e 20 P P S MR S ML S S MR S ML S

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e 60 e 60 g g a a t t n 40 n 40 e e c c r JL r VS e 20 e 20 P P S MR S ML S S MR S ML S

Figure 38: Discriminative performance in owls SL and VS during binocular (S; r equalled either +18 or, -18 arcmin) and monocular (MR/ML: right/left eye’s image) viewing conditions to static polarised (A) and, red/green anaglyph (B) RDSs. Note that the data were derived from responses to both object and hole configured RDSs and performance during the different viewing condition sessions (S,MR,S,ML,S) were measured consecutively. 76 On the Perceptual identity of Depth Vision in the Owl polarisation or colour. Moreover, irrespective of the used RDS presenting method, i.e., dichoptic stimulation through either polarisation (Figure 38A), or colour (Figure 38B) separation, the responsive behaviour was preserved and only co-varied with the manipulation of the filters.

4.3.4 Methodological considerations The results of psychophysical experiments with random-dot stereograms can be contaminated by cues originating from the equipment or the technique used to create visual stimuli. Such a contamination might not be obvious to human observers. To ensure that artefacts did not aid the owls several precautions were taken in combination with control experiments. (1) The ground-only stimulus of paradigm I was never changed and was taken to be the standard image. In this way owl JL could memorise the texture of the standard image during the training phase. However, it turned out that this animal did not use texture as a cue because it was not able to distinguish between the standard and a non-standard image when the latter also contained 50% grey dots (see the outer most left data point (black dot) of Figure 33). (2) The motion content of the motion-in-depth stimuli was constructed such that the owls could solve the task solely by determining in which eye’s image the dots were moved. In case the owls would not have been able to discriminate the difference in depth of the moving stereoscopic form relative to the surrounding texture, removal of the motion cue would necessarily abolish their discriminative behaviour. As can be appreciated from Figure 34 the latter was clearly not the case. (3) During all experiments with owls SL and VS the dot distribution of the RDSs was updated between trials. It is possible that if the positions of all the dots in the RDSs remained unchanged and were examined for thousands of trials, some feature of the random-dot pattern could be remembered and used for successful discrimination. Updating of the random-dot distribution at every new trial eliminated this possibility. (4) Precautions were taken to reduce de-correlation—in the region where the stereoscopic form is located—by superimposing the dot-matrix seen by one eye upon the matrix seen by the other eye when the disparity of the stereoscopic form is not an integral multiple of the dot width (Cobo-Lewis, 1994). This was done by randomising the positional shift of the stereoscopic form between the even and odd lines of the CRT screen. Thus, for example the left eye’s image could be projected on the even lines, or alternatively, the odd lines of the CRT screen irrespective of the depth configuration of the employed RDS. In addition, both eye’s images contained half of the total shift of the stereoscopic form. If decorrelation takes place, by randomising the shift of the stereoscopic form between the even and odd lines of the CRT, it is not possible to consistently forecast which stimulus has been presented. (5) To rule out the possibility of contamination of Chapter 4: Basic demonstration of functional stereopsis 77 the RDSs by monocular detectable cues all owls were tested under monocular viewing conditions (see Figure 38). In addition, I also tested whether the RDS presenting method influenced the performance of the owls. If performance would not be dependent on the stimulus presenting method that was employed during the learning phase, i.e., dichoptic stimulation of the eyes through polarisation separation, and all stimulus variables were held constant, it is difficult to avoid the conclusion that the animals were responsive only to the relevant stimulus dimension (retinal disparity). It turned out (Figure 38B) that dichoptic stimulation of the eyes through colour separation did not alter the discriminative behaviour of the tested owls. Conversely, performance fell to chance under monocular viewing. Thus, it is very likely that monocular cues were not involved in the discriminative judgements of the animals. 78 On the Perceptual identity of Depth Vision in the Owl 5 THE FUNCTIONAL SIGNIFICANCE OF OWL STEREOSCOPIC VISION

. . . In full, fair tide let information flow; That evil is half-cured whose cause we know. —Charles Churchill Abstract Stereopsis in the owl is generally assumed to have the same visual function as in primates—the perception of depth. By contrast, binocularity in the owl could be seen as an adaptation to nocturnal life in order to enhance the visibility of camouflaged immobile targets (e.g., prey or three branches) in dim light—camouflage-breaking. Thus, to discover the functional significance of stereopsis in the owl one needs to distinguish between these two alternatives. This was achieved by designing a comprehensive set of psychophysical experiments which specifically evaluate those properties of the owl visual system that set it apart from binocularity in primates. All data were obtained from barn owls trained to discriminate random-dot stereograms (RDSs) containing a flat surface that appeared to be floating either in front or behind a similar textured background. With this discrimination task I evaluated the psychophysical properties of stereopsis in the owl. Manipulation of the contrast levels in anaglyph RDSs produced well predicted changes in the owl’s responses—performance broke down and finally reversed in response to a gradual change in the background luminance. The measured psychometric functions of stereoscopic sensitivity showed that stereoacuity exceeds the anatomical resolving power of the eye. More significant, stereoacuity thresholds remained unchanged down to luminance levels that were within the range of human scotopic vision. Upper-disparity limits (dmax) were within the range of human patent stereopsis. I conclude 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. 80 On the Perceptual identity of Depth Vision in the Owl

5.1 Introduction A striking feature of binocular vision in the owl is stereopsis—the perception of relative depth achieved through the detection and analysis of binocular disparity cues. For disparity measurements to be possible, however, the visual system needs to compare the retinal images in the two eyes, and this means having binocularly driven neurons at some level within the visual system (Parker et al., 1996). Thus, binocular neurons form the neural substrate for stereopsis and have been found in the striate cortex of mammals such as primates and cats (Barlow et al., 1967). A functional similar region, the visual Wulst, has been identified in the barn owl (Pettigrew and Konishi, 1976; Pettigrew 1979; Nieder, 1999). Another key feature of stereopsis is its dependence on differences in the direction of two or more points in space—relative disparity—rather than the absolute position of a single point in space from two vantage points—absolute disparity (Howard and Rogers, 1995). Behavioural experiments have revealed that barn owls can discriminate the relative position of surfaces simulated by random-dot stereograms (RDSs) (van der Willigen et al., 1998). In these computer generated patterns the disparity information is camouflaged by random matrices of thousands of minute dots, and can only be revealed under binocular viewing conditions (Julesz, 1971). These lines of evidence have resulted in the view that stereopsis in the owl has the same visual function as in primates—enhancement of precise depth judgements Collett and Harkness 1982; Howard and Rogers, 1995; van der Willigen, Frost and Wagner, 1998). By contrast, binocularity in the owl could be seen as an adaptation to nocturnal life in order to enhance the visibility of camouflaged immobile targets (e.g., prey or three branches) in dim light—camouflage-breaking (Pettigrew, 1991). Thus, to discover the functional significance of owl stereopsis one needs to distinguish between these two alternatives. To achieve this I specifically evaluated those properties of the owl visual system that set it apart from binocularity in primates. Most owls hunt habitually at dusk and dawn (see e.g., Martin, 1986). Therefore, acceptance of the camouflage-breaking hypothesis would predict that stereopsis in the owl is effective in the detection of monocular disguised (static) targets at low levels of illumination. This is a clear distinction from human stereopsis because in humans stereoacuity thresholds rise by a factor five when luminance is shifted from photopic to scotopic levels (Graham, 1965). On the other hand, a stereo algorithm that only incorporates camouflage-breaking is clearly inferior to a neural mechanism that allows the enhanced discrimination of differences in depth as well. There does not seem to be any incompatibility, therefore, between camouflage-breaking and hyperacute depth perception. A distinctive feature of the owl visual system is the fixed position of the eyes because of their size (Steinbach and Money, 1973; Knudsen, 1989). This poses a major difference when compared to binocularity in humans and primates because Chapter 5: The functional significance of owl stereoscopic vision 81 these mammals can converge their eyes to bring their plane of fixation closer. In addition, adult barn owls have an interocular separation of approximately 45 mm and only a moderate visual acuity of about 7.9 c/deg (Wathey and Pettigrew, 1989; Schaeffel and Wagner, 1996). These properties of the owl visual system would predict that the disparity-range over which stereoscopic depth perception can occur will differ from the range observed in humans and primates. To summarise, to provide a critical evaluation of the functionality of binocular vision in the owl, it is essential to characterise the psychophysical properties of owl stereopsis and to compare these with the known properties of primate stereopsis. For this purpose I developed a comprehensive set of psychophysical tests based on a depth classification task with RDSs whereby the owls had to determine whether a flat squared surface was in front (object configuration) or behind (hole configuration) a similar textured background. These tests provide the first behavioural data that support the camouflage-breaking hypothesis.

5.2 Methods

5.2.1 Subjects, Apparatus and Stimuli Two barn owls (Tyto alba), SL and, VS were cared for and treated according to the “NIH Guide for the care and use of laboratory animals” and were subject to regular inspections by the state veterinarian. For a detailed description of the behavioural apparatus and the stimuli see Chapter 2.

5.2.2 Behavioural procedures All birds were trained and tested in a two phase procedure (see section 2.3). In the training phase, the birds learned to correctly associate object and hole configurations of static RDSs with one of the two response alternatives (left or right response bar; see paradigm I of Figure 12 on page 27). Hereafter, psychophysical testing began. The psychophysical analysis of stereopsis involved four measurements: (1) effect of luminance contrast on stereoscopic depth perception, (2) determination of stereoacuity in static and dynamic RDSs, (3) effect of stimulus illumination on stereoacuity in static RDSs and, (4) measurement of the upper-depth limit in static and dynamic RDSs. The measurements 1 and 2 were performed by use of the method of constant stimuli, 3 and 4 were performed by use of the method of limits as described below. A detailed description of the basic behavioural procedures is given in Chapter 2. 82 On the Perceptual identity of Depth Vision in the Owl

Psychometric procedures: Anaglyph RDSs were employed to determine the influence of luminance contrast on the perception of stereoscopic depth. The luminance of the non-coloured dots (Inon−colour) was systematically changed using 2 ranges of 6 luminance levels: .00, .10, .27, .50, .81 1.2 cd/m2, and 1.2, 1.7, 2.2, 2.7, 3.4 4.0 cd/m2. The red filter diminished the non-coloured luminance levels with a factor 19.2, the green filter with a factor 4.8. The luminance levels of the red and green dots (Icolour) measured through the red and green filter were .25 and .06 cd/m2, respectively. Consequently, the tested luminance contrast levels approximated -1.0 -.85 -.63 -.41 -.19 .00 .17 .29 .39 .48 .54. Relative contrast was given by the ratio (Inon−colour-Icolour)/(Inon−colour+Icolour). Also note, for a centred red or green stimulus, the extinction ratio equalled 1.5 and 6.2, respectively. The disparity of the figure in these static anaglyph RDSs equalled 6 arcmin. To ensure stimulus control, catch trail stimuli were used. Disparity of the figure region in these anaglyph RDSs—containing a black background—could be either +6 or, -6 arcmin and were presented with equal probability. The animals were tested with confined quasi-random sequences of trials. These blocks contained 6 catch trials and 6 test trials spanning a single luminance range. In total each luminance value was presented 25 times. Stereoacuity was measured using 15 retinal disparity levels i.e., ± 0, 1, 2, 3, 4, 5, 6 and 7 arcmin. Stimulus levels spanning two interleaved psychometric functions were presented in a randomly intermixed sequence of separate blocks to form a single psychometric session. In turn, each block contained a balanced quasi-random sequence of 10 images belonging to a single stimulus pair. Thus for any given block two stimulus levels were used that only differed in their sign, unless the disparity value was set to be 0 arcmin. In total each disparity value was presented 50 times.

Tracking procedure: The upper-depth limit for both object (r<0) and, hole (r>0) RDSs was determined separately using an one-up/one-down adaptive tracking procedure. Each correct/false detection resulted in a 5 arcmin increase/decrease for hole RDSs and a 5 arcmin decrease/increase for object RDSs, starting at +5 or -5 arcmin, respectively. To ensure stimulus control, catch stimuli were presented 50% of the time. Disparity of the ﬁgure in the catch trials equalled +18 or -18 arcmin, when tested with a object or hole RDS, respectively. The dependency of stereoacuity on the grey dot luminance level in static polarised RDSs was determined using an intermixed one-up/one-down adaptive tracking. In this case, both crossed and un-crossed RDSs were intermixed and presented from balanced quasi-random sequence. Each correct/false detection resulted in a 5 arcmin decrease/increase for hole RDSs and a 5 arcmin increase/decrease for object RDSs, starting at +5 or -5 arcmin, respectively. In total, eight grey-dot luminance levels 2 (Imax) were used i.e., .026, .022, .018, .012, .008, .006, .004, .002 cd/m . Luminance Chapter 5: The functional signiﬁcance of owl stereoscopic vision 83

contrast was set to 0.9 in order to make the luminance of the background (Imin) measurable. Contrast was given by the ratio (Imax-Imin)/(Imax+Imin). Consequently, the average level of illumination of the test RDSs equalled (Imax+Imin)/2. In both tracking procedures, a reverse in the direction of stimulus level was taken to be a single reversal and testing was continued until seven reversals took place. Such a sequence of trials represented a single run.

h b a r l l i d a f- a n c im p u k e o b a g r a g a g c e k k FILTER m c g p -i a a lf b ro ir a e u RED GREEN h it n h d w L O c l H o e W G n I v t e H l r

a t s s t a

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OBJECT HOLE

Figure 39: Reversal of depth in a red/green anaglyph RDS caused by a change in the background luminance. Along the positive diagonal (moving downwards) shown are two half-images with green+white and red+white dots, respectively. Along the negative diagonal (moving downwards) shown are two half-images with red+black and green+black dots, respectively. Furthermore, green on black and red on white will be seen with high contrast through the green filter. Conversely, red on black and green on white will be seen with high contrast through the red filter. If a subject wears a spectacle with a red and green filter that matches respectively the red and the green in the anaglyph RDS then the background luminance determines through which filter the red, or alternatively, the green coloured half-image will be seen with high contrast. This dependency reverses when the background is switched from black to white or vice versa. 84 On the Perceptual identity of Depth Vision in the Owl

5.2.3 Data analysis Data were collected in a successive viewing of a balanced quasi-random sequence of images belonging to a single stimulus pair. With the stimuli presented in this manner, 100% correct represents perfect discrimination and 50% chance responding. The obtained psychometric functions represented the probability that the owl’s response indicated the presence of a hole RDS as function of the varied parameter (i.e., disparity or luminance) and were fitted to the data by use of a logistic function. For this purpose an adapted version of the Psychophysica Mathematica notebook was used (Watson and Solomon, 1997). In all plots of the psychometric functions, the vertical grey bars indicate 95% confidence intervals. For the purpose of graphical display, it was assumed that the errors were normally distributed, and the 95% confidence intervals were calculated as described by Watson and Pelli (1983). Trials in which the animals responded to early (prior or, just 100 msec after stimulus onset) were discarded from the data. A single psychometric function was fitted to the data that combined at least 5 successive psychometric sessions in which the individual slopes deviated less than 20% from the mean slope. The position of the individual psychometric functions for stereoacuity determination constituted a measure of the owl’s bias (disparity at 50%). The stereoscopic thresholds for negative and positive disparities were estimated separately by use of a bootstrap method (Foster and Bischof, 1991). In this procedure, 75% correct was taken to be the threshold for positive, and 25% correct was taken to be the threshold for negative disparities. During tracking, the threshold value was calculated from six individual runs. In each run, the first two reversals were discarded and the remaining five reversals were averaged to derive an estimate of the threshold. Data of a single run were omitted the performance on the catch trials fell below 83% correct. The final threshold value was taken to be the mean value of 6 successive estimated thresholds which did not deviate more than 10% from the mean value.

5.3 Results

5.3.1 Stereopsis and its dependence on contrast When humans wear spectacles with a red and green filter that matches respectively the red and the green in anaglyph RDSs then the background luminance induced by the non-coloured dots determines through which filter the red or alternatively, the green coloured half-image will be seen with high contrast, as explained in Figure 39. This dependency reverses when the background is switched from black to white or vice versa. Effectively, switching from a black to a white background reverses the perceived Chapter 5: The functional significance of owl stereoscopic vision 85 depth because the half-images presented to each of the eyes are exchanged and hence change the sign of disparity. Thus, in one instance, using a black background, a hole configured RDS is perceived, or alternatively, when a white background is used, an object configured RDS is perceived.

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Figure 40: Reversal of perceived depth caused by a change in background luminance of red/green anaglyph RDSs with owls SL and VS. The used background luminance levels correspond with the following relative luminance contrast levels: -1.0 -.85 -.63 -.41 -.19 .00 .17 .29 .39 .48 .54. See section 5.2.2 for details. The psychometric functions represent the probability that the owls’ response indicated the presence of an object configured RDS. When performance equals 0% correct the RDSs are perceived to be holes and 50% correct indicates that depth perception is lost. If, however, performance equals 100% correct than the RDSs are perceived to be objects. The psychometric functions were fitted to the data by use of a logistic function. Each data point represents at least 24 trials and the vertical grey bars display 95% confidence intervals. 86 On the Perceptual identity of Depth Vision in the Owl

Moreover, it has been shown for human subjects that thresholds for the detection of depth in dynamic RDSs are effected by luminance contrast. At low contrasts, stereoacuity is inversely proportional to the square of luminance contrast (Cormack et al., 1991). Thus, it is to be expected that when owls are presented with low contrast anaglyph RDSs, then their discriminative behaviour should be diminished severely. In other words, an animal that has learned to respond differently to object and hole configured RDSs should change its responsive behaviour systematically when the luminance level of the background dots (and hence luminance contrast) in anaglyph RDSs is changed in small discrete steps. The psychometric functions, presented in Figure 40, illustrate the depth reversal effect as outlined above. Depth perception was evidently effected by the changes in the luminance contrast of the stimuli. As the background luminance of the hole configured RDSs increased, the probability of perceiving an object RDS increased. Moreover, in absence of any disparity information, when relative contrast was rather low—ranging from -.19 to .17—, the owls’ performance was at chance level. Interpolation of the data indicats that the owl’s critical Michaelson contrast value, when performance equalled 25% or 75% correct, approximates .4 for RDSs with a retinal disparity of ±6 arcmin. In other words, stereoacuity in the owl lies around 6 arcmin at a .4 contrast level. The latter is a factor 3 higher when compared with stereoacuity at a contrast level of 1.0 (see section 5.3.2). Note performance to the catch trial RDSs remained reliable throughout the whole of the experiment for both owls.

5.3.2 Stereo acuity The investigations of stereoacuity were performed by using the depth classification task with both static and dynamic RDSs. Note the background pattern was always kept non-disparate with respect to the stimulus presenting display. Consequently, the owls had to indicate the direction of the perceived depth of the stereoscopic form (object versus hole) relative to the surrounding background. By plotting the owl’s correct responses that indicated the discrimination of a hole configured RDS as function of the difference in retinal disparity between figure and ground, as is shown in Figure 41, one can easily determine response bias (50% correct) together with the stereo acuity for both negative and positive disparities. Figure 41 illustrates two important aspects of the behaviour expected from animals with stereopsis. First, the discriminative behaviour of the owls was directly coupled with the sign and magnitude of the disparity of the stereoscopic form. Performance ranged from zero for the largest negative disparities to 100% correct for the largest positive disparities with the slope reflecting the sensitivity of the subject’s depth perception. Stereoacuity Chapter 5: The functional significance of owl stereoscopic vision 87

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Figure 41: Psychometric functions obtained during the depth discrimination task (object versus hole RDSs) with owls SL and VS when viewing static (A) and dynamic (B) displays of polarised RDSs. All plots represent the percentage of trials in which the owl’s response correctly indicated the presence of a hole configured RDS as function of retinal disparity, r. The sign of the object and hole RDSs disparities were designated negative and positive, respectively, relative to the non-disparate background. Response bias (50% correct) is indicated by the dashed lines. Each data point represents at least 40 trials and the vertical bars display the 95% confidence intervals. The slopes, denoted by g, of the individual curves reflect the sensitivity of the owl’s depth perception. The steeper the slope the more sensitive the subject. 88 On the Perceptual identity of Depth Vision in the Owl values measured with static RDS were somewhat higher for negative disparities [SL: -2.3±.3 arcmin; VS:-2.9±.4 arcmin] when compared to positive disparities [SL: 1.9±.3 arcmin; VS: 2.0±.4 arcmin]. Stereoacuity values measured with dynamic RDSs were comparable for both negative [SL: -2.3±.4 arcmin; VS: -3.1±.4 arcmin], and positive [SL: 2.3±.4 arcmin; VS: 2.4±.4 arcmin] disparities. And when comparing between individuals, owl SL turned out to be more sensitive [g=.6] than owl VS [g=.4]. Turning to the aspect of the applied RDS presenting method, i.e., static versus dynamic RDSs, it can be appreciated from Figure 41 that the owls were equally sensitive to dynamic RDSs as compared to static RDSs. Second, both owls showed a very small but consistent bias to negative disparities to both static [SL: -0.3±.2 arcmin; VS: -0.5±.3 arcmin], and dynamic [SL: -0.0±.3 arcmin; VS: -0.4±.3 arcmin] RDSs, as indicated by the dotted lines in Figure 41. This small negative displacement of the psychometric function on the disparity axis (stereo-bias) represents an asymmetry in the sensitivities of the mechanisms for detecting negative and positive disparities. Both owls tended to be more sensitive towards positive than to negative disparities. This aspect of imbalanced stereopsis for negative and positive disparities was evaluated by logistic regression (Hosmer Jr and Lemeshow, 1989) on the pooled psychometric data to static and dynamic RDSs for each of the subjects. In turned out that the imbalance in stereopsis for negative and positive disparities was not significant [Logistic regression, df=2; owl SL: P (χ2=120)<.0001, 1486 observations; owl VS: P (χ2=118)<.0001, 1473 observations].

5.3.3 Stereo acuity as function of luminance

The investigation of stereoacuity at low luminance levels was performed by using static RDSs in an intermixed tracking procedure and without any attempt to dark-adapt the owls. Note that the viewing distance was set at 2.0 meters to obtain the required luminance levels. Despite the significant difference in sensitivity between the owls the two functions relating stereoacuity to luminance (Figure 42) had a similar shape. Decreasing the lu- 2 minance of the RDSs down to .012 (-2 log10) cd/m had little effect on the stereoacuity. 2 When luminance was reduced to .002 (-2.7 log10) cd/m , however, stereoacuity de- teriorated at least two-fold. Thus, the data show, as found in humans (Mueller and Lloyd, 1948), that the found relationship is asymptotic. Note also, that luminance contrast was not maximal (1.0) but equalled 0.9 to produce a measurable background luminance. Chapter 5: The functional significance of owl stereoscopic vision 89

5.0 ] n i 4.5 m c r a [

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Figure 42: Stereoscopic threshold as function of stimulus illumination in owls SL (grey line) and VS (black line) to static RDSs. Data points represent the mean value of 6 successive runs determined with the intermixed tracking procedure. The vertical bars denote the standard deviation at each data point. 90 On the Perceptual identity of Depth Vision in the Owl

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o 40 40 n i 30 30 B 20 20 10 10 0 0 0 20 40 60 80 100 120 0 20 40 60 80 100 120 140 Hole RDS test trial number

Figure 43: Graphical representations of upper disparity limit measurements with negative (Object RDSs: upper four plots) and positive (Hole RDSs: lower four plots) disparities in owls SL and VS. dmax (dotted lines) was determined for both static (open area) and dynamic (grey area) RDSs. Performance to the catch trial RDSs remained reliable (>85%) for both owls throughout the whole of the experiment. Chapter 5: The functional signiﬁcance of owl stereoscopic vision 91

5.3.4 Upper limit of stereopsis The upper limit of stereopsis is often interpreted as the diplopia or fusion threshold, when in fact it is not the disparity at which differences in depth can still be perceived accurately and diplopia (double vision) begins, or alternatively, fusion is lost (see e.g., Duwear, 1983; Arditi, 1986). Moreover, it is important to note that diplopia per se does not exist for RDSs (Tyler, 1990). No matter how large the disparity, an RDS will not appear diplopic in the sense of being perceived with twice the dot density, although the static type of RDS will eventually go into rivalry (Tyler, 1975). Dynamic RDSs do not exhibit rivalry, and are in some sense always fused. I avoid, the terms “diplopia” and “fusion”, because the here used behavioural procedure and RDS stimuli do not allow to differentiate between the loss of single vision and the loss of depth perception of non-fusable images. Instead I used dmax—maximum shift of the stereoscopic region in RDSs—as a measure for nondepth- producing disparities. Note dmax is here expressed in retinal disparity: an angular measure related to the owls’ interocular distance. Graphical representations of the dmax measurements are shown in Figure 43 for negative and positive disparities, respectively. The dmax values for positive disparities measured with either static (SL: 46±2; VS: 49±3, open area Figure 43), or dynamic RDSs (SL: 54±2; VS: 47±2, shaded area Figure 43) were significantly lower when compared with dmax values for negative disparities of static (SL: -99±3; VS: -99±3, open area Figure 43), or dynamic presented RDSs (SL: -94±3; VS:=-90±2, shaded area Figure 43). Generally, depth perception was lost at somewhat lower dmax values for dynamic RDSs than was the case for static RDSs and the upper disparity limit extended up to 99 arcmin of retinal disparity depending on the stimulus configuration. That is, the sign of the difference in disparity between figure and ground.

5.4 Discussion

5.4.1 Methodological issues Dichoptic stimulation of the eyes with RDSs is a very powerful technique in animal studies because a positive result makes it very likely that the discrimination was indeed being solved by stereopsis (Fox, 1978; De Valois and De Valois, 1980). Nonetheless, there are also several disadvantages and limitations to this stimulus presenting technique (Yeh and Silverstein, 1990; Patterson et al., 1992; Wann et al., 1995) and RDSs can be contaminated by monocular cues originating from the technique that created the disparities (Julesz, 1971, Cobo-lewis, 1995). Such a contamination might not be obvious to human observers. In the here described experiments, a change in the disparity content of the 92 On the Perceptual identity of Depth Vision in the Owl stimulus display that occurred during the transition form the observation random-dot pattern to the static RDSs could have produced a monocular detectable cue: apparent motion. To ensure that this artefact did not aid the owls’ performance I also used dynamic RDSs. That is, by coherently updating the random-dot distributions of each half-image with a high frequency apparent motion will be eliminated when the disparity is changed. For example, a significant lower dmax value obtained with dynamic RDSs as opposed to that measured with static RDSs may indicate that performance was affected by the motion signal that occurred when the observation stimulus was replaced by a static RDSs. Nevertheless, this was only the case for owl VS when presented with large negative disparities (Figure 43). Moreover, stereoacuity remained unaffected irrespective of fashion with which the RDSs were presented (Figure 41). An important aspect of the described manipulation of contrast levels in anaglyph RDSs is that this depth reversal test (for explanation see Figure 40) can be used to unambiguously demonstrate stereopsis in animals as will be explained below. For example, the study on stereopsis with an Kestrel (Fox et al., 1977) revealed that the falcon’s best performance on RDSs occurred in a disparity band between 8-12 arcmin. This is a rather puzzling finding, because 8 arcmin is a value well above the spatial resolution of this bird (Hirsch, 1982; Fox, Lehmkuhle and Westendorf 1976). This suggests that the discrimination was based on a monocular, rather than a binocular depth cue because stereopsis is highly sensitive to very small differences in disparity (see also McFadden, 1993). However, when stereopsis in the falcon would have been examined with the depth reversal test, one could have avoided the above described problem that discrimination is confounded by a monocular detectable cue that probably originated from the use of large disparity values. That is, in the depth reversal test the disparity content in the stimuli is invariant and the sign of disparity is only signalled through the polarity of the stimulus contrast. Thus all RDSs contain the same monocular artefact. In this respect, it is important to note that the animal should initially be trained with non-coloured RDSs. Otherwise a change in performance is not necessarily based on a reversal in perceived depth but could instead be guided by a change in contrast polarity.

5.4.2 The effect of contrast and stimulus illumination Stereopsis arises from a number of processes, some of which are interdependent, and some of which are dissociable. In my view there are two main dissociable components that limits stereoscopic depth perception other than spatial resolution and the range of convergence eye movements. These are luminance contrast and stimulus illumination. The result of the depth reversal experiment (Figure 40) indicate that stereopsis in the owl improves substantially with increasing levels of luminance contrast as has Chapter 5: The functional significance of owl stereoscopic vision 93 been found in humans (see e.g., Cormack et al., 1991). Figure 40 also suggests that stereopsis has a weak dependence on contrast levels at suprathreshold levels (e.g., performance at background luminance levels in the range .0 to .8 cd/m2 and 2.6 to 4.0 cd/m2). However, discriminative performance declines rapidly as contrast becomes very small (to what is presumably the contrast threshold) at background luminance levels in the range .8 to 2.4 cd/m2. The latter is what one would expect when performance is limited by a constant level of intrinsic noise. This in turn would suggest that disparity in the owl is obtained from visual information that has been filtered through channels tuned to different spatial frequencies (see e.g., Marr and Poggio, 1979). There is also evidence in humans which suggests that irrespective of the involved spatial filter mechanisms, higher contrast levels are required for stereopsis than for simple detection (Frisby and Mayhew, 1978). Because the green filter extinction ratio was relatively high compared to that of the red filter (see section 5.2.2 on page 82) contrast could not be balanced perfectly in the two eyes. Therefore, no attempt was made to measure stereoacuity as function of stimulus contrast. Thus, to obtain a more detailed view of the effect from luminance contrast on stereoscopic sensitivity further study is warranted. Nonetheless, the data of Figure 40, when compared with that of Figure 41, indicate that the stereo threshold rises with a factor 3 when the Michaelson luminance contrast decreases with a factor 2.5. This is not consistent with the finding that human stereoacuity is proportional to the square of contrast (Cormack et al., 1991) and could be explained by the fact that owl stereopsis requires less stimulus energy than is required for simple monocular detection. In other words, the constant level of intrinsic noise in the owl stereoscopic system appears to be lower than that of the human stereoscopic system. Another important factor that can determine stereoscopic sensitivity is the intensity of illumination of the stimulus. Most notably, in humans subjects—tested with line stereograms—a discontinuity in the asymptotic function relating stereoacuity to luminance is evident as luminance is reduced from the mesopic into the scotopic range 2 at between -0.5 and -1.5 log10 cd/m (Mueller and Lloyed, 1948). I measured owl stereoacuity at the lower end of this range of illumination (Figure 42), but a decrease 2 in luminance down to -2 log10 cd/m had no significant effect. Only at levels lower 2 than -2.3 log10 cd/m , sensitivity to binocular disparity started to deteriorate significantly. The absence of a discontinuity in the here found asymptotic function relating stereoacuity to luminance was to be expected because of two reasons. First, the owls were not dark adapted, the animals performed only 10 to 15 minutes in darkness and in between measurements they were exposed to photopic levels of illumination (1 log10 cd/m2). Second, the luminance levels used may have been above the owls’ cone and rod threshold (Ochme, 1961; Fite, 1968; Martin et al., 1975; Martin, 1977). Thus it remains unclear whether stereo sensitivity in the owl depends on both cones and rods in the light adapted state. 94 On the Perceptual identity of Depth Vision in the Owl

Livingstone and Hubel (1994) noted that human stereopsis to RDSs is also pos- 2 sible in the dark-adapted state. That is, 90% correct at -3 log10 cd/m for 10 trials with disparity ranging from 10 up to 100 in steps of 10 arcmin. This ﬁnding, however, 2 would suggest that at -3 log10 cd/m human stereopsis is not hyperacute (see section 5.4.3) and that global stereopsis in humans is only marginally better than in owls (see Figure 42). Although, this result was not discussed in relation to what causes this diminished depth sensitivity, it indicates that global stereopsis in humans is limited by quantal noise whereas this seems not to be the case in the owl; at least not for 2 luminance levels as low as -3 log10 cd/m (see also section 7.3).

5.4.3 Stereoscopic resolution Stereoacuity: The here determined stereoacuity thresholds (± 2 arcmin of retinal disparity) are in agreement with psychometric functions reported for primates (Harwerth and Boltz, 1979a), but are almost a factor 6 higher when compared with stereoacuities measured in humans and macaque monkeys which has been measured in the 0.3 to 0.7 arcmin range (Tyler, 1991; Tang, et al., 1995). Factors contributing to this rather low stereoacuity in the owl may have been: (1) the large size of the stereoscopic figure, since thresholds are only low with small stimuli composed of high spatial frequencies (Patterson, 1992), (2) the low spatial resolution of the owls retina when compared to the that of the human eye (Wathey and Pettigrew, 1989), (3) the interocular separation in humans is approximately 1.5 times that of owls and accordingly, only 2/3 the physical distance is required to obtain the same retinal disparity for humans as for owls and (4) the relatively large viewing distance. It is well known that a large viewing distance can have a significant effect on stereo sensitivity in humans—beyond 150 cm disparity scaling is less than veridical (see e.g., Cormack, 1984; Johnston et al., 1994). I used a viewing distance of 150 cm because this is the distance from which the barn owl usually attacks its prey (Curtis, 1952; Clarke, 1983; Erichsen, 1985). Nonetheless, the owls’ sensitivity to small disparities cannot be explained on the basis of probability summation alone—a simple two-point discrimination by each eye working in isolation. As the results indicate each eye would have to be able to discriminate a visual angle of only 0.8 arcmin, whereas data on retinal ganglion cells density of the barn owl’s eyes predicts only a spatial acuity of 4 arcmin (Wathey and Pettigrew, 1989). The later value—photoreceptor spacing—gives rise to a binocular-monocular sensitivity ratio of .2 : 1.0. Probability summation, on the other hand, would predict a ratio of .8 : 1.0, because in this case sensitivity increases in proportion to the square root of the number of observations (Campbell and green, 1965; Green and Swets, 1966). Thus, the precision of owls’ discriminative behaviour seems to reflect some sort of neural integration (stereopsis) which allows enhanced Chapter 5: The functional significance of owl stereoscopic vision 95 discriminability of the two monocular images. The stereoacuity measurements (Figure 41) did not reveal any asymmetry in sensitivity to negative and positive disparities. Stereoanomalies (i.e., strong biases to either negative or positive disparities) have been demonstrated in studies of cyclopean stereopsis with humans (Richards, 1971; Jones, 1977) and monkeys (Harwerth and Boltz, 1979). Other investigators, however, have reported that people classified as stereoanomalous when tested with brief exposure time perform normally when tested with longer exposure (Newhouse and Uttal, 1982; Patterson and Fox, 1984). Furthermore, stereoanomalies in humans also seem to subside with practice (Foley and Richards, 1974; Sowden et al., 1996). Interestingly, a bias to positive disparity was also found in the owls but this asymmetry in sensitivity disappeared almost completely after prolonged exposure to the RDSs along with a significant improvement in their stereo thresholds. The later has also been found in rhesus monkeys tested for local stereopsis (Harwerth et al., 1997).

Upper limit for stereopsis: In humans the upper depth limit may extend up to 2o of disparity for cyclopean stimuli, depending on stimulus configuration (Tyler and Julesz, 1976; Tyler, 1991). My measurements gave similar results: dmax in the tested owls extended up to -1.7o for negative, and up to .9o for positive disparities. This quantitative agreement (at least for negative disparities) and the size of the stereoscopic figure, 2.5o, suggest that in both cases the same perceptual phenomenon was measured. This phenomenon is known as patent stereopsis and refers to the perception of depth from large size stimuli (up to 6.6o), and fused or double retinal images (Ogle, 1964). While upper depth limits obtained with human subjects apply to both negative and positive disparities (Patterson, 1992), my measurements show a significant difference between positive and negative disparities. This finding, however, may be due to the lack of vergence eye movements in the owl. As pointed out by Howard and Rogers (1995), vergence movements made by human subjects may have had an effect because even briefly exposed stimuli with large disparities could evoke vergence responses that occurs after the stimulus has been removed. Thus, the subject’s judgements may be prompted by vergence rather than by a direct appreciation of depth. Furthermore, stimulus size above 2 arcmin can be the limiting factor for dmax in human stereopsis, —dmax increases with increasing stimulus size (Wilox, 1995). It is possible, therefore, that the here measured dmax values do indeed represent the upper limit of owl stereopsis since I used a stereoscopic figure that subtended 2.5o. 96 On the Perceptual Identity of Depth Vision in the Owl 6 STEREOPSIS AND MOTION PARALLAX PRODUCE SIMILAR IMPRESSIONS OF DEPTH

. . . In every object there is form; The mind shapes it into what the eye brings means of shaping. Between the one eyed and the two eyed, what a diﬀerent pair of Universes.

Abstract Although many sources of three-dimensional information have been isolated and demonstrated to independently contribute to depth vision in animal studies, it is not clear whether these distinct cues are perceived to be perceptually equivalent. Such ability is observed in humans and would seem to be advantageous for animals as well in coping with the often ambiguous information about the layout of physical space. I found that owls trained to detect relative depth as a perceptual category when speciﬁed by binocular disparity alone, immediately transferred this discrimination to novel stimuli where the equivalent depth categories were available only through motion-parallax information produced by head movements. The presence of primary-depth-cue equivalence in the visual system of the owl provides further conformation of the hypothesis that neural systems evolved to detect diﬀerences in either disparity or motion information are likely to share similar processing mechanisms because the nature of the information involved from stereopsis and motion-parallax can be related at a formal level (”spatial” versus ”spatial-temporal” disparities). 98 On the Perceptual Identity of Depth Vision in the Owl

6.1 Introduction

In primates (including humans) stereopsis and motion-parallax constitute the most effective visual sources for the recovery of depth from two-dimensional images (referred to as the ”primary-depth-cue” systems). When combined, these primary-depth-cue systems provide sufficient information to accurately perceive the three-dimensional (3D) layout of the environment (Richards 1985). Binocular disparity (disparity for short), the cue that underlies stereopsis, originates from viewing objects from two spatially separated vantage points (the left and right eye) at the same time (see for review by Howard and Rogers 1995). Motion-parallax, on the other hand, can be generated when static objects are viewed while moving ones head from side-to-side (Wallace 1959). Such translatory head movements are known as ”peering” and cause a larger retinal translation with higher velocities in close objects compared with objects that are more distant (Collett 1978). Thus, relative motion is the monocular cue that underlies motion-parallax. While disparity can be determined only by comparing the information in the two eyes at the same time (binocular vision), motion-parallax can be determined with a single eye (monocular vision). Human psychophysical experiments by Rogers and Graham (1982) were instrumental in showing that depth from disparity or from motion can yield similar levels of performance in tasks involving the measurement of depth sensitivity. The rationale behind making such a comparison was based on the insight that there are considerable similarities in the underlying computational theory of these two depth cues. Consider, for example, the condition in which the observer’s eye is moved through the distance that separates both eyes, and nothing is moved in the world: then depth computation of motion-parallax information (”spatio-temporal” disparity) is formally equivalent to that of ”spatial” disparity based stereopsis (Koenderink 1986; Bradshaw and Rogers 1996). In other words, motion-parallax can be described by the same geometry that governs stereopsis. Here, we introduce the expression ”primary-depth-cue equivalence” to refer to the ability to perceive mutual consistent depth information from either stereopsis or motion-parallax. This perceptual phenomenon has thus far only been demonstrated in humans (see for review by Howard and Rogers 1995). We hypothesized that if primary-depth-cue equivalence is indeed a consequence of the close formal relationship between stereopsis and motion-parallax then animals which are sensitive to differences in disparity should be able to perceive similar depth information based on relative motion. In a wide range of animal species depth discrimination based on stereopsis or motion-parallax has been demonstrated (see for review by Collett and Harkness 1982; Howard and Rogers 1995; Collett 1996; Kral 1998; Land 1999; Srinivasan et al. 1999). The possibility of primary-depth-cue equivalence, however, has not been tested in any Chapter 6: Stereopsis and motion parallax 99 of the species studied. In this respect, the owl provides an excellent animal model for such a test, because of the following considerations. First, barn owls possess a highly developed visual forebrain sharing many functions with the mammalian visual cortex (Karten et al. 1973; Pettigrew 1979; Medina and Reiner 2000; Nieder and Wagner 2000). Second, barn owls are capable of detecting the relative position of planar surfaces in random-dot stereograms (RDSs). That is, these birds can detect differences in depth (relative depth) using disparity as the sole cue for discrimination under experimental conditions (Figure 44) (van der Willigen et al. 1998). Third, barn owls are known to make head movements that resemble peering similar to that seen in insects that are sensitive to motion-parallax (Wagner 1989). Fourth, evidence of primary-depth-cue equivalence in the owl would be a strong indication that both the mammalian and, avian visual system have adopted a similar strategy to cope with the often co-varying information about the layout of physical space; this irrespective of the fact that binocular vision has evolved independently in mammals and birds (Karten et al. 1973; Pettigrew 1979; Medina and Reiner 2000; Nieder and Wagner 2000). To determine whether or not the owl visual system is capable of primary-depth- cue equivalence we trained two barn owls with an operant procedure (Figure 44A) and developed one set of stimuli specifying depth through binocular disparity, and a second set of interactive stimuli to mimic observer-produced motion-parallax (Figure 44B). A ”transfer” procedure (van der Willigen et al. 1998) was then used to assess whether or not the animals treated a particular depth configuration as being equivalent when specified by a ”novel” depth cue.

6.2 Methods 6.2.1 Animals and behavioural apparatus Two barn owls (Tyto alba), SL and, VS were cared for and treated according to the “NIH Guide for the care and use of laboratory animals” and were subject to regular inspections by the state veterinarian. The owls viewed the stimuli through a set of diﬀerently polarized ﬁlters—to control for stereopsis—and were interactively connected to the stimulus generating unit via a head-tracking sensor (Figure 44). Head tracking allowed the simulation of motion parallax during peering. A detailed description of the behavioural apparatus is given in Chapter 2.

6.2.2 Stimulus conﬁguration and parameters For a detailed description of the stimuli see section 2.4 of chapter 2. Here I suﬃce with a brief overview. 100 On the Perceptual Identity of Depth Vision in the Owl

Three types of depth stimuli were employed: random-dot stereograms (RDSs), random-dot kinematograms (RDKs), and motion-parallax displays (MPDs).These were displayed on a 150 cm distant cathode ray tube (CRT: P22-phosphor colour monitor; ELSA 17H96; interlaced stereo mode resolution at 120 Hz: 1280 H x 496 V pixels; http://www.elsa.de) using a multi-platform environment for developing portable, interactive 2D and 3D graphics applications (OpenGL: http://www.open.org). All stimuli were segmented into two distinct random-dot areas: (1) a large ”ground” (450 x 450 dot matrix), and (2) a smaller inner ”figure” region (150 x 150 dot matrix) and could be configured into two categories: OBJECT versus HOLE (Figure 44B). The dot matrices contained equal amounts of randomly placed grey and black ”squared” dots, 1 x 1 min of arc, with a luminance of .36 cd/m2 and .00 cd/m2, respectively. In addition, a 450 x 450 random-dot (ground-only) pattern functioned as the ”observation” stimulus. Note luminance was measured at the viewing distance (see below) through the polarizing liquid crystal display plus the polarized filters of the spectacles (Figure 44A) by averaging over at least 70 dots, using a Minolta LS-100 light meter (http://www.minoltainstruments.com). Note also, at any time, the stimuli were viewed through the polarized filters plus the polarizing display. Viewing distance was set to be 150 cm, because under natural conditions barn owls usually fly low (between one and two meters from the ground) just before they dive onto prey with talons extended (Martin 1990). Disparity was experimentally isolated using Julesz random-dot stereograms (RDSs) and relative depth in the employed RDSs was configured in two basic ways. They either revealed a surface floating in front or behind a similarly textured, larger random-dot pattern. I refer to these as “object” and “hole” depth configurations, respectively. Differerences in disparities of the dots were created through a time-multiplexed polarizing liquid crystal display modulator as described earlier (van der Willigen et al. 1998). That is, the differences in disparity between figure and ground were either -11 (hole RDS) or 11 min of arc (object RDS). Retinal disparity was calculated using an inter-ocular distance value of 45 mm (Cormack and Fox 1985). Motion in the MPDs was continuous (refreshed at a rate of 100 Hz) and coupled with side-to-side head movements (closed-loop condition). By varying the sign and magnitude of this coupling it is possible to simulate the parallax corresponding to a target at any experimenter-specified distance. When the sign is <0, then a hole is simulated, however, a sign >0 simulates an object. The geometry of this relationship has been described elsewhere (Sobel 1990). The configuration and parameters of the MPDs are explained in Figure 16. Stimulus transformation could occur in two- dimensions: horizontal, X-axis, and/or vertical, Y-axis (Figure 44A). The gain was set to be 1/10. As a result, the simulated difference in depth of the figure relative to the ground in object or hole configured MPDs approximates -13.6 cm or +16.7 cm, respectively; assuming a viewing distance of 150 cm. The latter is equivalent to object Chapter 6: Stereopsis and motion parallax 101 and hole RDS of approximately -10.3 min of arc or +10.3 min of arc, respectively.

A itor mon ulus stim spectacle frame + wired sensor

nal latio ans t tr men li ove ne of sight d m hea

er feed play dis +Y izing olar p HOLE

h magnetic field perc OBJECT transmitter

B Training RDSs Test MPDs STEREO MOTION

OBJECT HOLE OBJECT HOLE

Figure 44: Drawing of the experimental design and stimuli. (A) An owl wearing spectacles is shown while viewing a random-dot stimulus through the polarising display system (LCM). A push on either the HOLE or OBJECT response bar could be reinforced with a reward made available from the feeder. The owl’s head-movements were tracked in real-time by use of a small wired sensor in combination with a magnetic-ﬁeld generator. (B) Examples of the training and test stimulus pairs. Note each stimulus of such a pair was shown in isolation, and the pictorial black outlines - shown to depict depth and boundaries of the inner region - were not present in the displays used. The white arrows indicate the direction of movement of the dots that comprised the inner region. The black arrows indicate the head-movement direction. 102 On the Perceptual Identity of Depth Vision in the Owl

Motion in the RDKs was independent from the owl’s own movements and consisted of a sequence of discrete horizontal displacements (open-loop conﬁguration). The leading edge of the dot displacement was always initiated at the left-side border of the centrally positioned ﬁgure region. The dots were shifted rightwards by 3 dots each frame. The number of frames per second equalled 10; giving rise to an angular velocity of .5 deg s−2 assuming that a 150 cm distant owl remained motionless (i.e., passive viewing). By means of the head-tracking device we were able to verify on-line whether or not the owls kept their heads stationary.

6.2.3 Behavioural procedures, tests and controls All birds were trained and tested in a two phase procedure (see section 2.3) and a detailed description of the basic behavioural procedures is given in Chapter 2. Otherwise see the results section of this chapter During testing, stimuli were conﬁned to blocks of 12 trials. A single block contained only one stimulus type: RDSs, MPDs or RDKs. A trial was initiated after the owls attended (motionless) to the observation stimulus for up to 6 seconds. Trials in which the owls responded too quickly (100 msec after stimulus onset) were aborted and repeated somewhat later within the same session. When head movements occurred while viewing a RDK, the same correction procedure was enforced. On a daily basis the transfer tests consisted of two sessions. In the ﬁrst, ”stereo-and-feedback” session, the training RDS stimuli appeared, then in the second session stimuli were switched to the novel depth stimuli - either MPDs or RDKs. By only rewarding the owls for correct responses during the stereo-and-feedback sessions the owls were reminded of their discriminative task. To avoid feedback during the motion-parallax and no-head-movement sessions, however, the birds were rewarded in all cases regardless of the correctness of their behaviour (unconditional reinforcement).

6.2.4 Data analysis and off-line analysis Data were collected with a predetermined list of a balanced (quasi-random) sequence of objects and holes. With the stimuli presented in this manner, 100% and 50% correct responses represent perfect and chance discrimination, respectively. The P values in the main text and figures represent the independent binomial probability calculated from the number of correct and incorrect responses with an expectation of .5 of being correct. Head position signals were calibrated on the basis of stationary positions obtained during the stereo-and-feedback sessions. Peering movements (Wallace, 1959; Collett, 1978; Wagner, 1989) were analysed off-line by use of a computer algorithm which Chapter 6: Stereopsis and motion parallax 103 applied separate velocity and displacement direction criteria for peering movement reversal points, onset and offset, respectively. Examples of peering movements as detected by the above described algorithm are shown in Figure 45. The periodicity of a single peering movement was measured by determining the shortest duration of the individual oscillation periods (for details see Figure 45).

Peering C

Head position Head position m m c

2 2

1sec 1sec Fixation Fixation stimulus stimulus

MPD Stimulus on RDS Stimulus on

Bar Hit Bar Hit

Figure 45: (A) Spontaneous peering movements in owl SL and diagrams of the temporal sequence of events during one trial when either a MPD (B) or RDS (C) was presented. The peering movements differed in their amplitude and number of oscillation periods (A). Peering amplitude equaled the absolute distance between the outer most reversal points. An oscillation period was defined as the time that it took the owl move its head from the starting position to a reversal point and back. Note, as soon as the RDS appeared (C)) the owl responded whereas in case of the MPD (B) the owl only responded after making a peering movement. This change in response latency occurred because the owls could only become aware of the switch between the fixation stimulus and the MPD stimulus when peering was initiated, whereas switches from fixation stimulus to RDS became immediately evident to the owl. 104 On the Perceptual Identity of Depth Vision in the Owl

6.3 Results and Discussion

6.3.1 Behavioural task

Two owls were conditioned in a two-phase behavioural procedure. First, training with a stereoscopic depth classiﬁcation task (“stereo-task”) took place under conditional reinforcement. To be rewarded, the owls had to correctly associate either “object” or “hole” random-dot stereograms (RDSs) with one of the two response alternatives (left or right response bar, Figure 44). After the birds attained reliable performance [83% correct for 70 consecutive trials; P (X = 83%) < .0001], the test-phase began.

6.3.2 Transfer to motion parallax stimuli:

Motion parallax transfer under binocular viewing conditions: In previous described perceptual tests of Chapter 4 I have used a discrimination-transfer procedure to show that owls are able to categorise RDSs into two distinct depth classes (object versus hole, see section 2.4.1) across a wide range of disparities. Using a similar discrimination-transfer paradigm, I presented the pre-conditioned owls with a succession of distinct random-dot patterns. These patterns remained constant only in their depth configuration (object or hole) irrespective of the stimulus condition used. Two distinct stimulus conditions were tested: (i) “stereo-and-feedback”, (ii) “motion-parallax”. In the stereo-and-feedback condition, the training stimuli appeared (Figure 46B). Throughout the motion-parallax condition the differences in disparity were eliminated and instead the owls viewed object and hole motion parallax displays (MPDs) (Rogers and Graham, 1982). Note, with this switch in stimulus conditions the owls could only perceive depth by actively moving their heads. Essentially, a small-circumscribed region of random-dots (“figure”) in the centre of a larger static field of random-dots (“ground”) was transformed with every head-movement, thereby generating relative motion (Figure 46B). Thus in terms of the interaction between image transformation and head position the MPDs provided a closed-loop condition. Examples of such peering movements are given in Figure 45. Both owls—naive to motion parallax stimuli—were successful in extracting and categorising the depth information from the distinct MPDs (open bars Figure 46A) by immediately choosing the appropriate response bars which they had previously learned to associate with either stereoscopic object or hole RDSs depth configurations (shaded bars, Figure 46A). Although, the difference in performance to the learned RDKs (STEREO) and the novel MPDs (PARALLAX) was significant [Wilcoxon rank- sum test, SL: t(16)= 6.3, p<.001; VS:t(16)= 4.2, p<.001], performance to the MPD stimuli deviated significantly from chance performance in both owls [binomial indepen- Chapter 6: Stereopsis and motion parallax 105 dent probability (108 trials), SL: P (X = 77%) < .0001, VS: P (X = 67%) < .0001]. Closer inspection of the stimulus response relationship on the test trials (Figure 47) revealed that the birds, treated the hole and object MPDs as different [Pearson chi- square test, SL: χ2(1) = 31, p<.001; VS: χ2(1) = 18, p<.001]. This irrespective of the fact that owl VS had significant more difficulty to discriminate object from hole MPDs [Wilcoxon rank-sum test, VS: t(7)= 2, p<.05].

A B

T P<0.001 SL

C 100 T E R R A R I N O I C 80 N

E G G

S A T T I

60 M N U E L C I R E

P 40 STEREO PARALLAX

T VS C 100 P<0.001 E R T R E S O T C 80

S E T G I M A T U

N 60 L E I C R E

P 40 STEREO PARALLAX

Figure 46: Successful transfer with owls SL and VS to motion parallax stimuli after prior training on pure stereoscopic stimuli (A) and two sets of stimulus pairs (B). A: The histograms depict the mean percentage correct performance of 9 sessions with the training pair (shaded bars, SL: 95±4; VS: 91±3) and the test pair (open bars, SL: 77±6; VS: 67±5). The error bars indicate standard deviation. B: Shown are two sets of hole versus object conﬁgured stimulus pairs. The upper pair (training stimuli) contained no cues other than binocular disparity. The lower pair (test stimuli) contained no cues other than relative motion. 106 On the Perceptual Identity of Depth Vision in the Owl

A B T

C 100 SL Response alternative E LEFT RIGHT R e v R i E t L O a O n C r 80 42 12 54 H e E t

l correct false G a

T s A C u T l E u N 60 J 13 41 54 B E m i t O C false correct S R

E 55 53 P 40 HOLE OBJECT T

C 100 VS Response alternative E LEFT RIGHT R

P < 0.05 e R v i t E O a L C n O

80 r 40 14 54 e H E t false l correct G a

T A s C T u l E N u 60 J 18 36 54 E B m i t C false

O correct S R

E 58 50 P 40 HOLE OBJECT

Figure 47: Transfer performance of owls SL and VS on motion parallax stimuli (object versus hole) (A) and their respective stimulus-response matrices (B). A: The histograms depict the mean percentage correct performance from 9 sessions on hole (shaded bars, SL: 77±8; VS: 74±8), and object sessions (open bars, SL: 77±6; VS: 67±5). All performance levels differed signiﬁcantly from chance [independent binomial probability calculated for 54 responses, p <.005]. The error bars indicate standard deviation. B: Shown are the absolute number of outcomes on the hole and object trials. Numbers outside the cells indicate the sum of the respective rows and columns. Note both owls viewed the motion parallax stimuli under binocular conditions.

Motion parallax tested under monocular viewing conditions: The MPD discriminations, however, used binocular viewing. Consequently, stereo and motion parallax information specified incompatible depth cues. This conflict could have been the source of the observed diminished performance during the MPD condition when compared to the performance on the RDS trials (open bars, Figure 46A). To avoid conflicting depth information, I tested one owl under monocular viewing conditions using an eye patch. Nevertheless, results similar to those found during binocular viewing (Figure 47B) were obtained when the MPDs were viewed under monocular conditions (Figure 48C)[Pearson chi-square test, Left eye: χ2(1) = 16, p<.001; Right Chapter 6: Stereopsis and motion parallax 107

Eye: χ2(1) = 5.4, p<.02]. Note that performance during the left eye occlusion (right plot, Figure 48B) was somewhat hampered because owl SL was very unwilling to perform the task under these conditions.

A Left eye Right eye T 100 C E R R

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T T s s C C u u l l E E u u J 5 19 24 J 9 15 24 B B m m i i t t

O false false correct O correct S S 24 24 26 22 Monocular viewing left eye Monocular viewing right eye

Figure 48: Successful transfer with owl SL to motion parallax stimuli under monocular viewing conditions. A: The histograms depict the mean percentage correct performance of 4 sessions with the training stereo (shaded bars, Left eye: 88±8; Right eye: 75±11), and the test motion parallax stimulus pair (open bars, Left eye: 79±5; Right eye: 67±10) B: The histograms depict the mean percentage correct performance from 4 sessions on hole (Left eye: 79±1; Right eye: 71±14), and object trials (Left eye: 77±9; Right eye: 63±5). The error bars indicate standard deviation. C: Shown are the absolute number of outcomes on the hole and object trials. Numbers outside the cells indicate the sum of the respective rows and columns. 108 On the Perceptual Identity of Depth Vision in the Owl

6.3.3 Peering behaviour In the MPD tests the owls were free to move their heads. Peering movements exhibited variable amplitudes and speeds. To ﬁnd out more about the role of these parameters, peering amplitude was divided into three distinct bands: <2, 2-6, and >6 cm. This division was motivated by the reasoning given below.

Owl SL: binocular Owl VS: binocular 30 30

E N=54 N=54 L r O e 20 20 b H

10 10 n

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T 10 10 R

20 20

B CORRECT CORRECT

O INCORRECT N=54 INCORRECT N=54 30 30 < 2 [2-6] > 6 < 2 [2-6] > 6 Peering-movement amplitude [cm]

Figure 49: Depth-discrimination performance versus peering amplitude in owls SL and VS. The upper histograms show distributions of peering to hole, and the lower histograms to object conﬁgured motion parallax stimuli. Peering movements with amplitudes in the range of 2 to 6 cm resulted in highly reliable performance for both owls, irrespective of the simulated depth conﬁguration.

Measurements of stereoscopic sensitivity (van der Willigen et al. 1998) showed that (under the conditions described here) the owl’s stereoacuity approximated 2 min of arc. Thus, if motion-parallax is as sensitive as stereopsis then performance should be distributed around 1 cm (i.e., peering amplitudes of 1 cm, with a gain of 1/10, generate stimulus transformations of ≈2 min of arc). On the other hand, optimal performance might lie around the owls’ interocular distance (4.5 cm), since the formal relationship between motion-parallax and the disparity cue becomes identical for static objects when the head is moved horizontally through the distance that separates the eyes. Therefore, the first band ranged from zero up to 2 cm (1±1 cm), and the second Chapter 6: Stereopsis and motion parallax 109 band was chosen to range from [2-6] (4±2 cm). The range of 4 cm for the second band was also justified by the observation that amplitudes greater than 6 cm not only involved movement of the head but also of the body. Moreover, humans are less sensitive to motion-parallax than to stereo information (Rogers and Graham 1982). We therefore speculated that only movements in the [2-6] cm band might be under stimulus control (i.e., stimulus induced). If the latter is the case, then the amplitude values of the [2-6] band should be distributed normally. In addition, the mean of these amplitudes should differ significantly from the means of the two other bands.

A B .99 12 .98 s SL N=48 SL

e .95

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t .75

8 e u p l

e .50 o 6 d s

n .25 b 4 I A .10 2 .05 .02 0 .01 1 2 3 4 5 6 7 2 3 4 5 6 Amplitude [stereoacuity multiple] Amplitude [stereoacuity multiple] Figure 50: Analysis of of peering behaviour in owls SL and VS. (A) Distribution of peering amplitude of the pooled correct responses (object plus hole) in the [2-6] cm band as shown in plot A. Given are the values of the estimated parameters and their respective 95% conﬁdence intervals of the ﬁtted normal cumulative distribution function (black lines). Note peering amplitude on the x-axis is given in multiples of the owls’ stereo threshold, whereas the estimated parameters, µ and σ, are given in cm. (B) Test of normality of the distribution data as shown in plot B. When the data points fall near the black line, then the assumption of normality is valid. N denotes the number of responses.

Analysis of the owls’ peering behaviour taken from the motion-parallax transfer data (MPD, Figure 46A), revealed that performance depended on the amplitude of 110 On the Perceptual Identity of Depth Vision in the Owl the head’s translational movement as is shown in Figure 49. While the owls responded randomly to the MPDs when peering amplitudes were less than 2 cm, the scores obtained for amplitudes ranging from 2 to 6 cm (SL: 91% , P <.0001 and VS: 94%, P <.0001; Figure 49) were comparable to those obtained with RDSs (SL: 95%, P <.0001 and VS: 91%, P <.0001; Figure 46A). For amplitudes greater than 6 cm, however, performance broke down (SL: 78%, P <.002 and VS: 63%, P <.5; Figure 49). The peering amplitude values of the correct responses within the middle band, [2- 6] cm, were normally distributed around 4.3 cm, and the standard deviation of these mean values was considerable less than 2 cm (Figure 50A and Figure 50B). In view of this finding it is important to point out that for an animal with almost fixed eyes, such as the owl (Steinbach and Money 1973; Knudsen 1989), horizontal image displacement is equivalent to retinal disparity (Collett and Harkness 1982). Therefore, these data may indicate that both owls are a factor 4 less sensitive to motion-parallax than to stereoscopic information. The latter can be appreciated from Figure 50B because stereoacuity was determined for each owl individually, which allowed the calculation of the peering amplitude parameter in multiples of the owls’ stereothreshold. The observation that movements in the <2 cm band are inadequate to allow reliable performance (Figure 49) is significant because 1 cm in peering amplitude generates a stimulus transformation that approximates the owls’ best stereoacuity value of 2 arcmin. This suggests that the owl visual system is more sensitive to depth from the the spatial disparity cue when compared with the spatio-temporal disparity cue. The later has also been observed in human subjects (Rogers and Graham, 1979/1982; Cornilleau-Peres and Droulez, 1993; Durgin et al., 1995; Bradshaw and Rogers, 1996; Turner et al., 1997). Furthermore, the diminished performance when the owls were displaying very large peering movements (>6, Figure 49) may be due to the fact that in these instances the owls were more involved in making motor responses rather than paying attention to visual stimulus.

6.3.4 No transfer during passive viewing Up to this point we have demonstrated that actively generated motion-parallax, like stereopsis, can yield similar levels of performance. To discover the importance of peering during the motion-parallax discriminations we created a third stimulus condition. In this so-called ”no-head-movement” condition, random-dot kinematograms (RDKs) were presented to the owls while they kept their heads in a fixed relationship with the stimulus presenting display (passive viewing). We used RDKs because in humans, regions of common motion in random-dot patterns lead to the vivid emergence of surfaces. Moreover, the compelling visual percept induced by RDSs or RDKs may be tightly linked to depth vision because it is thought that surface representation forms a Chapter 6: Stereopsis and motion parallax 111 critical stage between the earliest pickup of visual information and later stages, such as object recognition (Nakayama et al. 1989). Therefore, RDKs can be regarded as the motion domain counterparts of RDSs (e.g., Frost et al. 1994). In the RDKs used here, horizontal rightward transformations of the figure-dots were not coupled to the animals’ own motion. Instead, the figure region transformations were supplied exogenously (”open-loop” configuration). That is, an object RDK was constructed by use of ”dynamic-boundaries” (separating the moving figure-dots from the static ground-dots) that moved coherently with the figure-dots. In contrast, a hole RDK was constructed by ”static-boundaries” that formed a window that remained at the centre of the ground region. When confronted with these RDKs, the owls responded randomly suggesting that these open-loop stimuli were not perceived as either objects or holes (Figure 51). The latter was confirmed by closer inspection of the stimulus-response relationship showing that none of the owls treated the distinct RDK categories as perceptually different [Pearson chi-square test, Left eye: χ2(1) = 1.1, p<.005; Right Eye: χ2(1) = 0.9, p<.25 n.s.].

Owl SL: binocular Owl VS: binocular s s e 100 e 100 s s n n o 80 o 80 p p s s e 60 e 60 r r

t t c c

e 40 40 N=108 N=108 e N=108 N=108 r r r P <.0001 P < .011 r P <.0001 P < 0.14 o 20 o 20 c c

% 0 % 0 RDS RDK RDS RDK

Figure 51: Test of transfer from RDS to RDK: Eﬀect of the no-head movement condition. The histograms depict the mean percentage correct performance of 9 sessions with the training pair (shaded bars, SL: 94±6; VS: 89±3) and the test pair (open bars, SL: 54±6; VS: 52±6). Both owls failed to generalize to the RDKs [independent two-sided binomial probability: P (X = 52%) 0.5]. The error bars represent standard deviation, N denotes number of trials. Note that during the RDK trials, head movement was monitored and peering was not observed

The clear difference in performance for the identical patterns of relative motion depending on whether or not these patterns were actively generated suggests that retinal motion was only converted into a strong depth signal when evoked through head movements. There is, however, a complication factor. To reproduce objects or 112 On the Perceptual Identity of Depth Vision in the Owl holes that matched those generated by the MPDs under the closed-loop configuration and to cope with the real world constraint that surfaces standing out in depth occlude other surfaces, only dots in the figure region of the RDKs were moved horizontally as outlined above. Moreover, the moderate velocity of these dynamic dots approximated the averaged retinal velocity [.5 deg/s] as induced by the highly effective peering movements that fell within the [2-6] cm amplitude band Figure 50B. Under passive viewing conditions, however, this rather low retinal velocity may have resulted in a too weak relative motion cue to signal one surface lying in front of another. The validity of this interpretation was tested through additional training with the RDKs, which resulted in highly reliable performances. Note also that the response latency, after reliable performance was attained, was quite long (mean latency and standard deviation: SL= 700 83 ms; owl VS= 900 104 ms, N=70). This is an important finding because under transfer conditions the owls were required to view the RDKs for at least two seconds before they were allowed to respond. Hence, these results suggest that, in principle, the employed RDKs provided the owls with adequate information to discriminate objects from holes but did not signal obvious differences in depth. Finally the here presented data suggest that depth computed from motion parallax by the visual system of the owl is not merely the result of image motion. Rather, it seems to require the comparison of head motion against the perceived image motion. The later has also been observed in human observers and insects (Ono and Steinbach, 1990; Poteser et al., 1995).

6.4 General discussion

The experiments described were designed to compare the owls’ ability to interpret the depth order of two-dimensional surfaces when the depth information is specified by relative motion, on the one hand, and binocular disparities on the other. The results of the motion-parallax transfer test and control conditions provide strong evidence for the occurrence of primary-cue equivalence in the owl visual system. Rogers and Collett (1989) have argued that the human visual system strives for mutual consistent stereo and motion parallax signals in an attempt to provide a single physical interpretation of depth (i.e., an object’s dimension along the line of sight) that is maximally consistent with all the available information. For example, in humans stereo dominates motion when the two sources are placed in conflict (Todd, Tittle and Norman, 1995). The functional significance of this ability lies in the notion that only when both signals are brought together harmoniously, then ambiguities can be resolved that arise when stereopsis or motion parallax information is available on its own (Richards, 1985; Johnston, Cumming and Landy, 1992; Bradshaw, Parton Chapter 6: Stereopsis and motion parallax 113 and Eagle 1998; Brenner and Landy 1999) On the face of it, the present observations seem to extent this interpretation to the owl visual system. As was predicted, owls trained to categorise depth configurations specified by binocular disparity can maintain the discrimination when being presented with equivalent depth configurations specified by patterns of relative motion. Nevertheless, our results also show that monocular viewing of the motion parallax stimuli did not improve the owl’s performance significantly. In my view this tells us that the visual system of the owl does not specify depth equivalence at the expense of the discrepancy between the amount of depth predicted by both disparity and motion parallax signals at the same time. For the conclusion that I want to draw from the present experiment, the beneficial effects of generating mutual consistent percepts from different kinds of depth cue systems is irrelevant. What is important is that the basis for primary-cue-equivalence lies in the fact the nature of the information involved from stereo and motion parallax (”spatial” or ”spatial-temporal” disparities) can be related at a formal level (Koenderink, 1986). This conclusion is consistent with the two major observations made from the transfer experiments. First, despite great variability the mean peering amplitude in this range approximated 4.3 cm in both owls. Furthermore, it is known that in an animal with fixed eyes (Steinbach and Money, 1973) image displacement is equivalent to retinal disparity ( Collett and Harkness, 1982). Thus, it is as though the owls measured depth by moving through their interocular distance to mimic the information that would have been obtained through binocular viewing of the stimulus. Second, the failed transfer tests with the no-head movement condition seem to indicate that depth perception shifts into motion perception when ego-motion is eliminated. The issue of the applied strategy to determine depth from differences in relative motion has been addressed by several authors but there is only consensus about the assumption that awareness of ego-motion is critical (Poteser and Kral, 1995; Ono and Steinbach, 1990; Sobel, 1990). 114 On the Perceptual Identity of Depth Vision in the Owl 7 GENERAL DISCUSSION

7.1 Discrimination transfer as a tool to study vision

There are several levels at which one can explore the functions of vision in animals. Most broadly, one can look at the ecology of a speciﬁc animal species, and ask what visual challenges it poses. In this thesis I have investigated the owl visual system more speciﬁcally by using highly abstract images that were displayed on a CRT-screen. How- ever, the owls’ visual world does not consist of two-dimensional (computer generated) random-dot patterns and nor do owls in their natural environment respond to such impoverished stimuli. They respond to real objects in a three-dimensional world. Thus, “How biologically relevant is the discrimination of such abstract images?” Furthermore, the problems of real object discrimination are not solved when one has established what simple discriminations can be achieved. For example what we, humans, regard as simple discriminations can pose a complex problem to animals. Learning to discriminate becomes then a problem of learning to abstract the critical information. Alternatively, discrimination that humans regard as complex may be learned faster by animals than apparently simpler ones. Nevertheless, discrimination of abstract images is no doubt what makes the discrimination of real objects possible. For example, although natural objects are highly variable, birds often respond to them in similar ways, suggesting that objects fall into common classes or categories (Stettner, 1974; Cerrela, 1979; Delius, 1992). And ab- stractions of salient stimuli can elicit typical behavioural patterns as has been demonstrated by early experiments of comparative ethologists (Tinbergen, 1951). It follows that any experiment aimed to uncovering what birds can and cannot discriminate should take the above-mentioned remarks into account. The majority of studies focusing on visual discrimination in behaving owls (Fite, 1973; Martin, 1974a,b,c; Martin, 1977), however, have only measured visual thresholds—using classic psychophysical testing: constant stimulus and tracking procedures (Niemiec, 1995)—and thus tell us merely about the limits of visual sensitivity. Consequently, little is known about how owls classify and structure their visual world. 116 On the Perceptual Identity of Depth Vision in the Owl

There is, however, one exception. In an recent study by Nieder and Wagner (1999), the perception and neural coding of subjective contours was studied in the barn owl by making use of a rather different approach: transfer tests. The latter refers to tests of discrimination between novel stimuli on the basis of classifications learned in earlier discriminations with different cues (Hulse, 1995). The ability to transfer between discriminations based on distinct sets of stimulus classes is known as generalisation, which tests how a feature or combinations of features can be categorised (see e.g., Cerrella, 1990). Although the transfer procedure can be valuable and reliable means of assessing perceptual processing of biological relevant stimuli in animals, it is highly vulnerable to misinterpretation. All stages of training and testing, and the configuration of the training and test stimuli must be carefully planned in order to be able to interpret the results unambiguously. When, however, properly implemented along with control experiments, transfer tests provide a window into the perceptual world of animals such as the owl. The empirical basis of the analysis throughout this thesis has been discrimination transfer. In this respect it is important to note that when only a single method is applied, it is impossible to know whether the resulting psychophysical data is due to perception itself or to response processes inherent in the method (see e.g., Baird, 1970; Wagner, 1985). Accordingly, several tests of transfer were used—category estimation, perceptual matching (Chapter 3, 4 and 6). These measurements were com- plimented with classic psychophysical testing—method of constant stimulus, tracking procedures (Chapter 3, 4 and 5). These psychophysical techniques were applied to assess the following visual functions in the owl: (1) figure-ground perception based on texture, relative motion, occlusion or, binocular disparity cues (Chapters 3 and 4), (2) camouflage-breaking (Chapter 4) and (3) “relative” depth perception based on binocular stereopsis (Chapter 4) or (monocular) motion parallax (Chapter 6). The observed commonalities (discussed below) between figure-ground and depth perception from the above mentioned converging measures are therefore likely to reflect fundamental aspects of visual perception in the owl.

7.2 Figure-ground perception

Feature analysis and stimulus generalisation: The behavioural tests of visual search, texture, and motion perception as implemented in Chapter 3, demonstrated that owls are physically capable to segregate figure from ground in random-dot patterns presented on a CRT screen. More significant, by using discrimination transfer as an assay for perceptual matching (paradigm I: signal versus no-signal) and category estimation (i.e., generalisation; paradigm II: signal versus different-signal) I was able to show that visual perception in the owl was preserved even in impoverished Chapter 7: General Discussion 117 stimuli—cue fading, substitution or elimination—and that generalisation in relation to figure-ground perception was highly specific. Owls immediate transfered to novel stimuli after they had learned to report the presence, or alternatively, the absence of a rectangle (texture perception task: Fig- ure 21, page 48). Tests of transfer with the same birds, however, failed when the concept of detecting an image containing a signal (in this case a rectangle) was not made explicit by the behavioural task (visual search: Figure 19). Moreover, the fact that owls JL and RG regarded a random-dot image containing either a grey, or black rectangle as perceptually the same leaves open two possible explanations. First, because the standard image was never changed, the owls only needed to compare each novel image to their memory of the standard and then had to decide if they were looking at the standard or non-standard stimulus. Second, owls have some innate concept of surfaces (i.e., generic rules to group textured patterns into figure and ground) and were able to abstract this feature from the novel stimuli. I favour the latter explanation because of the data shown in Figure 22 on page 50. Texture perception was only reliable when the amount of black-dots in the grey rectangle region of the non-standard image was relatively low (<20%). Thus, fading of the critical cue (differences in texture) that could have induced figure-ground perception diminished the discriminative behaviour of the owls considerably. Impoverishing of the non-standard stimulus by diminishing the luminance content—but leaving the figure-ground segregation optimal—did not diminish the owls’ ability to detect the non-standard stimulus. Owls SL and VS, showed immediate transfer to novel RDKs in which the motion contrast was reversed (motion perception: Figure 27, page 55). Tests of transfer with the same birds failed, however, when the difference in motion contrast that existed between the learned object and hole RDKs was eliminated (motion perception: Fig- ure 25, page 53). These results seem to suggest that the difference in motion contrast was critical to the discriminative behaviour and hence rule out the possibility of pure figure-ground perception. Nevertheless, signal detection analysis of the psychometric data shown in Figure 28 (see page 56) clearly indicates that the birds were under stimulus control even when the difference in motion contrast was eliminated (see the data points marked with 1 of Figure 29, page 57). Together with the fact that the same animals could be trained to reliable discriminate the equi-motion RDKs (Figure 30, page 58), these data give room to a rather different interpretation. Owls SL and VS could indeed abstract the difference in the figure-ground configuration of the novel RDKs but the salience of the difference in motion contrast was a much stronger cue than the difference in patterns of occlusion and dis-occlusion. In other words, differences in velocity were much easier to detect than occlusion. That motion can be a regarded as a natural category for birds has been demonstrated in the pigeon (Ditrich and Lea, 1993). It is also known that pigeons are sensitive to differences in velocity (Hodos et al., 1975). 118 On the Perceptual Identity of Depth Vision in the Owl

Of course, object position could also have been used as a cue during the motion perception task. Nevertheless, Figure 21, page 48 clearly demonstrated that positional information was not the critical cue that guided the owl’s discriminative responses. In my view, it is more likely that difference in the position of the figure region helped the owls to learn the task initially. Once the owls had mastered the task, this visual feature became irrelevant. A factor that must be considered in the interpretation of the owls’ discriminative behaviour is the distance at which the stimuli were being presented (Stamp Dawkins and Woodington, 1996). A viewing distance of 70 cm (texture perception task) and 150 cm (motion perception task) is probably different from distances that barn owls normally would use to view the world that surrounds them. For example, the deficiency in transfer to the equi-motion perception task (Figure 29, page 57) could be attributed to an inadequate viewing distance. Patterns of occlusion and dis-occlusion may become only apparent to the owls from a large distance. The induced retinal velocity at distances of 2 to 5 meters may be more natural to barn owls and could make the difference between hole and object RDKs more salient (see e.g., Martin, 1990).

Psychophysics and signal detection analysis: The psychophysical data and signal detection analysis in Chapter 3 described have several implications for the interpretation of visual perception in the owl. First, the discrimination apparatus and training procedure employed appear to be suitable to attain a high degree of stimulus control. Second, in contrast to other studies of operant responding in owls (Tawny owl: Martin, 1974), the tracking method to determine stimulus thresholds should not prove to be difficult when the amount of catch trials (i.e., trails containing the standard) is kept relatively high. Third, when turning to the signal-detection analysis of the determined psychometric functions (texture perception task: Figure 23; motion perception task: Figure 29) it was evident that the owls systematically altered their response criterion as the difference in stimulus level between the standard and non-standard image diminished. The latter occurred irrespective of the employed visual cues or discrimination paradigms. Factors that also could have affected response criterion were the probability of the occurrence of a stimulus and the probability of reinforcement of correct responses (Green and Swets, 1966). However, the probability of any type of stimulus was .5 and reinforcement was kept at 70% irrespective of the outcome of the responses—false or true. Therefore, the observed changes in response bias must have been dependent upon the owl’s failure to discriminate accurately the presence of the standard stimulus. This implies that the thresholds determined with discrimination paradigm II will be somewhat underestimated because of the consistent bias to the standard stimulus. Finally, the finding that positional information appears to be dominant over figure- Chapter 7: General Discussion 119 ground segregation in the owl would suggest that tasks which specifically require figure- ground perception, will be learned more easily when first linked with a spatial cue. By gradually eliminating the spatial cue one can than obtain the desired figure-ground segregation discrimination. As will become clear in the section on depth perception, described below, future experiments were designed with the above described implications in mind.

7.3 Depth perception

Absolute and relative depth perception: An interesting aspect of stereopsis in owls is the possible lack of functional significant vergence movements. The eyes move at most 1o and it is not known whether any of these movements involve vergence (Steinbach and Money, 1973; Knudsen, 1989). The barn owl’s limited ability to make eye movements could enable this species to use binocular disparity to code absolute depth as will be explained below. An important consequence of absolute sensitivity to depth through binocular vision is that disparity alone can adequately specify the Euclidean metric structure of the environment—recovery of accurate physical depth without distortions—without being “scaled” by some other monocular visible cue to identify its current functional relationship with physical depth. This is in clear contrast with human stereoscopic depth perception, because in humans there is a nonlinear relationship between disparity and physical depth that varies with convergence angle (see e.g., Todd, et al., 1995; Tittle et al., 1996). Simple geometry shows that the position of a point in space can be recovered completely and without ambiguity from visual directions of the point from two vantage points, together with knowledge of the distance between the vantage points (i.e., interocular distance) (Foley, 1985). Exploiting the advantages of having two eyes— binocular vision—is the obvious solution to resolve the distance information. A single point has an absolute disparity or absolute binocular parallax which corresponds to the difference in the visual directions from the eyes (see Figure 2 on page 4). As a result, distance can be recovered if the absolute disparity and interocular distance is known. Relative disparities (or simply disparities), exist between two or more points at different distances and are based on the difference in the visual direction of the two eyes. Relative distance, or depth, can be calculated from disparity and the interocular distance. Note that, as disparity is only available to the visual system in terms of angular measure, disparity only provides depth information relative to some reference point. Furthermore, Parker and Cumming (1999) have pointed out that relative disparity may be exploited by stereopsis in humans and primates to support depth judgements because of the geometric fact that this angular measure does not change when the eyes are moved. 120 On the Perceptual Identity of Depth Vision in the Owl

A different but related solution is to consider the changes of visual direction of a relatively close stationary object that occur when the line of sight is changed by side-to-side movements of the head or body. This solution is known as triangulation or range finding (see section 1.3 on page 6) and refers to an absolute or egocentric depth localisation (Collett, Udin, and Finch, 1987). The absolute distance of the object can then be recovered from the change in visual direction of the object, plus knowledge of the distance and direction through which the eyes have moved. In this case even a single vantage point would suffice. A single point would create an absolute parallax for each of the eyes which corresponds to the change in visual direction with displacement of the eyes. In other words, absolute parallax is analogous to vergence information in binocular stereopsis. With two or more points at different distances, there is relative motion or motion parallax. Relative depth can then be derived from the magnitude and direction of motion parallax and the displacement of the eye(s). Thus, theoretically, binocular fixation could be used by the owl to estimate both absolute and relative depth, by a transformation of the fixed convergence signal of the eyes. And it is therefore possible that the owl can recover veridical depth through stereopsis based on either binocular disparity or motion parallax information. In view of the above discussed theoretical considerations on depth perception one would predict that owl stereopsis depends primarily on absolute disparity because (1) the position of the owl’s eyes do not change much, (2) absolute disparity can be more easily determined than relative disparity (i.e., requires less computation), and (3) absolute disparity provides the owl with veridical distance information rather than differences in depth. Nevertheless, the depth ordering test described in Chapter 4 (Fig- ure 35A on page 71) clearly demonstrated the owl’s ability to determine differences in depth on the basis of relative disparity information alone. In terms of the explanation given above—about how the owl might be able to recover depth—one would expect the owl to move its head during the depth ordering task in order to produce motion parallax information. Figure 37 (on page 73) clearly shows that this is not the case. Furthermore, when the stereoscopic target was misaligned relative to the owls’ midline during this transfer test, the owls did not need to assume a fixed relationship between stereoscopic depth and position in the visual field. Collett and Harkness (1982), have suggested that this strategy would enable the owl to compensate for the lack of eye vergence movements as is discussed in section 4.3.2 on page 74. Thus, the results of the depth ordering test constitute the first behavioural evidence that owls can perceive relative depth from RDSs in a manner similar to that found in primates and do not rule out the possibility of convergent eye movements. Nevertheless, the experiments of Chapter 4 still leave open the possibility that the owl can use disparity to determine absolute depth by transformation of the convergence signal of the fixed eyes. Chapter 7: General Discussion 121

Camouflage breaking and internal representations: Sensitivity to binocular disparity not only enables the perception of relative depth, it also allows to differentiate features from their obscuring backgrounds (Julesz, 1971). In addition, Pettigrew (1990) noted that stereopsis in the owl serves a special function in breaking camouflage since neither prey nor predator have to move in order for the prey to be detected. The latter argument is corroborated by a recent investigation by Mckee and others (Mckee et al., 1997) which concluded that human stereopsis is only generally useful in breaking camouflage when both the observer and the scene are stationary. The experiments in Chapter 4 provide direct evidence supporting the notion that owl stereopsis is extremely useful in breaking camouflage of static targets. The data also suggest that the owl visual system is capable to build internal representations of the surrounding visual world. In what follows both findings will be discussed starting with the former. The falcon study of Fox et al. (1977) was instrumental in showing that the avian visual system can indeed exploit the retinal disparity cue of RDSs to break camouflage. The tests of transfer from monocular to pure binocular configured random-dot patterns has confirmed this finding (see Figure 35A on page 71). More significant, the immediate transfer from non-stereoscopic to stereoscopic “figure-ground” perception (Figure 33 on page 69) has never, to the best of my knowledge, been demonstrated in animals before (McFadden, 1994; Bough, 1970; Harwerth and Boltz, 1979; Ptito, 1992; Fox et al., 1978) and reveals that “camouflage breaking” of static targets is an important function of avian stereopsis (van der Willigen, Frost and Wagner, 1998). In my view, the concept of an internal representation implies that exposure to a stimulus produces a neural trace that preserves essential characteristics of the stimulus so that these remain accessible for some variable period and can affect discriminative behaviour even in absence of the original stimulus (see also Cerella, 1982). For example, the successful transfer with owl JL (Figure 33 on page 69) showed the owl’s capacity to deal with different discriminations in a manner suggesting that it can encode and store information about stimuli in the form of internal representations. In this case, the owl must have had some internal representation of shape since the only constant feature that existed in both the monocular (texture) and binocular (disparity) stimuli was the border of the rectangle. In other words, this owl was able to segregate figure from ground based on a learned texture cue and could extrapolate this ability to novel stimuli using retinal disparity as the critical cue to discriminate. Similarly, the successful transfer in owls SL and VS (Figure 34 on page 70) has provided evidence for the capacity to encode and store the depth information of moving stimuli because they were able to use this type of abstract visual information to deal with binocular stimuli that lacked the motion cue. These findings are consistent with the the demonstration that owls can transfer from a subjective contour discrimination based on gratings with gaps to gratings with phase-shifted abutting gaps (Nieder and Wagner, 1999). 122 On the Perceptual Identity of Depth Vision in the Owl

The functional significance of stereopsis: In view of the literature on visual perception in the owl, although based on only a few owl species (see for review Martin, 1990), it is hard to avoid the conclusion that adaptations of the owl visual system to nocturnal life are insufficient within them to account for nocturnal mobility and hunting. It has therefore been argued that hearing plays a critical role in the nocturnal behaviour of owls (Payne, 1962). Nevertheless, sound localisation alone can not explain how owls avoid branches of trees at dim light, why hunting success is maximal only during clear moonlight nights and the fact that owls are extremely reluctant to fly in environments which they have not inspected with their eyes (see e.g., Dice, 1945; Clarke 1983; Erichsen, 1985). The dominance of vision in the barn owl is also man- ifested behaviourally by the gradual shift in sound localisation behaviour that occurs during development in response to a sustained discordance between visual and auditory localisation (Knudsen and Knudsen, 1990). From the data presented in Chapters 4 and 5, however, there emerges a different view on the functionality of vision in the owl. The data suggests that binocularity in the owl plays an important role in the detection of camouflaged immobile targets—such as prey or tree branches—at low levels of illumination in addition to its well known role in relative depth perception. I came to this conclusion because of the following considerations. For a nocturnal hunter, such as the owl, an increase in signal/noise ratio above and beyond that required for simple monocular detection—probability summation—is of prime importance because quantal fluctuations at low light levels reduce the detectability of distant objects, as argued by Pettigrew (1990). It is also known that in humans disparity per se cannot specify metrically accurate information about depth without being “scaled” to some other source of information such as relative motion (Todd et al., 1995) (see section 7.3). This is an important issue because in day light conditions there is access to multiple sources of depth information (e.g., shading, motion, texture, disparity) and in humans these cues are not necessarily redundant. The functional significance of stereopsis in the owl can thus be seen as the utility by which detection of static and monocular camouflaged targets can be improved at low light levels, when monocular cues become inaccessible. In other words, in dim light it would be of advantage to the owl if it could enhance the visibility of targets when the use of monocular cues cannot improve detection. In my opinion this is the only scenario whereby information solely derived from the binocular disparity cue is superior to information derived from a combination of monocular cues. The experiments of 2 Chapter 5 showed that at luminance levels lower than -2.3 log10 cd/m , the owl’s sensitivity to binocular disparity started to deteriorate significantly (see Figure 42 on page 89) whereas human stereoacuity already rises a factor 2 to 4 when luminance 2 is reduced to -1.5 log10 cd/m (Mueller and Lloyed, 1948). This finding does indeed suggest that binocular vision in the owl has a lower susceptibility to photonic noise Chapter 7: General Discussion 123 when compared to stereopsis in humans (see also Livingstone and Hubel, 1994). This result may seem unsurprising when one considers that the primary optical features of the barn owl’s eyes are image size and photoreceptor convergence which enhance visibility at low light levels (Scheaffel and Wagner, 1996). The important theoretical issue, however, is whether stereopsis requires stimulus energy above and beyond that required for simple monocular detection. My data does not address this issue directly and thus requires further study. Nevertheless, the suggestion of lower susceptibility to photonic noise of owl stereopsis when compared to human data is in contradiction with the finding that the absolute visual sensitivity of the tawny owl (Strix aluco) is only slightly higher than that of humans (Martin, 1977). It may very well be that this aspect of the owl visual system only becomes apparent when the behavioural task can only be solved through binocular vision (i.e., stereopsis). To summerise, when thinking about the functional significance of stereopsis, it seems undeniable that the stereoscopic systems of owls and primates incorporate an highly effective “camouflage breaking” algorithm. This algorithm is known as stereopsis and allows these very different animal species to use binocular disparity as the sole source of information to enhance visibility of targets in their natural viewing situ- ations. The opposite situation is true for the explanation that stereopsis has evolved to improve precise depth judgements, because the latter is only true when the disparity cue can be combined with monocular depth cues. Thus, improved precision per se cannot account for the functional significance of owl stereopsis, since in dim light the detection of monocular cues becomes problematic. In other words, in view of the data presented in this thesis it seems highly plausible that binocular vision in the form of stereopsis has evolved in the owl solely for the reason that this adaptation has provided this nocturnal hunter with the necessary—or rather only—means to improve signal detection at dim light conditions. The word “only” in the later sentence is more appropriate I think because it is not possible to design an eye that would be capable of achieving the same spatial resolution at night-time as during day-time levels (see e.g., Green, Powers and Banks, 1980).

Disparity and motion parallax compared: Both stereopsis and motion parallax rely on multiple views of the visual sense to recover its three-dimensional structure. Binocular disparity exists between two objects at distinct distances and originates from viewing these objects from two spatially separated vantage points (the left and right eye) at the same time (Howard and Rogers, 1995). Motion parallax, however, can be determined with one eye only and exists when the same objects are viewed while moving the head from side-to-side at a right angle to the line of sight (Wallach and O’Connel, 1953; Richards, 1985). These translational head movements are known as peering and make closer objects appear to move faster and further than more distant objects (Wallace, 1959, Collett, 1987). 124 On the Perceptual Identity of Depth Vision in the Owl

The discrimination-transfer experiments of Chapter 6 were designed to compare the owls’ ability to interpret the depth order of two-dimensional planar random-dot surfaces when the depth information is specified by relative disparities on the one hand and relative motion on the other. I interpret the generalization of depth from stereo to motion-parallax and the results of the control conditions as strong evidence for the occurrence of primary-depth-cue equivalence in the owl visual system. That is, actively generated motion-parallax, like stereopsis, can yield similar levels of performance in tasks involving the discrimination of differences in depth. In my view the basis for the here observed primary-depth-cue equivalence lies in the consideration that the nature of information involved between stereo and motion- parallax can be related at a formal level (”spatial” versus ”spatial-temporal” disparities). This conclusion is consistent with two major observations made from the transfer experiments. First, side-to-side movements of the head in a horizontal plane yielded the most effective depth judgements. Moreover, I did not find any evidence of distance dependent rotation as observed by (Wagner 1989) in peering barn owls. This phenomenon of translatory peering motion combined with rotational fixation motion is a specific way of acquiring parallax information. That is, rotations of the head about the vertical axis can, at least for small-field stimuli, compensate for retinal target displacement induced by the side-to-side head movements (Koenderink 1986). On the other hand, pure lateral translations, without rotation of the head (or eyes), would enable the owl to determine the absolute depth (i.e., the distance relative to the observer) of static objects from de relationship of the magnitude (or velocity) of the head movement to the magnitude (or velocity) of the induced retinal image shift. Such use of head movements to provide motion-parallax for distance estimation of static objects has been demonstrated in several animal species (see for review by Collett, 1996; Kral 1998). Second, the mean peering amplitude in the highly effective [2-4] cm band approximated 4.3 cm (Figure 50A) in both owls. The latter distance approximates the owl’s interocular distance. Thus, it appears as though the owls measured differences in depth from the motion-parallax displays by moving their heads through the interocular distance to mimic the geometry that otherwise would have been obtained through binocular viewing (i.e., stereopsis) of a real object. Taken together, the here discussed features of peering in the owl strongly suggest that the behaviour pattern is carefully designed for extracting motion-parallax information. Moreover, the owls’ ability to maintain reliable performance in monocular viewing conditions (Figure 48) supports this conclusion. Although the issue of the applied strategy to determine depth from differences in relative motion has been addressed in a wide range of animals and in humans by several authors (e.g., Rogers and Graham 1979; Koenderink 1986; Sobel 1990; Dijkstra et al. 1995; Poteser and Kral 1995; Land 1999; Wexler et al. 2001), many of the important psychophysical and neural elements are still not known. Nevertheless, humans Chapter 7: General Discussion 125 can detect differences in depth from both actively generated and passively observed motion-parallax (Ono and Steinbach 1990; Howard and Rogers 1995). In passive viewing, motion must be computed simultaneously with depth. In active vision, on the other hand, extra-retinal information about motion is available, and could in principle be used to help compute depth (as explained above). Therefore, the failed transfer to the no-head-movement condition (Figure 51) may indicate that depth perception based on relative motion shifts into motion perception when extra-retinal information is eliminated. Nonetheless, the failure of the owls to generalize the RDKs (Figure 51) was un- expected because of the following findings. First, in previous experiments (van der Willigen et al. 1998) I have been able to show that an owl trained to perceptually segregate figure from ground based on monocular cues (i.e., determination of the presence or absence of a rectangle defined by differences in texture) immediately transferred this discriminative behaviour to RDSs. Second, in the same study another owl was trained to detect the presence of a stereoscopic planar surface moving in front of, or alternatively, behind a non-disparate static background. This type of stereoscopic display is called motion-in-depth (Cumming and Parker 1994) because in addition to binocular disparity it contains a monocular discernable cue (i.e., structure from motion). I found that this animal could perceive similar depth impressions from static RDS displays without the need of additional training. In our view, these previous examples of generalization suggest that the barn owl is able to apply generic rules about shape or depth for grouping stimuli into appropriate classes. By contrast, in case of motion-parallax there may be aspects of perceptual knowledge (depth perception) involved with motor interactions (peering) and this relationship becomes apparent only when a certain visuo-motor task is performed. In other words, motion-parallax (or relative motion) might not present by itself a salient cue to readily distinguish differences in depth. The appeal of this hypothesis is that it is consistent with the failed transfer test (Figure 48) in which the owls were required to passively observe the motion-parallax displays. A complicating factor, however, that arises in this respect is whether the failure to generalize the RDKs might be due to the fact that stereopsis and motion-parallax specified incompatible depth relations because testing necessarily occurred under binocular viewing (see Behavioural training and test procedures of of Chapter 2). This interpretation is supported by the recent finding in human subjects that when ”static perspective” and ”dynamic motion” depth cues are in conflict, the comparison of the magnitude (or velocity) of the head movement against the perceived magnitude (or velocity) of the retinal image shift becomes critical in judgements of 3D structure (an object’s dimensions along the line of sight) of stationary objects (Wexler et al. 2001). 126 On the Perceptual Identity of Depth Vision in the Owl

The functional importance of primary-depth-cue equivalence: Taking the discussion above into account, the functional importance of primary-depth-cue equivalence in the owl can be understood as follows. While the presence of stereopsis in the owl has been demonstrated, both electro- physiologically and behaviourally (Pettigrew 1979; Wagner and Frost 1993; van der Willigen et al. 1998; Nieder and Wagner 2000), the functional importance of binocular vision in this nocturnal prey capturing bird is not fully understood (Pettigrew 1990; van der Willigen et al. 1998; Martin and Katzir 1999). As pointed out by Julesz (1971), it is possible for a stationary predator with stereoscopic ability to ”break” camouflage since a static target which is invisible to monocular inspection may be visible stereoscopically if it has a slightly different depth plane from the background. On the other hand, stereopsis is such an accurate and direct means of judging depth; it is very intuitive to see why it might be advantageous to an avian predator hurtling towards the ground at high speed. Nevertheless, several authors have claimed that too much time is required to reach a sufficient level of accuracy in estimating depth through stereopsis to guide rapid gross bodily movements, especially during critical rapid flight manoeuvres such as pray capture or landing (see for review by Davies and Green 1994). Under these circumstances motion-parallax may seem to be much more readily available. Thus, it might very well be that in terms of perceived depth during flight manoeuvres, the owl relies on motion-parallax information rather than stereopsis. By contrast, for a nocturnal hunter, such as the barn owl, an increase in the signal/noise ratio above and beyond that required for simple monocular detection ”probability summation” through binocular vision is of prime importance because quantal fluctuations at low light levels reduce the detectability of distant objects, as argued by Pettigrew (1990). In other words, in dim light it would be of advantage to the owl if it could enhance the visibility of targets when the use of monocular cues cannot improve detection. This conclusion provides an interesting scenario whereby information solely derived from the binocular disparity cue is superior to information derived from a combination of monocular cues. Hence, remains the question ”What is the functional importance of primary-depth-cue equivalence in the owl?” A functional explanation for the occurrence of primary-depth-cue equivalence in the owl might be that motion-parallax information is used to calibrate stereoscopic information during development. The rationale behind this explanation stems from the following considerations. First, it is known that human subjects can calibrate motion-parallax according to absolute distance information (Ono et al. 1986). Sec- ond, viewing distance can be determined when stereo and motion-parallax information is combined (i.e., the unique distance at which disparity and motion specify the same amount of relative depth); as pointed out by Brenner and Landy (1999). Although the latter does not appear to occur in humans, and our data does not address this issue directly, the observation that young owls spend a considerable amount of time Chapter 7: General Discussion 127 engaging in peering movements (Martin, 1990) makes it likely that this information is used by the owl visual system during development.

Primary-depth-cue equivalence implies the possibility of common neural mechanisms: The here presented evidence of primary-depth-cue equivalence in the owl strongly suggest that both the mammalian and, avian visual system have adopted a similar strategy to cope with the often co-varying information about the layout of physical space; this irrespective of the fact that binocular vision has evolved independently in mammals and birds (Karten et al. 1973; Pettigrew 1979; Medina and Reiner 2000; Nieder and Wagner 2000). Acceptance of this conclusion strengthens support for the idea that neural systems that have evolved to detect motion or disparity do not operate independently as has been suggested by numerous authors that have studied human subjects by means of psychophysical testing (e.g., Nawrot and Blake 1991; Bradshaw and Rogers 1996; Thompson and Nawrot 1999; Kham and Blake 2000). Nevertheless, in spite of the increasing electrophysiological evidence to suggest that motion and depth are processed together in the visual system of primates and cats, the neural basis of this phenomenon is largely unknown (Nawrot and Blake 1991; Bradley et al. 1995; DeAngelis et al. 1998; Anzai et al. 2001). In this respect, the highly developed visual forebrain of the barn owl —the visual Wulst shares many functions with the mammalian visual cortex (Karten et al. 1973; Pettigrew 1979; Medina and Reiner 2000; Nieder and Wagner 2000)— provides a promising substrate in which to explore the underlying mechanisms of primary-depth-cue equivalence in awake behaving owls. This close integration of behavioural and physiological approaches has recently proven to be a powerful research strategy to investigate the presence of neural correlates of visual abilities in the owl (Nieder and Wagner 1999).

Stereopsis as a unitary phenomenon: Physiological and anatomical studies of neural structures invite speculations regarding their developmental organisation and evolutionary history. But proof of the functional significance of neuronal solutions can only come from behavioural demonstrations of perceptual capabilities (van der Willi- gen, Frost and Wagner 1998). Nonetheless, specific neuronal solutions to problems of sensory information processing may reflect their evolutionary history (Pettigrew, 1986; Pettigrew, 1989; Heiligenberg, 1991; Martin and Katzir, 1999). Furthermore, highly evolved organisms, such as the owl (Medina and Reiner, 2000), generally derive their superior perceptual and behavioural qualities not so much from novel neural mechanisms as from highly specialised neuronal structures of basic designs that they share with simpler organisms. Such structures incorporate and optimise particular algorithms that may be less conspicuous in organisms lacking these superior capabilities. Thus the behavioural exploration of depth perception in the barn owl should reveal the diversity and limitations of stereoscopic depth perception. It is exactly this argument that Pet- 128 On the Perceptual Identity of Depth Vision in the Owl tigrew (1989) used to suggest that there may be a single, most efficient algorithm for achieving stereopsis and that this is the one, which is discovered independently by the mammalian, and the avian visual system. It has been argued (McFadden, 1994; Martin and Katzir, 1999) that stereopsis is not a unitary phenomenon and may occur in varies forms. However, behavioural evidence of binocular depth perception based upon relative binocular disparity has only been demonstrated in animals that possess global stereopsis (monkey: Bough, 1970; Falcon: Fox et al., 1977; cat: Ptito, 1992; horse: Timney and Keil, 1999). The surprising fact that stereopsis in all these species can occur without prior monocular pattern recognition suggest that image processing until after information from both eyes is brought together is an essential feature of any neural algorithm that underlies stereopsis (Pettigrew, 1989). Therefore, I suggest that it is not so much a question of different forms of stereopsis as claimed by McFadden (1994) but rather different visual systems that take advantage of the same neural solution—global stereopsis (see page 6 of Chapter 1). The finding that the barn owl is susceptible to relative disparity and motion parallax in much the same way as humans strengthens the notion of stereopsis as a unitary phenomenon.

7.4 Final word

This is the end of my endeavour to understand the function of binocular stereoscopic vision in the barn owl. Taken together with the electrophysiological data on the mechanisms that underlie depth perception in this species Tyto alba (Ph.D. thesis by Andreas Nieder, 1999) our lab—under supervision of Professor Hermann Wagner—begins to make an serious effort to understand how disparity is coupled to depth perception and other types of visual information such as motion, figure-ground perception and the perception of forms (van der Willigen, Frost and Wagner, 1998; Nieder and Wagner, 1999, 2000). We (i.e., the people at Wagner’s lab) are only now beginning to appreciate the extent to which depth perception in the owl relies on binocular disparities and on complex patterns and spatial derivatives of disparity. We are also beginning to appreciate the sheer complexity of the neural organisation of the owl’s visual Wulst and its perceptual capabilities. Our lab has also increased the repertoire of psychophysical and physiological techniques to make a credible attempt to better understand the neural machinery involved in disparity processing. This close integration of behavioural and physiological approaches is a powerful research strategy. Whereas behavioural studies guide the search for neural implementations (i.e., functional significance), the growing knowledge of the owl’s sensory and central-nervous physiology will constrain computational models pro- posed to explain behavioural phenomena. For example, the use of interactive stimuli Chapter 7: General Discussion 129 in combination with telemetric recordings in awake behaving owls provides us with the possibility to investigate the neural mechanisms that bring together different types of information that are required to compute a coherent impression of three dimensional space. 130 On the Perceptual Identity of Depth Vision in the Owl ABBREVIATIONS & SYMBOLS

SUBJECTS BEHAVIOURAL APPARATUS

JL ...... owl Julia ANSI . . . . . American national standard for information RG ...... owl Regina C ...... C-code programming language SL ...... owl Silvester CRT ...... cathode ray tube VS ...... owl Vespucci DC ...... direct current

NIH ...... national institutes of health STIMULI LC ...... liquid crystal

MPD ...... motion parallax display LCM ...... liquid crystal modulator

RDK ...... random-dot kinematogram OPF ...... oppositely polarised ﬁlters

RDS ...... random-dot stereogram RGB ...... red, green and blue

ML ...... RDS viewed with left eye only SGI ...... silicon graphics industries

MR ...... RDS viewed with right eye only TM ...... trade mark S ...... RDS viewed binocularly TTL ...... transitor-transitor logic SL . . . .stimulus linked with left response bar

SR . . stimulus linked with right response bar

Sz ...... observation stimulus α...... depth-ordering training RDS pair

β ...... depth-ordering test RDS pair

γ ...... depth-ordering test RDS pair 132 On the Perceptual Identity of Depth Vision in the Owl

SYMBOLS AND UNITS

arcmin ...... minutes of arc T ...... time interval baud . . . . . unit of signalling speed [bits per second] X ...... azimuth

c ...... cycle Y ...... elevation Z ...... distance dmax ...... maximal nondepth disparity

cm ...... centimetres µ ...... mean

cd ...... candela σ ...... standard deviation 2 deg ...... degree of visual angle χ ...... chi-square test

df ...... degree of freedom 3-D ...... three-dimensional

f ...... anterior focal length

anteriorfocallength f/number ...... entrancepupildiameter

g ...... psychometric function slope

Hz . . . unit of frequency in cycles per second

Icolour ...... luminance coloured dots

Inon−colour ...... luminance grey dots

Imax ...... maximal luminance level

Imin ...... minimal luminance level

log10 ...... logarithm

m ...... meters

msec ...... milli-seconds

N ...... number

r ...... binocular retinal disparity

P(X≥r) ...... gives probability of observing a hit rate,X, equal or greater than the observed hit rate, r

p . two-side independent binomial probability

sec ...... seconds

t ...... two-sample test Abbreviations & Symbols 133 134 On the Perceptual Identity of Depth Vision in the Owl REFERENCES

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I am greatly indebted to a number of people who, through their support, comments and criticism, have kept me enthused, put up with moanings, and helped me transform the initial ideas into reality. I appreciate their assistance and effort, especially my friends at Professor Hermann Wagner’s Institut für Zoologie of the RWTH Aachen. Foremost, I would like to thank Hermann— my Ph.D. advisor—for his support and confidence throughout. He has given me the opportunity to work with a fascinating animal—the barn owl— and an intriguing research theme—stereopsis. He tolerated my preoccupations, my badly spoken German, shared disappointments and read many, if not all, of my drafts. During all of this, I have learned to appreciate his harsh criticism. Through his scholarship and by his insistence on what I should omit he has helped me give focus to the thesis. Personal thanks must also extend to Barrie Frost—Professor of Psychology at the Queen’s University, Kingston, Canada—for his, encouragement, support and explanations. Barrie gave me the knowledge, means and the Idea to unravel the role of motion parallax in the owl visual system. Most of the parallax research we did together and I have to say it was great fun! In depth knowledge about the computational approach to vision, I gained through vigorous discussions with friend and brilliant colleague Joerg Lippert. He often not shared my interpretations and saved me from errors of logic. With my dear friend Dirk Kautz, I always found a willing ear, his love for culture and knowledge about the German way of life made my stay in Munich much more pleasant. Fellow scholar Andreas Nieder operated on “my” owls, supplied me with crucial parts for the apparatus and was always willing to listen to my misgivings about animal training. David Fleet, Tom Collett, Jamie Mazer, Mark Bradshaw, Harald Luksch and Joerg May, I thank for reading and improving earlier parts of the manuscript. Their comments were much appreciated. My father, who has been my principal guide, I sadly miss. To dedicate this thesis to him is a conspicuous understatement, but for me this is my greatest gift and acknowledgement of gratitude towards my parents.

Sweet Mireille, It is thy love alone that gives worth to all things I do 152 On the Perceptual Identity of Depth Vision in the Owl CURRICULUM VITAE

About the Author

Biologist, Robert Frans van der Willigen, research fellow in visual depth perception—School of Human Sciences, University of Surrey, United Kingdom—was Born in Goes, Zeeland the Netherlands, on the 9th of March 1967 and raised in Vlissingen. Robert graduated from Athenaeum “de Rijkss- cholengemeenschap Scheldemond” in 1987 and studied biology in the most ancient city of the Netherlands—Nijmegen—at the University of Nijmegen (KUN). At the KUN he first majored in Animal Physiology & Biochemistry, 1992, and subsequently in Biophysics (KUN, RUU), 1994. As an undergrad- uate in biophysics Robert realised two master projects. The first project was conducted at the department of Medical Physics and Biophysics, KUN. This study—titled: Audio-Visually Evoked Saccadic Eye movements— focused upon the question how multiple sensory modalities interact and influence eye movement generation. During this period, Robert also analysed a neural network that modelled the primate oculomotor response towards auditory targets in the horizontal plane. During his second masters project, at the department of Comparative Animal Physiology, University of Utrecht (RUU, Neuroethology group), Robert designed a voltage clamp for recordings of electroreceptor activity with in vitro skin preparations of cat fish. In January 1995 he received his “bul” and published his first paper (Frens, van Opstal and van der Willigen, 1995). In November of 1994, he was given the opportunity by Professor Hermann Wagner—who was at that time “Privat Dozent” at the Technical University of Munich (TUM)— to study stereopsis in the barn owl as part of a Ph.D. project. About one year later, 1995, Hermann Wagner was offered a chair in Zoology and animal-physiology at the university of Aachen (Institut für Biologie II, RWTH Aachen). Here upon, it was decided to move to Aachen 154 On the Perceptual Identity of Depth Vision in the Owl

in November of the same year and it was at the RWTH Aachen that most of the owl stereopsis data was obtained. In 1997, the author worked together with David Fleet, Associate Profes- sor of Computing and Information Science at Queen’s University, Kingston, Canada (van der Willigen, et al., 1997). In this year, Robert also visited the Queen’s Psychology department of Professor Barrie Frost. During this stay, plans were made to study motion parallax in the owl. In the year hereafter, 1998, the parallax study was realised in collaboration with professor Frost at the RWTH Aachen (van der Willigen, Frost and Wagner, 1998). As from the 1st of September 1998, the author was appointed to the position of research fellow and joined the lab of Dr. Mark Bradshaw who is Senior Reader within the department of Psychology at the University of Sur- rey (UniS), Guildford, United Kingdom. Roberts’ current research focuses on the roleˆ of the primary visual cues— disparity and motion—, in the initiation and control of reaching and grasping behaviour in humans (Hibbard, Brad- shaw and Van der Willigen, 2000; Van der Willigen, Bradshaw and Hibbard, 2000; Bradshaw et. al., 2000). The 22th of September 2000, Michelle was born and Robert rejoined his family in Maastricht. In October of that same year the author joined the Cen- tre for User System Interaction (IPO) at the university of Eindhoven (TUE). His current research involves the development of formal methods based on knowledge of natural human communication processes to support the design of multimedia user interfaces and to improve the interactive characteristics. Besides his scientiﬁc endeavours, Robert became involved in computer programming and UNIX system administration while working at the KUN in 1992, and has since been developing graphical user interface software on computer platforms such as, UNIX (DEC, SUN, SGI), Mac OS and windows NT. Currently, Robert is involved in the development of OpenGL based graphical interfaces that allow real-time motion tracking and the on-line control of three-dimensional stereoscopic displaying. Curriculum Vitae 155 156 On the Perceptual Identity of Depth Vision in the Owl