Haidong D. Lu

Functional organization for color and orientation in macaque V4

Visual area V4 in the macaque monkey is a cortical area that is strongly involved in color and shape perception. However, fundamental questions about V4 are still debated. V4 was initially characterized as a color-processing area, but subsequent studies revealed that it contains a diverse complement of cells, including those with preference for color, orientation, disparity and higher-order feature preferences. This has led to disputes and uncertainty about the role of V4 in vision. Using intrinsic signal optical imaging methods in awake, behaving monkeys, we found that different feature preferences are functionally organized in V4. Optical images revealed that regions with preferential response to color were largely separate from orientation-selective regions. Our results help to resolve long-standing controversies regarding functional diversity and retinotopy in V4 and indicate the presence of spatially biased distribution of featural representation in V4 in the ventral visual pathway.

A map for horizontal disparity in monkey V2.

The perception of visual depth is determined by integration of spatial disparities of inputs from the two eyes. Single cells in visual cortex of monkeys are known to respond to specific binocular disparities; however, little is known about their functional organization. We now show, using intrinsic signal optical imaging and single-unit physiology, that, in the thick stripe compartments of the second visual area (V2), there is a clustered organization of Near cells and Far cells, and moreover, there are topographic maps for Near to Far disparities within V2. Our findings suggest that maps for visual disparity are calculated in V2, and demonstrate parallels in functional organization between the thin, pale, and thick stripes of V2.

A Motion Direction Map in Macaque V2

In mammals, the perception of motion starts with direction-selective neurons in the visual cortex. Despite numerous studies in monkey primary and second visual cortex (V1 and V2), there has been no evidence of direction maps in these areas. In the present study, we used optical imaging methods to study the organization of motion response in macaque V1 and V2. In contrast to the findings in other mammals (e.g., cats and ferrets), we found no direction maps in macaque V1. Robust direction maps, however, were found in V2 thick/pale stripes and avoided thin stripes. In many cases direction maps were located within thick stripes and exhibited pinwheel or linear organizations. The presence of motion maps in V2 points to a newfound prominence of V2 in motion processing, for contributing to motion perception in the dorsal pathway and/or for motion cue-dependent form perception in the ventral pathway.

The Organization of Orientation-Selective, Luminance-Change and Binocular- Preference Domains in the Second (V2) and Third (V3) Visual Areas of New World Owl Monkeys as Revealed by Intrinsic Signal Optical Imaging

Optical imaging was used to map patterns of visually evoked activation in the second (V2) and third (V3) visual areas of owl monkeys. Modular patterns of activation were produced in response to stimulation with oriented gratings, binocular versus monocular stimulation, and stimuli containing wide-field luminance changes. In V2, luminance-change domains tended to lie between domains selective for orientation. Regions preferentially activated by binocular stimulation co-registered with orientation-selective domains. Co-alignment of images with cytochrome oxidase (CO)-processed sections revealed functional correlates of 2 types of CO-dense regions in V2. Orientation-responsive domains and binocular domains were correlated with the locations of CO-thick stripes, and luminance-change domains were correlated with the locations of CO-thin stripes. In V3, orientation preference, luminance-change, and binocular preference domains were observed, but were more irregularly arranged than those in V2. Our data suggest that in owl monkey V2, consistent with that in macaque monkeys, modules for processing contours and binocularity exist in one type of compartment and that modules related to processing-surface features exist within a separate type of compartment.

Intrinsic-signal optical imaging reveals cryptic ocular dominance columns in primary visual cortex of New World owl monkeys

A significant concept in neuroscience is that sensory areas of the neocortex have evolved the remarkable ability to represent a number of stimulus features within the confines of a global map of the sensory periphery. Modularity, the term often used to describe the inhomogeneous nature of the neocortex, is without a doubt an important organizational principle of early sensory areas, such as the primary visual cortex (V1). Ocular dominance columns, one type of module in V1, are found in many primate species as well as in carnivores. Yet, their variable presence in some New World monkey species and complete absence in other species has been enigmatic. Here, we demonstrate that optical imaging reveals the presence of ocular dominance columns in the superficial layers of V1 of owl monkeys (Aotus trivirgatus), even though the geniculate inputs related to each eye are highly overlapping in layer 4. The ocular dominance columns in owl monkeys revealed by optical imaging are circular in appearance. The distance between left eye centers and right eye centers is approximately 650 μm. We find no relationship between ocular dominance centers and other modular organizational features such as orientation pinwheels or the centers of the cytochrome oxidase blobs. These results are significant because they suggest that functional columns may exist in the absence of obvious differences in the distributions of activating inputs and ocular dominance columns may be more widely distributed across mammalian taxa than commonly suggested.

Rivalry-Like Neural Activity in Primary Visual Cortex in Anesthetized Monkeys

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. SIGNIFICANCE STATEMENT When visual input is ambiguous, for example, in viewing bistable images, human subjects normally perceive one of the interpretations at a particular moment. Previous studies have shown that both low-level visual processing and high-level attention contribute to the establishment of the final visual perception. However, it is not clear whether attention is indispensable in such a process. Here we show that rivalry-like neural activity persisted in monkey V1 when the monkeys were anesthetized and viewed binocularly incongruent stimuli. Such activity has many key features similar to those observed in conscious human subjects. These findings indicate that low-level visual processes play a critical role in solving visual ambiguity such as binocular rivalry.

Orientation and Direction-of-Motion Response in the Middle Temporal Visual Area (MT) of New World Owl Monkeys as Revealed by Intrinsic-Signal Optical Imaging.

Intrinsic-signal optical imaging was used to evaluate relationships of domains of neurons in middle temporal visual area (MT) selective for stimulus orientation and direction-of-motion. Maps of activation were elicited in MT of owl monkeys by gratings drifting back-and-forth, flashed stationary gratings and unidirectionally drifting fields of random dots. Drifting gratings, typically used to reveal orientation preference domains, contain a motion component that may be represented in MT. Consequently, this stimulus could activate groups of cells responsive to the motion of the grating, its orientation or a combination of both. Domains elicited from either moving or static gratings were remarkably similar, indicating that these groups of cells are responding to orientation, although they may also encode information about motion. To assess the relationship between domains defined by drifting oriented gratings and those responsive to direction-of-motion, the response to drifting fields of random dots was measured within domains defined from thresholded maps of activation elicited by the drifting gratings. The optical response elicited by drifting fields of random dots was maximal in a direction orthogonal to the map of orientation preference. Thus, neurons in domains selective for stimulus orientation are also selective for motion orthogonal to the preferred stimulus orientation.

A rapid topographic mapping and eye alignment method using optical imaging in Macaque visual cortex

In optical imaging experiments, it is often advantageous to map the field of view and to converge the eyes without electrophysiological recording. This occurs when limited space precludes placement of an electrode or in chronic optical chambers in which one may not want to introduce an electrode each session or for determining eye position in studies of ocular disparity response in visual cortex of anesthetized animals. For these purposes, we have developed a spot imaging method that can be conducted rapidly and repeatedly throughout an experiment. Using small 0.2 degrees -0.5 degrees spots, the extent of the imaged field of view is mapped by imaging cortical response to single spots, placed at different positions (0.2 degrees steps) in either the horizontal or vertical axes. By shifting the relative positions of two spots, one presented to each eye, eye convergence can be assessed to within 0.1 degrees resolution. Once appropriate eye alignment is determined, stimuli for further optical imaging procedures (e.g. imaging random dot stimuli for study of disparity responses) can then be confidently placed. This procedure can be quickly repeated throughout the experiment to ensure maintained eye alignment.

Quantitative inference of population response properties across eccentricity from motion-induced maps in macaque V1

Interpreting population responses in the primary visual cortex (V1) remains a challenge especially with the advent of techniques measuring activations of large cortical areas simultaneously with high precision. For successful interpretation, a quantitatively precise model prediction is of great importance. In this study, we investigate how accurate a spatiotemporal filter (STF) model predicts average response profiles to coherently drifting random dot motion obtained by optical imaging of intrinsic signals in V1 of anesthetized macaques. We establish that orientation difference maps, obtained by subtracting orthogonal axis-of-motion, invert with increasing drift speeds, consistent with the motion streak effect. Consistent with perception, the speed at which the map inverts (the critical speed) depends on cortical eccentricity and systematically increases from foveal to parafoveal. We report that critical speeds and response maps to drifting motion are excellently reproduced by the STF model. Our study thus suggests that the STF model is quantitatively accurate enough to be used as a first model of choice for interpreting responses obtained with intrinsic imaging methods in V1. We show further that this good quantitative correspondence opens the possibility to infer otherwise not easily accessible population receptive field properties from responses to complex stimuli, such as drifting random dot motions.

Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2).

Significance Using a computational method to analyze neuronal responses evoked by natural scene stimuli, we performed a comprehensive identification of secondary visual cortex (V2) neuronal receptive fields (RFs) and found several novel spatial structures of RFs. This approach imposes no assumption about the selectivity of the neurons, thus allowing a more objective search of RFs. Furthermore, by combining single-unit recording with optical imaging of intrinsic signals, we examined the spatial distribution of V2 neurons exhibiting different RFs, with respect to the V2 stripes defined previously by cytochrome oxidase staining. The identified V2 RFs could be explained by convergence of V1 neurons with well-known primary visual cortex RFs. This study illustrates that computational approach is useful for comprehensive RF identification in higher visual cortices. Visual processing depends critically on the receptive field (RF) properties of visual neurons. However, comprehensive characterization of RFs beyond the primary visual cortex (V1) remains a challenge. Here we report fine RF structures in secondary visual cortex (V2) of awake macaque monkeys, identified through a projection pursuit regression analysis of neuronal responses to natural images. We found that V2 RFs could be broadly classified as V1-like (typical Gabor-shaped subunits), ultralong (subunits with high aspect ratios), or complex-shaped (subunits with multiple oriented components). Furthermore, single-unit recordings from functional domains identified by intrinsic optical imaging showed that neurons with ultralong RFs were primarily localized within pale stripes, whereas neurons with complex-shaped RFs were more concentrated in thin stripes. Thus, by combining single-unit recording with optical imaging and a computational approach, we identified RF subunits underlying spatial feature selectivity of V2 neurons and demonstrated the functional organization of these RF properties.