1. Visual area V2 of macaque monkey cerebral cortex is the largest of the extrastriate visual areas, yet surprisingly little is known of its neuronal properties. We have made a quantitative analysis of V2 receptive field properties. Our set of measurements was chosen to distinguish neuronal responses reflecting parvocellular (P) or magnocellular (M) inputs and to permit comparison with similar measurements made in other visual areas; we further describe the relationship of those properties to the laminar and cytochrome oxidase (CO) architecture of V2. 2. We recorded the activity of single units representing the central 5 degrees in all laminae and CO divisions of V2 in anesthetized, paralyzed macaque monkeys. We studied responses to geometric targets and to drifting sinusoidal gratings that varied in orientation, spatial frequency, drift rate, contrast, and color. 3. The orientation selectivity and spatial and temporal tuning of V2 neurons differed little from those in V1. As in V1, spatial and temporal tuning in V2 appeared separable, and we identified a population of simple cells (more common within the central 3 degrees) similar to those found in V1. Contrast sensitivity of V2 neurons was greater on average than in V1, perhaps reflecting the summation of inputs in V2's larger receptive fields. Many V2 neurons exhibited some degree of chromatic opponency, responding to isoluminant color variations, but these neurons differed from V1 in the linearity with which they summate cone signals. 4. In agreement with others, we found that neurons with selective responses to color, size, and motion did seem to cluster in different CO compartments. However, this segregation of qualitatively different response selectivities was not absolute, and response properties also seemed to depend on laminar position within each compartment. As others also have noted, we found that CO stripe widths in the macaque (unlike in the squirrel monkey) did not consistently appear different. We relied on the segregation of qualitatively distinct cell types, and in some cases the pattern of Cat-301 staining as well, to distinguish CO stripes when the staining pattern of CO alone was ambiguous. Although all cell types were found in all CO compartments and laminae, unoriented cells were more prominent in layers 2-4 of "thin" stripes, direction-selective cells in layers 3B/4 of "thick" stripes, color-selective cells in the upper layers of thin and pale stripes, and end-stopped cells mainly outside of layer 4 in thin stripes.(ABSTRACT TRUNCATED AT 400 WORDS)
Amblyopia is a developmental disorder of pattern vision. After surgical creation of esotropic strabismus in the first weeks of life or after wearing -10 diopter contact lenses in one eye to simulate anisometropia during the first months of life, macaques often develop amblyopia. We studied the response properties of visual cortex neurons in six amblyopic macaques; three monkeys were anisometropic, and three were strabismic. In all monkeys, cortical binocularity was reduced. In anisometropes, the amblyopic eye influenced a relatively small proportion of cortical neurons; in strabismics, the influence of the two eyes was more nearly equal. The severity of amblyopia was related to the relative strength of the input of the amblyopic eye to the cortex only for the more seriously affected amblyopes. Measurements of the spatial frequency tuning and contrast sensitivity of cortical neurons showed few differences between the eyes for the three less severe amblyopes (two strabismic and one anisometropic). In the three more severely affected animals (one strabismic and two anisometropic), the optimal spatial frequency and spatial resolution of cortical neurons driven by the amblyopic eye were substantially and significantly lower than for neurons driven by the nonamblyopic eye. There were no reliable differences in neuronal contrast sensitivity between the eyes. A sample of neurons recorded from cortex representing the peripheral visual field showed no interocular differences, suggesting that the effects of amblyopia were more pronounced in portions of the cortex subserving foveal vision. Qualitatively, abnormalities in both the eye dominance and spatial properties of visual cortex neurons were related on a case-by-case basis to the depth of amblyopia. Quantitative analysis suggests, however, that these abnormalities alone do not explain the full range of visual deficits in amblyopia. Studies of extrastriate cortical areas may uncover further abnormalities that explain these deficits.
Neurons in primary visual cortex (V1) are thought to receive inhibition from other V1 neurons selective for a variety of orientations. Evidence for this inhibition is commonly found in cross-orientation suppression: responses of a V1 neuron to optimally oriented bars are suppressed by superimposed mask bars of different orientation. We show, however, that suppression is unlikely to result from intracortical inhibition. First, suppression can be obtained with masks drifting too rapidly to elicit much of a response in cortex. Second, suppression is immune to hyperpolarization (through visual adaptation) of cortical neurons responding to the mask. Signals mediating suppression might originate in thalamus, rather than in cortex. Thalamic neurons exhibit some suppression; additional suppression might arise from depression at thalamocortical synapses. The mechanisms of suppression are subcortical and possibly include the very first synapse into cortex.
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