Mesoscale functional connectivity in macaque visual areas.

Studies of resting-state functional connectivity (rsFC) have provided rich insights into the structures and functions of the human brain. However, most rsFC studies have focused on large-scale brain connectivity. To explore rsFC at a finer scale, we used intrinsic signal optical imaging to image the ongoing activity of the anesthetized macaque visual cortex. Differential signals from functional domains were used to quantify network-specific fluctuations. In 30-60 min resting-state imaging, a series of coherent activation patterns were observed in all three visual areas we examined (V1, V2, and V4). These patterns matched the known functional maps (ocular dominance, orientation, color) obtained in visual stimulation conditions. These functional connectivity (FC) networks fluctuated independently over time and exhibited similar temporal characteristics. Coherent fluctuations, however, were observed from orientation FC networks in different areas and even across two hemispheres. Thus, FC in the macaque visual cortex was fully mapped both on a fine scale and over a long range. Hemodynamic signals can be used to explore mesoscale rsFC in a submillimeter resolution.

Orientation anisotropies in macaque visual areas.

In mammals, a larger number of neurons in V1 are devoted to cardinal (horizontal and vertical) orientations than to oblique orientations. However, electrophysiological results from the macaque monkey visual cortex are controversial. Both isotropic and anisotropic orientation distributions have been reported. It is also unclear whether different visual areas along the visual hierarchy have different orientation anisotropies. We analyzed orientation maps in a large set of intrinsic signal optical imaging data and found that both V1 and V4 exhibited significant orientation anisotropies. However, their overrepresented orientations were very different: in V1, both cardinal and radial orientations were overrepresented, while in V4, only cardinal bias was presented. These findings suggest that different cortical areas have evolved to emphasize different features that are suitable for their functional purposes, a factor that needs to be considered when efforts are made to explain the relationships between the visual environment and the cortical representation and between the cortical representation and visual perception.

Function-specific projections from V2 to V4 in macaques.

Previous studies have revealed modular projections from area V2 to area V4 in macaques. Specifically, V2 neurons in cytochrome oxidase (CO)-rich thin and CO-sparse pale stripes project to distinct regions in V4. However, how these modular projections relate to the functional subcompartments of V4 remains unclear. In this study, we injected retrograde fluorescent tracers into V4 regions with different functional properties (color, orientation, and direction) that were identified with intrinsic signal optical imaging (ISOI). We examined the labeled neurons in area V2 and their locations with respect to the CO patterns. Covariation was observed between the functional properties of the V4 injection sites and the numbers of labeled neurons in particular CO stripes. This covariation indicates that the color domains in V4 mainly received inputs from thin stripes in V2, whereas V4 orientation domains received inputs from pale stripes. Although motion-sensitive domains are present in both V2 and V4, our results did not reveal a functional specific feedforward projection between them. These results confirmed previous findings of modular projections from V2 to V4 and provided functional specificity for these anatomical projections. Together, these findings indicate that color and form remain separate in ventral mid-level visual processing.

Processing of motion boundary orientation in macaque V2.

Human and nonhuman primates are good at identifying an object based on its motion, a task that is believed to be carried out by the ventral visual pathway. However, the neural mechanisms underlying such ability remains unclear. We trained macaque monkeys to do orientation discrimination for motion boundaries (MBs) and recorded neuronal response in area V2 with microelectrode arrays. We found 10.9% of V2 neurons exhibited robust orientation selectivity to MBs, and their responses correlated with monkeys' orientation-discrimination performances. Furthermore, the responses of V2 direction-selective neurons recorded at the same time showed correlated activity with MB neurons for particular MB stimuli, suggesting that these motion-sensitive neurons made specific functional contributions to MB discrimination tasks. Our findings support the view that V2 plays a critical role in MB analysis and may achieve this through a neural circuit within area V2.

Curvature-processing domains in primate V4.

Neurons in primate V4 exhibit various types of selectivity for contour shapes, including curves, angles, and simple shapes. How are these neurons organized in V4 remains unclear. Using intrinsic signal optical imaging and two-photon calcium imaging, we observed submillimeter functional domains in V4 that contained neurons preferring curved contours over rectilinear ones. These curvature domains had similar sizes and response amplitudes as orientation domains but tended to separate from these regions. Within the curvature domains, neurons that preferred circles or curve orientations clustered further into finer scale subdomains. Nevertheless, individual neurons also had a wide range of contour selectivity, and neighboring neurons exhibited a substantial diversity in shape tuning besides their common shape preferences. In strong contrast to V4, V1 and V2 did not have such contour-shape-related domains. These findings highlight the importance and complexity of curvature processing in visual object recognition and the key functional role of V4 in this process.

Visual Motion Processing in Macaque V2.

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.

Cloning and characterization of a novel chondroitin sulfate/dermatan sulfate 4-O-endosulfatase from a marine bacterium.

Sulfatases are potentially useful tools for structure-function studies of glycosaminoglycans (GAGs). To date, various GAG exosulfatases have been identified in eukaryotes and prokaryotes. However, endosulfatases that act on GAGs have rarely been reported. Recently, a novel HA and CS lyase (HCLase) was identified for the first time from a marine bacterium (Han, W., Wang, W., Zhao, M., Sugahara, K., and Li, F. (2014) J. Biol. Chem. 289, 27886-27898). In this study, a putative sulfatase gene, closely linked to the hclase gene in the genome, was recombinantly expressed and characterized in detail. The recombinant protein showed a specific N-acetylgalactosamine-4-O-sulfatase activity that removes 4-O-sulfate from both disaccharides and polysaccharides of chondroitin sulfate (CS)/dermatan sulfate (DS), suggesting that this sulfatase represents a novel endosulfatase. The novel endosulfatase exhibited maximal reaction rate in a phosphate buffer (pH 8.0) at 30 °C and effectively removed 17-65% of 4-O-sulfates from various CS and DS and thus significantly inhibited the interactions of CS and DS with a positively supercharged fluorescent protein. Moreover, this endosulfatase significantly promoted the digestion of CS by HCLase, suggesting that it enhances the digestion of CS/DS by the bacterium. Therefore, this endosulfatase is a potential tool for use in CS/DS-related studies and applications.