Comparison of the color selectivity of macaque V4 neurons in different color spaces.

Chromatic selectivity has been studied extensively in various visual areas at different stages of visual processing in the macaque brain. In these studies, color stimuli defined in the Derrington-Krauskopf-Lennie (DKL) color space with a limited range of cone contrast were typically used in early stages, whereas those defined in the Commission Internationale de l'Eclairage (CIE) color space, based on human psychophysical measurements across the gamut of the display, were often used in higher visual areas. To understand how the color information is processed along the visual pathway, it is necessary to compare color selectivity obtained in different areas on a common color space. In the present study, we tested whether the neural color selectivity obtained in DKL space can be predicted from responses obtained in CIE space and whether stimuli with limited cone contrast are sufficient to characterize neural color selectivity. We found that for most V4 neurons, there was a strong correlation between responses measured using the two chromatic coordinate systems, and the color selectivities obtained with the two stimulus sets were comparable. However, for some neurons preferring high- or low-saturation colors, stimuli defined in DKL color space did not adequately capture the neural color selectivity. This is mainly due to the use of stimuli within a limited range of cone contrast. We conclude that regardless of the choice of color space, the sampling of colors across the entire gamut is important to characterize neural color selectivity fully or to compare color selectivities in different areas so as to understand color representation in the visual system.

Supranormal orientation selectivity of visual neurons in orientation-restricted animals.

Altered sensory experience in early life often leads to remarkable adaptations so that humans and animals can make the best use of the available information in a particular environment. By restricting visual input to a limited range of orientations in young animals, this investigation shows that stimulus selectivity, e.g., the sharpness of tuning of single neurons in the primary visual cortex, is modified to match a particular environment. Specifically, neurons tuned to an experienced orientation in orientation-restricted animals show sharper orientation tuning than neurons in normal animals, whereas the opposite was true for neurons tuned to non-experienced orientations. This sharpened tuning appears to be due to elongated receptive fields. Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment. The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons. This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

Neural representation of motion-in-depth in area MT.

Neural processing of 2D visual motion has been studied extensively, but relatively little is known about how visual cortical neurons represent visual motion trajectories that include a component toward or away from the observer (motion in depth). Psychophysical studies have demonstrated that humans perceive motion in depth based on both changes in binocular disparity over time (CD cue) and interocular velocity differences (IOVD cue). However, evidence for neurons that represent motion in depth has been limited, especially in primates, and it is unknown whether such neurons make use of CD or IOVD cues. We show that approximately one-half of neurons in macaque area MT are selective for the direction of motion in depth, and that this selectivity is driven primarily by IOVD cues, with a small contribution from the CD cue. Our results establish that area MT, a central hub of the primate visual motion processing system, contains a 3D representation of visual motion.

Representation of 3-D surface orientation by velocity and disparity gradient cues in area MT.

Neural coding of the three-dimensional (3-D) orientation of planar surface patches may be an important intermediate step in constructing representations of complex 3-D surface structure. Spatial gradients of binocular disparity, image velocity, and texture provide potent cues to the 3-D orientation (tilt and slant) of planar surfaces. Previous studies have described neurons in both dorsal and ventral stream areas that are selective for surface tilt based on one or more of these gradient cues. However, relatively little is known about whether single neurons provide consistent information about surface orientation from multiple gradient cues. Moreover, it is unclear how neural responses to combinations of surface orientation cues are related to responses to the individual cues. We measured responses of middle temporal (MT) neurons to random dot stimuli that simulated planar surfaces at a variety of tilts and slants. Four cue conditions were tested: disparity, velocity, and texture gradients alone, as well as all three gradient cues combined. Many neurons showed robust tuning for surface tilt based on disparity and velocity gradients, with relatively little selectivity for texture gradients. Some neurons showed consistent tilt preferences for disparity and velocity cues, whereas others showed large discrepancies. Responses to the combined stimulus were generally well described as a weighted linear sum of responses to the individual cues, even when disparity and velocity preferences were discrepant. These findings suggest that area MT contains a rudimentary representation of 3-D surface orientation based on multiple cues, with single neurons implementing a simple cue integration rule.

Contributions of excitation and suppression in shaping spatial frequency selectivity of V1 neurons as revealed by binocular measurements.

Neurons in the early visual cortex are generally highly sensitive to stimuli presented to the two eyes. However, the majority of studies on spatial and temporal aspects of neural responses were based on monocular measurements. To study neurons under more natural, i.e., binocular, conditions, we presented sinusoidal gratings of a variety of spatial frequencies (SF) dichoptically in rapid sequential flashes and analyzed the data using a binocular reverse correlation technique for neurons in cat area 17. The resulting set of data represents a frequency-domain binocular receptive field from which detailed selectivities, both monocular and binocular, could be obtained. Consistent with previous studies, the responses could generally be explained by linear summation of inputs from the two eyes. Suppressive responses were also observed and were delayed typically by 5-15 ms relative to excitatory responses. However, we have found more diverse nature of suppressive responses than those reported previously. The optimal suppressive frequency could be either higher or lower than that of the excitatory responses. The bandwidth of SF tuning of the suppressive responses was usually broader than that of the excitatory responses. Cells with lower optimal SFs for suppression tended to show high optimal SFs and sharp tuning curves. The dynamic shift of optimal SF from low to high SF was accompanied by suppression with earlier onset and higher peak SF or later onset and lower peak SF than excitation. These results suggest that the suppression plays an essential role in generating the temporal dynamics of SF selectivity.

Encoding of three-dimensional surface slant in cat visual areas 17 and 18.

How are surface orientations of three-dimensional objects and scenes represented in the visual system? We have examined an idea that these surface orientations are encoded by neurons with a variety of tilts in their binocular receptive field (RF) structure. To examine whether neurons in the early visual areas are capable of encoding surface orientations, we have recorded from single neurons extracellularly in areas 17 and 18 of the cat using standard electrophysiological methods. Binocular RF structures are obtained using a binocular version of the reverse correlation technique. About 30% of binocularly responsive neurons have RFs with statistically significant tilts from the frontoparallel plane. The degree of tilts is sufficient for representing the range of surface slants found in typical visual environments. For a subset of neurons having significant RF tilts, the degrees of tilt are correlated with the preferred spatial frequency difference between the two eyes, indicating that a modified disparity energy model can account for the selectivity, at least partially. However, not all cases could be explained by this model, suggesting that multiple mechanisms may be responsible. Therefore an alternative hypothesis is also examined, where the tilt is generated by pooling of multiple disparity detectors whose preferred disparities progressively shift over space. Although there is evidence for extensive spatial pooling, this hypothesis was not satisfactory either, in that the neurons with extensive pooling tended to prefer an untilted surface. Our results suggest that encoding of surface orientations may begin with the binocular neurons in the early visual cortex.