For nearly all of the classical work on neural processing of binocular disparity, the assumption has been that the relevant separation of signals to the two eyes occurs because of a position shift of one image with respect to the other. Nearly all the work on the physiological basis of disparity processing assumes a position shift. However, there is an alternative mechanism involving a phase shift that can also achieve retinal disparity. Phase shift can occur when the internal structure of the receptive fields for right and left eyes are dissimilar. Although previous studies did not find dissimilarities,9 we used a specific quantitative technique that provided detailed receptive field maps and found clear evidence of asymmetries in left and right eye patterns.10,11 Position and phase disparity processes are illustrated in Figs. 6 and 7. In both diagrams, fixation planes are shown along with relatively far and near positions. The depicted receptive field shapes in Fig. 6 illustrate a gradual lateral shift in image position in the right eye whereas that in the left remains constant. In Fig. 7, the left receptive field image remains constant whereas those in the right eye change shape but not position. The creation of retinal disparity by these two different mechanisms is illustrated in Fig. 8. At the top, a relatively far distance is indicated by the disparity tuning function shown on the right. At the bottom, the same relative shift in disparity is illustrated and is achieved by different internal receptive field structure between left and right eyes. We have performed detailed neurophysiological experiments in which we recorded from individual cells in the primary visual cortex (Area 17) of the cat. In these studies, binocular neurons were activated with sinusoidal gratings arranged to test phase or position disparities. Results demonstrate clearly that most cortical cells respond to both phase and position in varying degrees.10,11
A basic functional question that we have addressed concerns the rules by which signals from left and right eyes are combined in the visual cortex. The simplest mechanism might be a symmetrical linear combination of inputs from the two eyes. A second possibility is that of multiplicative convergence in which a given cortical cell may be unresponsive to input through either eye but responds clearly to simultaneous input from both eyes together. Another possibility is to have symmetrical inputs that are modified by presynaptic or postsynaptic input of an inhibitory or excitatory nature. For a considerable amount of published data, the mechanism appears to be that of linear summation in combination with a threshold mechanism that follows binocular convergence. Another type of binocular interaction consists of a multiplicative process that may apply to both simple and complex cortical cell types.12,13
We have designed and used a unique test to determine the degree of linearity of binocular summation as illustrated in Fig. 9.12,14 Two processing systems are depicted. On the left, input to the right eye is blocked whereas that to the left is open. The initial input goes to a series of subunits and then via nonlinearities (triangles), the pathway converges to a cortical cell. It is assumed that the subunits have identical neural images via linear binocular convergence. The stimulus to the left eye is a counter-phase grating, which results in a frequency-doubled response as shown in previous work.15 The second diagram, on the right, is similar to that on the left, but visual stimulation occurs to both left and right eyes. In this case, the left eye is activated by a sinusoidal grating that drifts to the right at 2 Hz. An identical grating stimulates the right eye, but the direction of drift is to the left instead of the right. We know from wave theory that the combination depicted on the right of this diagram is a combined sinusoidal pattern of twice the amplitude of either stimulus alone which counter-phases in place instead of drifting in either direction. If there is a linear combination of left and right eye stimuli, the resulting input at the combined stage is a counter-phase grating identical to that illustrated in the diagram on the left. If this occurs in the neurophysiological test of cortical cells, we may conclude that binocular summation is linear. Experimental tests with cortical cells have verified this prediction.14
We have conducted a series of experiments in which single neuron recordings have been made in visual cortex to determine binocular characteristics.12–14,16–18 An example of the kind of data we have obtained for a typical simple cell is illustrated in Fig. 10. The upper two panels show typical monocular tuning functions for orientation and spatial frequency variables. As the data demonstrate, tuning functions are similar for left and right eye stimulus conditions for both orientation and spatial frequency variables. Right and left eye response strength varies for both parameters. The lower left panel shows results of binocular stimulation in the form of harmonic analysis of post-stimulus time histograms of responses to different relative intraocular phase values. The data show typical modulated discharge with bursts of firing at the first harmonic of the temporal frequency of the stimulus grating. Note the differences in response as relative intraocular phase is varied. For some relative intraocular phases, responses are strong whereas others are weak and, in this case, even silent at a relative intraocular phase of 180°. The graphical form of this histogram is shown on the lower right, which plots responses for relative phase differences. The sinusoidal response curve shown here is typical for simple cells in the visual cortex.
In the example shown above, left and right eye stimuli are identical. It is also of interest to do similar tests when stimuli to the two eyes are different. Specifically, what happens to binocular interaction when the stimulus to one eye is weaker than that to the other? Adaptation to different levels of visual stimuli is a basic feature of processing. The retina adjusts to absolute light levels and visual cortical cells adapt to different contrast levels.19,20 Comparisons of monocular and binocular contrast encoding suggest that the main adjustments occur at a monocular level.21 Effective contrast in the human visual system can be weak in one eye and strong in the other. Clinically, this can occur and cause diminished binocular function. Behavioral tests verify that reduced contrast in one eye can cause a marked reduction in stereo function.22,23 We undertook neurophysiological studies in which contrast differences were used for left and right eye sinusoidal grating stimuli to determine effects on binocular interaction. Our findings, illustrated in Fig. 11, show two sets of results for phase-varying binocular stimulation. In the upper sequence, results are shown for two identical gratings presented at different relative intraocular phases to a cortical cell. The result shown on the top left is a typical response pattern, as noted above, for a cortical simple cell. In the bottom part of the figure, an identical test is conducted with the same neuron only in this case; there is an order of magnitude difference in contrast levels (5% and 50%) between left and right eye stimuli. What is surprising here is that the response curve shown on the left exhibits a closely similar sinusoidal response to that for the equal contrast stimuli. The only clear difference is that the response magnitude at the bottom is reduced to about half that exhibited above for the equal contrast left and right eye gratings.
These results have been verified for a population of cortical cells in our work and that of others (for example24) and suggest clearly that there is a compensatory mechanism that provides a relatively constant binocular interaction. If we assume that a low contrast grating stimulus causes a raised response threshold, the implication is that there is a synaptic gain of signals from the weak input eye. The gain is presumably high when input contrast is low and the reverse for high input contrast. Two compensatory mechanisms are suggested. In one, a threshold process occurs after convergence of input from both eyes. A second possible mechanism is a monocular gain control that occurs at the synaptic contact between an eye and a cortical neuron. This latter process can result in the relatively similar binocular interaction profile for different right and left eye contrast grating stimuli. We have recently confirmed using behavioral techniques that a degree of binocular integration occurs even during substantial differences in signal strength between left and right eyes.25
The frontal position of the two eyes in the primate visual system provides the basis for fine binocular perception. Specifically, left and right eye views provide corresponding retinal images that are slightly displaced from each other. This retinal disparity is the necessary and sufficient condition for stereoscopic depth discrimination. Numerous behavioral and electrophysiological studies have been conducted to elucidate this system. Investigations of individual cortical neurons have resulted in a basic understanding of the neural organization of binocular vision. Our laboratory has undertaken a series of studies of this process. The current brief review concerns three aspects of binocular vision. First, binocular disparity is encoded by differences in relative retinal position or receptive field internal structure of images from left and right eyes. Second, we designed a unique test to determine that early binocular combination in the visual cortex is a linear process. Subsequent processing involves intracortical nonlinear events. Third, binocular interaction in the visual cortex is retained during unequal stimulation of left and right eye pathways. This suggests the involvement of a gain control mechanism.
1. Pettigrew JD. Binocular Interaction on Single Units of the Striate Cortex of the Cat. Bachelor of Science thesis. Sydney, Australia: University of Sydney; 1965.
2. Barlow HB, Blakemore C, Pettigrew JD. The Neural Mechanism of Binocular Depth Discrimination. J Physiol 1967;193:327–42.
3. Bishop PO, Henry GH, Smith CJ. Binocular Interaction Fields of Single Units in the Cat Striate Cortex. J Physiol 1971;216:39–68.
4. Joshua DE, Bishop PO. Binocular Single Vision and Depth Discrimination. Receptive Field Disparities for Central and Peripheral Vision and Binocular Interaction on Peripheral Single Units in Cat Striate Cortex. Exp Brain Res 1970;10:389–416.
5. Nikara T, Bishop PO, Pettigrew JD. Analysis of Retinal Correspondence by Studying Receptive Fields of Binocular Single Units in Cat Striate Cortex. Exp Brain Res 1968;6:353–72.
6. Poggio GF, Fischer B. Binocular Interaction and Depth Sensitivity in Striate and Prestriate Cortex of Behaving Rhesus Monkey. J Neurophysiol 1977;40:1392–405.
7. Poggio GF, Talbot WH. Mechanisms of Static and Dynamic Stereopsis in Foveal Cortex of the Rhesus Monkey. J Physiol 1981;315:469–92.
8. Poggio GF, Gonzalez F, Krause F. Stereoscopic Mechanisms in Monkey Visual Cortex: Binocular Correlation and Disparity Selectivity. J Neurosci 1988;8:4531–50.
9. Hubel DH, Wiesel TN. Receptive Fields, Binocular Interaction and Functional Architecture in the Cat’s Visual Cortex. J Physiol 1962;160:106–54.
10. Anzai A, Ohzawa I, Freeman RD. Neural Mechanisms Underlying Binocular Fusion and Stereopsis: Position vs. Phase. Proc Natl Acad Sci U S A 1997;94:5438–43.
11. Anzai A, Ohzawa I, Freeman RD. Neural Mechanisms for Encoding Binocular Disparity: Receptive Field Position Versus Phase. J Neurophysiol 1999;82:874–90.
12. Ohzawa I, Freeman RD. The Binocular Organization of Simple Cells in the Cat’s Visual Cortex. J Neurophysiol 1986;56:221–42.
13. Freeman RD. The Cortical Organization of Binocular Vision. In: Werner JS, Chalupa LM, eds. The New Visual Neurosciences. Cambridge, MA: MIT Press; 2014; chapter 27.
14. Ohzawa I, Freeman RD. The Binocular Organization of Complex Cells in the Cat’s Visual Cortex. J Neurophysiol 1986;56:243–59.
15. Movshon JA, Thompson ID, Tolhurst DJ. Spatial and Temporal Contrast Sensitivity of Neurones in Areas 17 and 18 of the Cat’s Visual Cortex. J Physiol 1978;283:101–20.
16. Ohzawa I, DeAngelis GC, Freeman RD. Stereoscopic Depth Discrimination in the Visual Cortex: Neurons Ideally Suited as Disparity Detectors. Science 1990;249:1037–41.
17. Ohzawa I, DeAngelis GC, Freeman RD. Encoding of Binocular Disparity by Simple Cells in the Cat’s Visual Cortex. J Neurophysiol 1996;75:1779–805.
18. Ohzawa I, DeAngelis GC, Freeman RD. Encoding of Binocular Disparity by Complex Cells in the Cat’s Visual Cortex. J Neurophysiol 1997;77:2879–909.
19. Ohzawa I, Sclar G, Freeman RD. Contrast Gain Control in the Cat’s Visual System. J Neurophysiol 1985;54:651–67.
20. Sclar G, Ohzawa I, Freeman RD. Contrast Gain Control in the Kitten’s Visual System. J Neurophysiol 1985;54:668–75.
21. Truchard AM, Ohzawa I, Freeman RD. Contrast Gain Control in the Visual Cortex: Monocular versus Binocular Mechanisms. J Neurosci 2000;20:3017–32.
22. Schor C, Heckmann T. Interocular Differences in Contrast and Spatial Frequency: Effects on Stereopsis and Fusion. Vision Res 1989;29:837–47.
23. Legge GE, Gu YC. Stereopsis and Contrast. Vision Res 1989;29:989–1004.
24. Smith EL 3rd, Chino YM, Ni J, et al. Residual Binocular Interactions in the Striate Cortex of Monkeys Reared with Abnormal Binocular Vision. J Neurophysiol 1997;78:1353–62.
25. Kim T, Freeman RD. Binocular Function during Unequal Monocular Input. Eur J Neurosci 2017;45:601–9.