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.

Sanada, Takahisa M. and Izumi Ohzawa. Encoding of threedimensional surface slant in cat visual areas 17 and 18. J Neurophysiol 95: 2768 -2786, 2006. First published January 4, 2006 doi:10.1152/jn.00955.2005. How are surface orientations of threedimensional 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. I N T R O D U C T I O NOne of the fundamental roles of the visual system is to reconstruct a three-dimensional (3D) model of the external world from a pair of two-dimensional images on the two retinae. Horizontal displacement of the eyes causes small differences between the retinal images. This difference of the retinal images is called binocular disparity and stereopsis is the process of determining depth from binocular disparity. Visual information processing for stereopsis begins in the primary visual cortex and neurons found in this area are known to encode binocular disparities of stimuli for a small area of visual field (Barlow et al. 1967;Ferster 1981; Wiesel 1962, 1968;LeVay and Voigt 1988;Nikara et al. 1968; Ohzawa and Freeman 1986a,b;Ohzawa et al. 1990Ohzawa et al. , 1996Ohzawa et al. , 1997.How does the processing of stereoscopic information proceed once binocular disparity for small localized areas is available? Is a possible next stage of processing that of detecting the rate of change of binocular disparity, i.e., detecting 3D orientations of surfaces in depth? Some recent studies have examined these possibilities and report that a sub...

Sanada TM, Nguyenkim JD, DeAngelis GC. Representation of 3-D surface orientation by velocity and disparity gradient cues in area MT. J Neurophysiol 107: 2109 -2122, 2012. First published January 4, 2012; doi:10.1152/jn.00578.2011.-Neural coding of the threedimensional (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. depth; slant; surface; tilt; visual cortex; middle temporal area THE VISUAL SYSTEM RECONSTRUCTS three-dimensional (3-D) scene structure from images projected onto the two retinas. Many cues, including binocular disparity, relative motion, texture, shading, and perspective, are used to perceive 3-D structure. Most complex surfaces can be approximated by combinations of locally planar surfaces. Thus understanding how planar surfaces are coded in visual cortex may help reveal how complex surface representations are constructed. The 3-D orientation of a plane (tilt and slant) can be specified by gradients of binocular disparity, motion (velocity), or texture. Human perception of 3-D surface orientation from these cues has been well studied, and the findings are often well explained by Bayesian models (Girshick and Banks 2009;Hillis et al. 2004;Jacobs 1999;Knill 2007;Knill and Saunders 2003).Physiological studies in macaques have identified neurons that signal the 3-D orientation of planar surfaces. In the ventral stream, 3-D orientation tuning has been reported in area V4 for disparity gradients (Hegde and Van Ess...

Ninomiya T, Sanada TM, Ohzawa I. Contributions of excitation and suppression in shaping spatial frequency selectivity of V1 neurons as revealed by binocular measurements. J Neurophysiol 107: 2220 -2231, 2012. First published January 11, 2012 doi:10.1152/jn.00832.2010Neurons 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 frequencydomain 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.frequency-domain binocular receptive field; cat area 17; reverse correlation VISUAL INFORMATION IS SEPARATELY acquired from two retinae and is first integrated in the early visual cortex. Since Wiesel (1959, 1962) showed that many of the neurons in the early visual cortex could be activated by inputs from either eye, the nature of binocular information processing has been one of the major interests in this stage (Anzai et al. 1999a,b; Bishop et al. 1971;Cumming and DeAngelis 2001; Ohzawa and Freeman 1986a,b;Ohzawa et al. 1990Ohzawa et al. , 1996Ohzawa et al. , 1997Pettigrew et al. 1968).Previous studies performing binocular measurement have mainly been focused on its characteristics in the space domain because the response properties of neurons in the early visual cortex are generally well-described in this domain. However, neurons in this stage exhibit high selectivity for the spatial frequency (SF;Campbell et al. 1969;De Valois et al. 1982;Maffei and Fiorentini 1973), and therefore the SF domain is also useful for capturing the feature of their responses. Many previous studies have revealed the properties of monocular responses in the SF domain Jones...

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.