# Binocular disparity can explain the orientation of ocular dominance stripes in primate V1

## I INTRODUCTION

The perception of depth in primates relies on recombining information coming from both eyes. This is accomplished by a retinotopic mapping , of the two retinal images onto the primary visual area V1. In many primates, neurons dominated by each eye are segregated into the system of alternating stripes known as the ocular dominance pattern ,. A complete reconstruction of the pattern in a macaque V1 is shown in Fig.1.

Although this pattern may seem random, the orientation of the ocular dominance stripes on the cortical surface follows systematic trends found in other macaques  and in Cebus monkeys . These trends are easiest to see when the ocular dominance pattern is transformed back into visual field coordinates by dividing all cortical distances by the local magnification factor. (The magnification factor  gives the distance in millimeters on the cortex which corresponds to a $`1\mathrm{deg}`$ separation on the retina.) The transformed pattern shown in Fig.2 (as obtained by LeVay et al. (1985) following Hubel and Freeman (1977)) reveals two major trends: in the parafoveal region stripes tend to run horizontally, while farther from the fovea stripes follow roughly concentric circles. These trends in the orientation of the stripes call for explanation.

Many theorists have successfully modeled the development of ocular dominance columns ,,, and some have addressed the trends in stripe orientation. It was suggested originally by LeVay et al. (1985) and later investigated by others ,, that the mapping from the two almost circular LGN layers to the more elongated representation in V1 requires least stretching (or anisotropy of the magnification factor within ocular dominance stripes) if the stripes run perpendicular to the long axis of V1. However, this theory does not explain the different orientation of ocular dominance stripes in the parafoveal region. Moreover, it is unlikely that the shape of V1 dictates its internal organization; more probably, its internal organization will dictate its shape. Goodhill et al. (1997) have instead proposed that the global pattern of ocular dominance stripes arises from anisotropic and spatially non-uniform correlations in the neural input from the retinae. This seems like a plausible developmental mechanism, although anisotropic correlations have yet to be demonstrated experimentally.

Rather than modeling development, I have taken a different approach to explain the orientation of ocular dominance stripes. I propose that the stripe orientations follow from V1’s role in depth perception according to the principle of wiring economy. In other words, I focus on understanding why the stripes are arranged as they are, rather than how they become so arranged.

The wiring economy principle amounts to the following ,,,, ,: because of limitations on head size, there is pressure to keep the volume of the cortex to a minimum. This implies that wiring, i.e. axons and dendrites, should be as short as possible, while maintaining function. In general, the function of a given cortical circuit specifies the connections between neurons. Therefore the problem presented by the wiring economy argument is to find, for a given set of connections, the spatial layout of the neurons that minimizes wiring length. This problem can be extremely difficult because of the large number of neurons and even larger number of interconnections within a cortical region. However, the columnar organization of the cortex  allows me to consider the layout of cortical columns (each consisting of $`10^4`$ neurons) rather than individual neurons, reducing the problem to two dimensions.

The wiring economy principle has been used to explain retinotopic map , and ocular dominance stripes , in V1. In the first case, the construction of receptive fields requires connections between neurons representing neighboring points in the visual field. Topographic mapping of the visual field minimizes the length of these connections. In the second case, each cortical neuron connects more often to cortical neurons dominated by the same eye than to neurons dominated by the opposing eye. Thus the segregation of neurons into alternating monocular stripes minimizes the total length of intra-cortical connections.

Here I use the principle of wiring economy to find the optimal orientation of the ocular dominance stripes (given they exist) from the function of V1 in processing binocular disparity. Disparity arises when an object closer or farther than the point of fixation forms images on the two retinas that are in different positions relative to the fovea. Because the cortex is retinotopically mapped, the left and the right eye representations of this object in the cortex will fall some distance away from each other, as determined by the magnitude and direction of the retinal separation. Recombining these representations requires extensive wiring between cortical columns.

In the next Section, I show that the left and right eye representations in V1 will be farther apart if the ocular dominance stripes run perpendicular, rather than parallel, to the direction of retinal separation. Therefore I argue that in order to minimize wirelength, the orientation of the stripes should correspond to the direction of binocular disparity. However, for any given point on the cortex the disparity in the corresponding point of the visual field depends on the viewing conditions, that is, direction of gaze and distance to the object. In Section III, I calculate a distribution of disparities averaged over viewing conditions. I obtain a map of typical disparities in the visual field which then determines the optimal orientation of the ocular dominance stripes.

The orientation of stripes predicted by this theory agrees with actual patterns obtained from macaque and Cebus monkeys, see Section IV. My results show that the two major trends of stripe orientation result from two main contributions to disparity. In the parafoveal region, binocular disparity is due mainly to the horizontal displacement of the eyes, consistent with the horizontal stripes in the (transformed) ocular dominance pattern. Farther from the fovea, the pattern consists of isoeccentric lines. These are explained by binocular disparity due to unequal rotation of the eyeballs around the gaze line (cyclotorsion).

## II Disparity direction determines orientation of ocular dominance stripes

Because the left and the right eye pathways do not converge before V1, the existence of binocular neurons in V1  suggests that the information from both eyes is recombined there. Moreover, many binocular neurons in V1 are disparity-tuned. , This requires intra-cortical wiring which connects cortical columns containing left/right eye representations of an object. To minimize the wirelength, the distance between these columns should be as small as possible.

For a given magnitude of binocular disparity, the distance between the columns containing left/right representations of an object depends on the orientation of ocular dominance stripes relative to the separation of the columns. To see this consider two alternative arrangements: ocular dominance stripes oriented perpendicular, Fig.3a, or parallel, Fig.3b, to the separation of the columns. One can think of V1 as being composed of interleaved stripes cut from the two topographic maps belonging to the two eyes. If one were to move across the stripes the representation of every point in the visual field is encoutered twice: once in a right-eye column, once in a left-eye column. Therefore the separation between the two columns containing left/right eye representations of the object is twice as big if the stripes are perpendicular compared to parallel to the separation between the columns. Thus for a given magnitude of disparity in the visual field the length of inter-eye connections is minimized if the ocular dominance stripes run in the direction corresponding to the disparity direction.

Several assumptions were made in this argument. First, I assumed the absence of stretching within the stripes which could change the distances across vs. along the stripes. To see whether this is a valid assumption I restate the argument in terms of the cortical magnification factor which has been measured experimentally. The separation between the two columns in V1 is given by the retinal disparity times the magnification factor. If the magnification factor across the stripes is greater than that along the stripes, the separation between the columns and hence the length of inter-eye connections is minimized by aligning the stripes with the disparity direction. Experiments show that the cortical magnification factor along the stripes is, indeed, about 1.5 times smaller than that across the stripes. Therefore, even though some stretching exists, my argument remains valid.

Second, I did not include wirelength of intra-eye connections in the cortex. These connections are responsible for monocular functions of V1 such as processing of contour orientation and color. The reason for neglecting these connections is their isotropy, that is they do not depend on the direction in the visual field. Therefore, orientation of the ocular dominance stripes should not affect the length of intra-eye connection.

Third, I neglected a possible specificity of inter-eye connections in respect to monocular functions of V1 such as orientational selectivity. Binocular neurons are likely to receive information from the neurons with the same preferred orientation. Moreover this preferred orientation should correlate with the disparity direction. However, this effect should not affect my argument because it averages out. Once all the possible orientations are included, the combined connections should be non-specific because different orientations are approximately equally represented.

Fourth, I assumed retinotopic mapping in V1. Although there is scatter in the receptive field location in a given cortical column, the magnitude of the scatter does not exceed the period of the ocular dominance pattern. Because I rely on retinotopy on the scales of several stripe widths (Fig.3) the argument remains valid.

Thus I showed that the orientation of ocular dominance stripes should follow the direction of disparity for the corresponding point of the visual field. To determine the optimal pattern of ocular dominance stripes I need to find disparity for all points in the visual field. Thus I need to calculate a binocular disparity map.

## III Calculation of the typical disparity map

In the previous Section, I argued that the ocular dominance pattern should follow the map of binocular disparity in order to minimize the length of intra-cortical wiring. However the direction and magnitude of the disparity for a given point in the visual field depends on the viewing conditions such as the distance to the object and the direction of gaze. Therefore I need to average disparity over these variables. The typical direction of disparity should determine the optimal orientation of ocular dominance stripes.

In order to find the disparity map I consider the origins of disparity in some detail. This is done in several steps by first considering a primate with the gaze direction fixed at straight ahead and then gradually adding degrees of freedom available to the eyeballs.

Consider two eyes fixating at optical infinity. Then, by definition, the images of the fixation point fall on the foveae of the two eyes. Moreover, all objects at infinity are imaged on the retinal locations which are the same distance and direction from the fovea in both eyes. Such locations send afferents to adjacent cortical columns and are called corresponding. (In reality, images of infinite objects may not fall on exactly corresponding points. For example, there is a $`2\mathrm{deg}`$ tilt of the vertical meridians., In this paper I neglect these deviations because they do not alter the results qualitatively.) Physiologically, stimulation of corresponding points results in a single perception of the object. Objects at finite distance away, however, are imaged at different retinal locations relative to the fovea, called non-corresponding. Binocular disparity is defined as a displacement of the left-eye image from the location on the left retina corresponding to the right-eye image of the same point object. Physiologically, finite-distance objects may still appear single due to sensory fusion if the disparity falls within a range called Panum’s fusional area. Otherwise the doubling of the perception or diplopia is experienced.

When the eyes fixate at optical infinity all the infinitely removed objects appear with zero disparity. To find disparity of other objects I use a geometrical construction illustrated in Fig.4. I fix the direction of gaze at straight ahead. The image of point $`O`$ in the right eye falls on the retinal point $`R`$ which belongs to the line passing through $`O`$ and the nodal point of the right eye $`N_R`$. The image of point $`O`$ in the left eye falls on the retinal point $`L^{}`$. A line passing through the left-eye nodal point $`N_L`$ and parallel to $`OR`$ intersects the retina at the point $`L`$, a point corresponding to $`R`$. The arc $`LL^{}`$ is the binocular disparity of point $`O`$. This arc belongs both to the retina and to a plane that passes through point $`O`$ and the nodal points of the two eyes, known as an epipolar plane. The common of the epipolar plane and the retina is called an epipolar line. Therefore the direction of disparity $`LL^{}`$ is along the epipolar line while its magnitude depends on the distance to point $`O`$. If point $`O`$ had a different elevation its disparity direction will be aligned with another epipolar line formed by the intersection of another epipolar plane and the retina. Therefore possible directions of disparity in the visual field are along epipolar lines formed by great circles passing through the interocular line. I call this disparity translational because it results from the horizontal displacement of the eyes.

Now I allow eyes to change the direction of gaze in the horizontal plane, while assuming that the center of rotation of an eyeball coincides with its nodal point. Then point $`O`$ is projected onto the same locations $`L^{}`$ and $`R`$ in head-centered coordinates. Point $`L`$ remains corresponding to $`R`$. However the eyes, and hence the retinae rotate under those points. Therefore, the direction of disparity in the retinal coordinates changes depending on the gaze direction. I calculate the frequency distribution of disparity directions by averaging over a uniform distribution of gaze directions within $`\pm 30\mathrm{deg}`$ of straight ahead.

The result is shown in Fig.5 as a grid of polar plots each of which corresponds to a particular point in the retinal coordinates. Each polar plot shows the frequency of different directions of disparity for a given point on the retina. The distribution of disparity exhibits strong anisotropy and the dominant disparity direction can be easily determined for all the retinal locations. If the only movements allowed to the eye were rotations around vertical axis then this would be a complete disparity map. Optimal ocular dominance pattern would be determined by transforming this map into cortical coordinates by using the magnification factor. This map agrees with the parafoveal stripe orientation in macaque but disagrees with it farther from the fovea.

Inclusion of different gaze elevations eliminates this disagreement. Naively, one may expect that the disparity map remains intact because the interocular line is the axis of rotational symmetry. However, vertical eye movements are accompanied by cyclotorsion,, or rotation of the eyeballs around the direction of gaze. The amplitude of cyclotorsion depends on the direction of gaze as specified by Listing’s law. (Listing’s law states that to determine the amplitude of cyclotorsion for an arbitrary direction of gaze one has to rotate the eye into that direction from the primary position around an axis which lies in a (Listing) plane.) According to the recent measurements  the amplitude of cyclotorsion is often unequal in the two eyes. Thus, although points $`L^{}`$ and $`R`$ remain fixed in the head-centered coordinates, point $`L`$ corresponding to $`R`$ rotates around the direction of gaze direction. This causes a cyclotorsional contribution to disparity which is oriented along concentric circles around the fovea.

The full binocular disparity includes cyclotorsional and translational contributions. Because translational contribution depends on the distance to an object while cyclotorsional does not, the direction of disparity depends on the distance to an object. Therefore, finding the typical disparity direction requires specifying a range of distances to objects that are perceived stereoscopically.

To define this range of distances I use the following argument. Because the cost of connections grows with their length, the pattern of connections in the cortex should not be far from isotropic. For a given location on the cortex, the circle of intra-cortical connections corresponds to an ellipse in the visual field because of the anisotropic magnification factor. The short axis of this ellipse $`a`$ is perpendicular to the direction corresponding to the stripes while the long axis $`b`$ is parallel. Information is recombined from all objects with disparity less than $`a`$ and is not recombined from any object with disparity greater than $`b`$. Whether information is recombined from objects with disparity in the interval $`[a;b]`$ depends on the orientation of ocular dominance stripes. In order to choose the optimal direction I need to calculate the frequencies of disparity directions for the object locations whose magnitude of disparity falls in the interval $`[a;b]`$. I choose the values of $`a`$ and $`b`$ as explained in Methods. Although, results of the calculation depend on the choice of parameters, they do not change qualitatively (see Discussion). The typical disparity map is shown in Fig.6.

## IV Discussion

Orienting ocular dominance stripes in the direction locally corresponding to the typical disparity optimizes the length of intra-cortical wiring needed for the perception of depth. Therefore, the wiring economy principle predicts that the ocular dominance pattern follows the map of typical disparities. This prediction agrees with the data as can be seen by comparing the map of typical disparities in Fig.6 with the data of LeVay et al. (1985), Fig.2. The map of typical disparities reproduces correctly the two major trends in the data: in the parafoveal region stripes tend to run horizontally, farther from the fovea, the pattern consists of isoeccentric stripes.

These trends result from the two major components of disparity: translational, due to the horizontal displacement of the eyes, and cyclotorsional, due to unequal rotation of the eyeballs around the gaze line (cyclotorsion). The relative magnitude of the two components depends on the distance to the fovea, Fig.7. In the parafoveal region, cyclotorsional disparity goes to zero linearly with eccentricity because rotational displacement is proportional to the radial distance from the axis of rotation passing through the fovea. At the same time, translational disparity remains finite for objects closer or farther than the point of fixation. Therefore, translational disparity dominates in the parafoveal region. Since the translational disparity is mostly horizontal, this explains the horizontal trend in the stripe orientation in parafoveal region. Farther from the fovea, cyclotorsional component of disparity may (or may not) become dominant depending on several parameters: the amplitude of cyclotorsion, the frequency of different viewing conditions, and the typical limit of depth perception. Along the horizontal meridian, cyclotorsional disparity is vertical, while translational is horizontal. Hence, the direction of the ocular dominance stripes must switch at the point where cyclotorsional component of disparity takes over the translational. This switch is evident in the macaque data, Fig.2 at about $`8\mathrm{deg}`$ eccentricity.

These trends in the orientation of ocular dominance stripes are not qualitatively affected by assumptions made in the calculation. For example, I assumed a uniform distribution of the gaze directions. Any reasonable bell-shaped distribution should lead to the same two trends in the ocular dominance pattern. Although I considered fixation at infinity my results are qualitatively correct for fixation at nearby objects. A simple geometrical argument shows that the translational disparity has a greater vertical component for close distances. Also, cyclotorsional disparity is greater because cyclotorsion increases with the vergence angle.,, Qualitatively, the ocular dominance pattern displays the same two trends. However the switch in the stripe orientation may occur at different eccentricity.

Generality of the trends in the stripe orientation confirms their functional significance. Ocular dominance patterns imaged in several macaques  show the two trends in the stripe orientation. Rosa et al. (1992) transformed into visual field cooridinates a complete ocular dominance pattern of Cebus monkeys. They found that the pattern was qualitatively similar to macaque with the stripe orientation switching at $`6\mathrm{deg}`$ and the first trend sometimes lacking. Preliminary data  on the ocular dominance pattern in humans is hard to analyze because precise topography in V1 is not known. Although the two trends are present, there is a significant interpersonal variability, possibly indicating varying significance of the two contributions to disparity from person to person.

Although, this theory reproduces the two major trends in the data, there is an unexplained trend in the macaque  and Cebus monkey  data. In the foveal region, less than $`1\mathrm{deg}`$ eccentricity, the orientation of stripes differs from the typically horizontal disparity there. I speculate that this may be due to fixation point being projected away from the V1-V2 border. To verify this suggestion a combined topographic and ocular dominance mapping is needed.

This theory relates ocular dominance pattern to the function of V1 allowing me to make several predictions. The location of the switch in the orientation of the ocular dominance stripes along the horizontal meridian should depend on the following parameters. Greater amplitude of cyclotorsion (or a greater frequency of gaze directions requiring cyclotorsion) increases cyclotorsional disparity and pushes the location of the switch in the stripe orientation towards the fovea. A greater extent of the Panum’s fusional area, $`b`$, achieves fusion for more objects with largely translational disparity. This should increase the eccentricity of the switch. Schwartz (1980) suggested that the size of the Panum’s fusional area and the width of the ocular dominance stripes are correlated between different species. If this is correct my theory implies that the species with greater width of ocular dominance stripes in the visual field should have the switch at higher eccentricity.

According to the theory, the functional significance of the orientation of ocular dominance stripes is in accommodating the typical disparity direction. Then processing of binocular disparity for any point of the visual field should be more efficient in the direction corresponding to the stripe orientation at that point. This predicts a greater number of disparity selective neurons for the direction of disparity corresponding to the stripe orientation as can be verified electrophysiologically. Also the limits of depth perception (for example, Panum’s fusional area) should be greater in the direction along the stripes than across as can be tested psychophysically.

In conclusion, I argued that the orientation of the ocular dominance stripes optimizes the length of intra-cortical wiring needed to process binocular disparity for depth perception. This argument supports the utility of the wiring economy principle as a powerful tool in relating organization of the cortex to its function.

## Methods

I obtained the disparity maps numerically for a grid of points on the right retina using the following algorithm. I found points in the visual field that project onto a given point on the right retina and calculated the location of their image on the left retina. The difference between the images’ coordinates on the left and the right retinae is binocular disparity. Multiplying it by the magnification factor I found disparity in cortical coordinates. Including only the points in the visual field with cortical disparity magnitude in the interval $`[a;b]`$ I calculated the frequencies of disparity directions averaged over all possible directions gaze.

I implemented the algorithm in MATLAB using the following parameters. The azimuth of the gaze directions as well as the elevation were uniformly distributed within $`30\mathrm{deg}`$ of straight ahead. The cyclotorsional misalignment was $`10\%`$ of the elevation angle. The point of fixation was at finite but large (2000 times interocular) distance. The expression for the cortical magnification factor was proportional to $`1/(e+e_2)`$ where $`e`$ is eccentricity and $`e2=2\mathrm{deg}`$. For the map shown in Fig.6 I chose $`a=0.5b`$ and $`b=0.13e`$ corresponding to the diameter of the Panum’s fusional area.

## Acknowledgments

I thank M.R. DeWeese, A.M. Zador, J.D. Pettigrew, R.J. Krauzlis, J.C. Horton, B.G. Cumming, E.M. Callaway, T.D. Albright and, in particular, C.F. Stevens for helpful discussions. This research was supported by a Sloan Fellowship in Theoretical Neurobiology.