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Receptive fields of disparity-selective neurons in macaque striate cortex

A Correction to this article was published on 01 April 2000

Abstract

To identify neuronal mechanisms underlying stereopsis, we characterized interactions between inputs from the two eyes in disparity-selective neurons in macaque V1. All disparity-selective cells showed suppressive interactions between the right and left eyes, and some showed facilitatory interactions. Disparity selectivity was narrower than the receptive-field width and was constant across the receptive field. Such position-invariant disparity selectivity is also found in anesthetized cat V1. Complex cells have been suggested to inherit their disparity selectivity from simple cells with receptive fields mismatched between the two eyes. However, we found no such antecedent disparity-tuned simple cells. We did find disparity-selective cells with some simple-cell characteristics, but surprisingly, they also showed position-invariant disparity selectivity rather than simple linear binocular interactions.

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Figure 1: Objects nearer or farther than the plane of fixation cast images on noncorresponding parts of the two retinae; arrowheads indicate corresponding positions.
Figure 2: Responses from a 'tuned near' complex cell.
Figure 3: Reverse-correlation binocular-response maps corrected for eye position (top row) and binocular nonlinear interaction maps (bottom row) at 60 ms before each spike for a 'tuned far' complex cell recorded in alert macaque V1.
Figure 4: Elongation ratio and angle of the peak region in binocular response maps for all disparity-tuned cells in this study in addition to 27 non-stereo cells.
Figure 5: Reverse-correlation binocular-response maps corrected for eye position and binocular non-linear interaction maps for a 'tuned inhibitory' cell.
Figure 6: Reverse-correlation binocular-response maps corrected for eye position for four cells with spatially offset light- and dark-excitatory response regions.
Figure 7: (a) Optimum horizontal disparities (determined from binocular response maps) as functions of spatial offset of the peaks in the two eyes' receptive fields for complex cells and for spatially offset cells.

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Acknowledgements

This work was funded by NIH grant EY10203. David Freeman did the computer programming. Gail Robertson provided technical assistance. Clay Reid, Bevil Conway, Terrence Sejnowski, Rajesh Rao, Niall McLoughlin, Bartlett Mel and Tomaso Poggio provided suggestions on the manuscript.

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Correspondence to Margaret S. Livingstone.

Supplementary information

These two figures show the spatial resolution of our reverse-correlation mapping technique after correction for eye position. The first figure shows binocular response maps and receptive-field profiles for two binocular, nonstereo-tuned cells that had small receptive fields, to demonstrate the resolution of the technique for both eyes mapped simultaneously. These cells had receptive fields very near the fovea, so the receptive fields were relatively small, allowing us to compare the resolution of the mapping for the two eyes. Despite monitoring only one eye, the receptive-field maps for both cells were approximately the same size for the two eyes. The fact that the right-eye maps were not noticeably less precise than the left-eye maps indicates that, at least during these mapping sessions, most of the time the monkey kept his eyes at a constant vergence, presumably because he was fixated on the plane of the monitor. The maps of foveal receptive fields in the first figure show that we could map receptive fields at least as small as 0.2ƒ wide. We never mapped smaller receptive fields, so that may be the resolution limit of our technique.

Figure 1

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Binocular-response maps (first and third rows) and receptive-field profiles (second and fourth rows) for two parafoveal binocular cells with tiny receptive fields recorded in alert macaque V1. The receptive-field eccentricities for these two cells were 1.5ƒ for the upper cell and 1.6ƒ for the lower cell. For the maps, two bar stimuli, one for each eye, were flashed simultaneously. The binocular-response maps represent firing rate as a function of stimulus location on the left retina (horizontal axis) and right retina (vertical axis). Vertical and horizontal lines in each panel indicate the center of the stimulus-presentation range for the left and right eyes, respectively. The binocular-interaction maps in the first row and the receptive-field profiles in the second row are from one cell, and the maps in the third row and the profiles in the fourth row are from a another cell. The left column shows responses to light bars on a black background, and the right column shows responses to dark bars on a light background. In the receptive-field profiles, red traces indicate right-eye responses; green, left-eye responses. Note that the horizontal arms and red traces (right-eye response; unmonitored eye) are not much less precise than the vertical arms and green traces. Note also that the receptive field widths (height at 1/e of peak) are about 0.2ƒ wide.

Figure 2

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The second figure shows that we can map receptive-field subunits at eccentricities as small as4-6ƒ, at least for some cells. This figure shows binocular-interaction maps for three monocular units that showed spatial segregation of ON and OFF responses. Each row represents a different cell mapped with light bars or dark bars, as indicated. (We deduce that these cells were monocular because they show only one arm instead of a cross in the binocular reponse profiles.) The middle unit was not orientation selective and was recorded in the white matter, and therefore probably represents a geniculate afferent fiber. It shows center/surround antagonism, in that a 0.3ƒ wide area shows an excitatory response to dark stimuli, and a slightly wider (0.5ƒ) region shows inhibition by light stimuli. The upper and lower units were orientation selective and, on physiological criteria, were probably located in layer 4C. The lower unit shows a central dark-excitatory region flanked by two light-excitatory regions. The upper unit shows spatially offset light-excitatory and dark-excitatory subregions, with the OFF subregion lying to the left of the ON subregion. The top cell had a receptive-field eccentricity of 4.6ƒ; the middlecell, 5ƒ and the bottom cell, 5.5ƒ. Conventions as in Fig. 1. The vertical maps (top and bottom rows) represent cells driven only by the left eye; the middle map represents a cell driven by the right eye.

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Livingstone, M., Tsao, D. Receptive fields of disparity-selective neurons in macaque striate cortex . Nat Neurosci 2, 825–832 (1999). https://doi.org/10.1038/12199

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