In the primate visual system, area V4 is located in the ventral pathway and is traditionally thought to be involved in processing color and form information. However, little is known about its functional role in processing motion information. Using intrinsic signal optical imaging over large fields of view in V1, V2, and V4, we mapped the direction of motion responses in anesthetized macaques. We found that V4 contains direction-preferring domains that are preferentially activated by stimuli moving in one direction. These direction-preferring domains normally occupy several restricted regions of V4 and tend to overlap with orientation- and color-preferring domains. Single-cell recordings targeting these direction-preferring domains also showed a clustering, as well as a columnar organization of V4 direction-selective neurons. These data suggest that, in contrast to the classical view, motion information is also processed in ventral pathway regions such as area V4.

Two incongruent images viewed by the two eyes cause binocular rivalry, during which observers perceive continuous alternations between these two visual images. Previous studies in both humans and monkeys have shown that the primary visual cortex (V1) plays a critical role in the rivalry perception. However, it is unclear whether the rivalry activity observed in V1 relies on conscious influences. Here, we examine the responses of V1 in monkeys under general anesthesia. With intrinsic signal optical imaging and single-trial analysis, alternating activation of ocular dominance columns in V1 was observed during binocularly incongruent stimulation. Left-and right-eye columns exhibited counterphase activation, which were modulated by stimulus features in ways similar to those found in conscious human observers. These observations indicated that binocular rivalry occurs in V1 without consciousness, suggesting that the low-level automatic mechanisms play a more important role than previously believed in handling visual ambiguities.

The ability to extract the shape of moving objects is fundamental to visual perception. However, where such computations are processed in the visual system is unknown. To address this question, we used intrinsic signal optical imaging in awake monkeys to examine cortical response to perceptual contours defined by motion contrast (motion boundaries, MBs). We found that MB stimuli elicit a robust orientation response in area V2. Orientation maps derived from subtraction of orthogonal MB stimuli aligned well with the orientation maps obtained with luminance gratings (LGs). In contrast, area V1 responded well to LGs, but exhibited a much weaker orientation response to MBs. We further show that V2 direction domains respond to motion contrast, which is required in the detection of MB in V2. These results suggest that V2 represents MB information, an important prerequisite for shape recognition and figure-ground segregation.

Graphical Abstract Highlights d DS neurons in a non-dorsal visual area (V2) were studied with map-guided recordings d V2 DS neurons exhibit features distinct from the DS neurons in the dorsal area MT d Clusters of V2 DS neurons form functional architectures sensitive to motion contrast d Response properties of V2 DS neurons are suitable for figureground segregation SUMMARY In the primate visual system, direction-selective (DS) neurons are critical for visual motion perception. While DS neurons in the dorsal visual pathway have been well characterized, the response properties of DS neurons in other major visual areas are largely unexplored. Recent optical imaging studies in monkey visual cortex area 2 (V2) revealed clusters of DS neurons. This imaging method facilitates targeted recordings from these neurons. Using optical imaging and single-cell recording, we characterized detailed response properties of DS neurons in macaque V2. Compared with DS neurons in the dorsal areas (e.g., middle temporal area [MT]), V2 DS neurons have a smaller receptive field and a stronger antagonistic surround. They do not code speed or plaid motion but are sensitive to motion contrast. Our results suggest that V2 DS neurons play an important role in figure-ground segregation. The clusters of V2 DS neurons are likely specialized functional systems for detecting motion contrast.

Binocular disparity information is an important source of 3D perception. Neurons sensitive to binocular disparity are found in almost all major visual areas in nonhuman primates. In area V4, disparity processes are suggested for the purposes of 3D-shape representation and fine disparity perception. However, whether neurons in V4 are sensitive to disparity-defined edges used in shape representation is not clear. Additionally, a functional organization for disparity edges has not been demonstrated so far. With intrinsic signal optical imaging, we studied functional organization for disparity edges in the monkey visual areas V1, V2, and V4. We found that there is an orientation map in V4 activated by edges purely defined by binocular disparity. This map is consistent with the orientation map obtained with regular luminance-defined edges, indicating a cue-invariant edge representation in this area. In contrast, such a map is much weaker in V2 and totally absent in V1. These findings reveal a hierarchical processing of 3D shape along the ventral pathway and the important role that V4 plays in shape-from-disparity detection.

The way we perceive objects as permanent contrasts with the short-lived responses of visual cortical neurons. A theory postulates pointers that give objects continuity, predicting a class of neurons that respond not only to visual objects but also when an occluded object moves into their receptive field. Here, we tested this theory with a novel paradigm in which a monkey freely scans an array of objects while some of them are transiently occluded.

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