There is no generally accepted account of the function of the second visual cortical area (V2), partly because no simple response properties robustly distinguish V2 neurons from those in primary visual cortex (V1). We constructed synthetic stimuli replicating the higher-order statistical dependencies found in natural texture images, and used them to stimulate macaque V1 and V2 neurons. Most V2 cells responded more vigorously to these textures than to control stimuli lacking naturalistic structure; V1 cells did not. fMRI measurements in humans revealed differences between V1 and V2 that paralleled the neuronal measurements. The ability of human observers to detect naturalistic structure in different types of texture was well predicted by the strength of neuronal and fMRI responses in V2 but not in V1. Together, these results reveal a novel and particular role for V2 in the representation of natural image structure.

As information propagates along the ventral visual hierarchy, neuronal responses become both more specific for particular image features and more tolerant of image transformations that preserve those features. Here, we present evidence that neurons in area V2 are selective for local statistics that occur in natural visual textures, and tolerant of manipulations that preserve these statistics. Texture stimuli were generated by sampling from a statistical model, with parameters chosen to match the parameters of a set of visually distinct natural texture images. Stimuli generated with the same statistics are perceptually similar to each other despite differences, arising from the sampling process, in the precise spatial location of features. We assessed the accuracy with which these textures could be classified based on the responses of V1 and V2 neurons recorded individually in anesthetized macaque monkeys. We also assessed the accuracy with which particular samples could be identified, relative to other statistically matched samples. For populations of up to 100 cells, V1 neurons supported better performance in the sample identification task, whereas V2 neurons exhibited better performance in texture classification. Relative to V1, the responses of V2 show greater selectivity and tolerance for the representation of texture statistics. These responses are typically characterized by measuring selectivity for specific visual attributes, such as light intensity or color, and local structural properties, such as spatial position, orientation, and spatial frequency. Stimulus selectivity, along with the complementary notion of "invariance" or "tolerance" to irrelevant variation, provides a de facto language for describing the functional roles and relationships of neurons in visual areas. For example, simple cells in the primary visual cortex, area V1, are selective for orientation (1) and spatial frequency (2-4). Complex cells exhibit similar selectivity, but are also more tolerant to changes in spatial position (1,5,6). Component cells in area MT (or V5) exhibit selectivity for orientation and speed, but (relative to their V1 inputs) are more tolerant of changes in location and spatial frequency, whereas MT pattern cells are tolerant to changes in orientation (and, more generally, spatial structure) (7).Neurons in the inferotemporal visual cortex (IT) are selective for visual images of particular objects, but are tolerant to identitypreserving transformations, such as translation, rotation, or background context (8,9). This tolerance increases from area V4 to IT (10), suggesting that an increase in selectivity is balanced by an increase in tolerance, preserving overall response levels and their distribution across neurons (11). However, the selectivity and tolerance of visual representations in midventral areas, particularly area V2, have been more difficult to establish because we lack knowledge of the relevant visual attributes. V2 neurons receive much of their afferent drive from V1, have receptive fields that are r...

Amblyopia is a developmental disorder resulting in poor vision in one eye. The mechanism by which input to the affected eye is prevented from reaching the level of awareness remains poorly understood. We recorded simultaneously from large populations of neurons in the supragranular layers of areas V1 and V2 in 6 macaques that were made amblyopic by rearing with artificial strabismus or anisometropia, and 1 normally reared control. In agreement with previous reports, we found that cortical neuronal signals driven through the amblyopic eyes were reduced, and that cortical neurons were on average more strongly driven by the non-amblyopic than by the amblyopic eyes. We analyzed multiunit recordings using standard population decoding methods, and found that visual signals from the amblyopic eye, while weakened, were not degraded enough to explain the behavioral deficits. Thus additional losses must arise in downstream processing. We tested the idea that under monocular viewing conditions, only signals from neurons dominated by – rather than driven by – the open eye might be used. This reduces the proportion of neuronal signals available from the amblyopic eye, and amplifies the interocular difference observed at the level of single neurons. We conclude that amblyopia might arise in part from degradation in the neuronal signals from the amblyopic eye, and in part from a reduction in the number of signals processed by downstream areas.

Responses of individual task-relevant sensory neurons can predict monkeys' trial-by-trial choices in perceptual decision-making tasks. Choice-correlated activity has been interpreted as evidence that the responses of these neurons are causally linked to perceptual judgments. To further test this hypothesis, we studied responses of orientation-selective neurons in V1 and V2 while two macaque monkeys performed a fine orientation discrimination task. Although both animals exhibited a high level of neuronal and behavioral sensitivity, only one exhibited choice-correlated activity. Surprisingly, this correlation was negative: when a neuron fired more vigorously, the animal was less likely to choose the orientation preferred by that neuron. Moreover, choice-correlated activity emerged late in the trial, earlier in V2 than in V1, and was correlated with anticipatory signals. Together, these results suggest that choice-correlated activity in task-relevant sensory neurons can reflect postdecision modulatory signals.