Residual Binocular Interactions in the Striate Cortex of Monkeys Reared With Abnormal Binocular Vision

Abstract

We investigated the nature of residual binocular interactions in the striate cortex (V1) of monkey models for the two most common causes of visual dysfunction in young children, specifically anisometropia and strabismus. Infant rhesus monkeys were raised wearing either anisometropic spectacle lenses that optically defocused one eye or ophthalmic prisms that optically produced diplopia and binocular confusion. Earlier psychophysical investigations had demonstrated that all subjects exhibited permanent binocular vision deficits and, in some cases, amblyopia. When the monkeys were adults, the responses of individual V1 neurons were studied with the use of microelectrode recording techniques while the animals were anesthetized and paralyzed. The manner in which the signals from the two eyes were combined in individual cells was investigated by dichoptically stimulating both eyes simultaneously with drifting sine wave gratings. In both lens- and prism-reared monkeys, fewer neurons had balanced ocular dominances and greater numbers of neurons were excited by only one eye. However, many neurons that appeared to be monocular exhibited clear binocular interactions during dichoptic stimulation. For the surviving binocular neurons, the maximum binocular response amplitudes were lower than normal; fewer neurons, particularly complex cells, were sensitive to relative interocular spatial phase disparities; and the remaining disparity-sensitive neurons exhibited lower degrees of binocular interaction. In prism-reared monkeys, an unusually high proportion of complex cells exhibited binocular suppression during dichoptic stimulation. Binocular contrast summation experiments showed that for both cooperative and antagonistic binocular interactions, contrast signals from the two eyes were combined by individual neurons in a normal linear fashion in both lens- and prism-reared monkeys. The observed binocular deficits appear to reflect a reduction in functional inputs from one eye and/or spatial imprecision in the monocular receptive fields rather than an aberrant form of binocular interaction. In the prism-reared monkeys, the predominance of suppression suggests that inhibitory connections were, however, less susceptible to diplopia and confusion than excitatory connections. Overall, there were many parallels between V1 physiology in our monkey models and the residual vision of humans with anisometropia or strabismus.

Excitatory Contribution to Binocular Interactions in Human Visual Cortex Is Reduced in Strabismic Amblyopia

“…This indicated that the visual inputs from the two eyes were extremely imbalanced in strabismic amblyopes but not in anisometropic amblyopes, compared with normal binocular vision. This finding is consistent, at least in part, with a previous study that measured responses of single units in V1 of strabismic monkeys to dichoptic stimuli and attributed the observed binocular deficits to a reduction in functional inputs from one eye rather than an aberrant form of binocular interaction (Smith et al, 1997).…”

“…Overall, our results with low W target values in strabismic amblyopes along with the findings from single-neuron recordings and MEG/EEG measurements are in agreement with the proposal of attenuation of the visual input from the amblyopic eye in a psychophysical study (Baker et al, 2008). However, our study differs from these studies (Smith et al,1997;Baker et al, 2008;Chadnova et al, 2017), as it reveals not only weak input from the amblyopic eye of strabismic amblyopes (low W target ), but also poor excitation (low p term), resulting in poor binocular interactions.…”

Excitatory Contribution to Binocular Interactions in Human Visual Cortex Is Reduced in Strabismic Amblyopia

“…This indicated that the visual inputs from the two eyes were extremely imbalanced in strabismic amblyopes but not in anisometropic amblyopes, compared with normal binocular vision. This finding is consistent, at least in part, with a previous study that measured responses of single units in V1 of strabismic monkeys to dichoptic stimuli and attributed the observed binocular deficits to a reduction in functional inputs from one eye rather than an aberrant form of binocular interaction (Smith et al, 1997).…”

“…Overall, our results with low W target values in strabismic amblyopes along with the findings from single-neuron recordings and MEG/EEG measurements are in agreement with the proposal of attenuation of the visual input from the amblyopic eye in a psychophysical study (Baker et al, 2008). However, our study differs from these studies (Smith et al,1997;Baker et al, 2008;Chadnova et al, 2017), as it reveals not only weak input from the amblyopic eye of strabismic amblyopes (low W target ), but also poor excitation (low p term), resulting in poor binocular interactions.…”

Using high-resolution functional MRI to differentiate impacts of strabismic and anisometropic amblyopia on evoked ocular dominance activity in humans

“…Post-hoc analysis further showed that the evoked OD response in V1 was significantly larger in strabismic (p<10 -3 ) and anisometropic (p<10 -5 ) participants compared to controls without a significant difference between strabismic and anisometropic participants (p=0.22). Thus, in line with previous studies in humans (Conner et al, 2007) and non-human primates (Crawford and Von Noorden, 1979;Crawford et al, 1996;Smith III et al, 1997b;Kiorpes et al, 1998;Bi et al, 2011) studies, amblyopia increased the amplitude of the OD response in human V1 in our fMRI data.…”

Neuronal Correlates of Amblyopia in the Visual Cortex of Macaque Monkeys with Experimental Strabismus and Anisometropia

“…Yet the proportion of binocularly driven units was similar among neurons preferring low and high spatial frequencies for both strabismic and anisometropic monkeys; this is consistent with our previous results of amblyopia following unilateral atropinization (Movshon et al, 1987). However, it should be noted that our tests would not have detected the residual binocular interactions demonstrated by simultaneous binocular stimulation in strabismic and anisometropic monkeys by Smith et al (1997).…”

Excitatory Contribution to Binocular Interactions in Human Visual Cortex Is Reduced in Strabismic Amblyopia

“…This indicated that the visual inputs from the two eyes were extremely imbalanced in strabismic amblyopes but not in anisometropic amblyopes, compared with normal binocular vision. This finding is consistent, at least in part, with a previous study that measured responses of single units in V1 of strabismic monkeys to dichoptic stimuli and attributed the observed binocular deficits to a reduction in functional inputs from one eye rather than an aberrant form of binocular interaction (Smith et al, 1997).…”

“…Overall, our results with low W target values in strabismic amblyopes along with the findings from single-neuron recordings and MEG/EEG measurements are in agreement with the proposal of attenuation of the visual input from the amblyopic eye in a psychophysical study (Baker et al, 2008). However, our study differs from these studies (Smith et al,1997;Baker et al, 2008;Chadnova et al, 2017), as it reveals not only weak input from the amblyopic eye of strabismic amblyopes (low W target ), but also poor excitation (low p term), resulting in poor binocular interactions.…”

Using high-resolution functional MRI to differentiate impacts of strabismic and anisometropic amblyopia on evoked ocular dominance activity in humans

“…Post-hoc analysis further showed that the evoked OD response in V1 was significantly larger in strabismic (p<10 -3 ) and anisometropic (p<10 -5 ) participants compared to controls without a significant difference between strabismic and anisometropic participants (p=0.22). Thus, in line with previous studies in humans (Conner et al, 2007) and non-human primates (Crawford and Von Noorden, 1979;Crawford et al, 1996;Smith III et al, 1997b;Kiorpes et al, 1998;Bi et al, 2011) studies, amblyopia increased the amplitude of the OD response in human V1 in our fMRI data.…”

Neuronal Correlates of Amblyopia in the Visual Cortex of Macaque Monkeys with Experimental Strabismus and Anisometropia

“…Yet the proportion of binocularly driven units was similar among neurons preferring low and high spatial frequencies for both strabismic and anisometropic monkeys; this is consistent with our previous results of amblyopia following unilateral atropinization (Movshon et al, 1987). However, it should be noted that our tests would not have detected the residual binocular interactions demonstrated by simultaneous binocular stimulation in strabismic and anisometropic monkeys by Smith et al (1997).…”

Excitatory Contribution to Binocular Interactions in Human Visual Cortex Is Reduced in Strabismic Amblyopia

“…This indicated that the visual inputs from the two eyes were extremely imbalanced in strabismic amblyopes but not in anisometropic amblyopes, compared with normal binocular vision. This finding is consistent, at least in part, with a previous study that measured responses of single units in V1 of strabismic monkeys to dichoptic stimuli and attributed the observed binocular deficits to a reduction in functional inputs from one eye rather than an aberrant form of binocular interaction (Smith et al, 1997).…”

“…Overall, our results with low W target values in strabismic amblyopes along with the findings from single-neuron recordings and MEG/EEG measurements are in agreement with the proposal of attenuation of the visual input from the amblyopic eye in a psychophysical study (Baker et al, 2008). However, our study differs from these studies (Smith et al,1997;Baker et al, 2008;Chadnova et al, 2017), as it reveals not only weak input from the amblyopic eye of strabismic amblyopes (low W target ), but also poor excitation (low p term), resulting in poor binocular interactions.…”

Using high-resolution functional MRI to differentiate impacts of strabismic and anisometropic amblyopia on evoked ocular dominance activity in humans

“…Post-hoc analysis further showed that the evoked OD response in V1 was significantly larger in strabismic (p<10 -3 ) and anisometropic (p<10 -5 ) participants compared to controls without a significant difference between strabismic and anisometropic participants (p=0.22). Thus, in line with previous studies in humans (Conner et al, 2007) and non-human primates (Crawford and Von Noorden, 1979;Crawford et al, 1996;Smith III et al, 1997b;Kiorpes et al, 1998;Bi et al, 2011) studies, amblyopia increased the amplitude of the OD response in human V1 in our fMRI data.…”

Neuronal Correlates of Amblyopia in the Visual Cortex of Macaque Monkeys with Experimental Strabismus and Anisometropia

“…Yet the proportion of binocularly driven units was similar among neurons preferring low and high spatial frequencies for both strabismic and anisometropic monkeys; this is consistent with our previous results of amblyopia following unilateral atropinization (Movshon et al, 1987). However, it should be noted that our tests would not have detected the residual binocular interactions demonstrated by simultaneous binocular stimulation in strabismic and anisometropic monkeys by Smith et al (1997).…”