Hue and Orientation Pinwheels in Macaque Area V4.

Area V4 is an intermediate-level area of the macaque visual cortical hierarchy that serves key functions in cortical visual processing by integrating feedforward inputs from multiple functional compartments in lower areas such as V1 and V2 and providing feedforward inputs to many areas in inferotemporal, parietal, and prefrontal cortex. While many previous imaging studies of V4 have analyzed the differential responses to color, orientation, disparity, and motion stimuli, many details of the spatial organization of significant hue and orientation tuning have not been fully described. The Support Vector Machine (SVM) decoding of intrinsic cortical single-condition responses was used to generate high-resolution maps of hue and orientation tuning in V4. Like V1 and V2, V4 contains maps of iso-orientation domains organized around pinwheel centers. V4 contains maps of hue that consist of iso-hue domains surrounding pinwheel centers. The circular organization of these pinwheels more closely represents the perception of hue than is observed in antecedent cortical areas. Domains significantly tuned for hue occupy roughly four times the surface of the orientation domains, are largely segregated from each other, and overlap by roughly 5%. The spatial organization of hue and orientation pinwheels and their domains are largely consistent with the largely segregated inputs arising from the thin and interstripe compartments of V2. This modular segregation of processing suggests that further integration of color and shape must occur in inferotemporal cortical areas that receive direct projections from V4.

Visual Interhemispheric and Striate-Extrastriate Cortical Connections in the Rabbit: A Multiple Tracer Study.

Previous studies in rabbits identified an array of extrastriate cortical areas anatomically connected with V1 but did not describe their internal topography. To address this issue, we injected multiple anatomical tracers into different regions in V1 of the same animal and analyzed the topography of resulting extrastriate labeled fields with reference to the patterns of callosal connections and myeloarchitecture revealed in tangential sections of the flattened cortex. Our results extend previous studies and provide further evidence that rabbit extrastriate areas resemble the visual areas in rats and mice not only in their general location with respect to V1 but also in their internal topography. Moreover, extrastriate areas in the rabbit maintain a constant relationship with myeloarchitectonic borders and features of the callosal pattern. These findings highlight the rabbit as an alternative model to rats and mice for advancing our understanding of cortical visual processing in mammals, especially for projects benefiting from a larger brain.

A wireless transmission neural interface system for unconstrained non-human primates.

OBJECTIVE: Studying the brain in large animal models in a restrained laboratory rig severely limits our capacity to examine brain circuits in experimental and clinical applications. APPROACH: To overcome these limitations, we developed a high-fidelity 96-channel wireless system to record extracellular spikes and local field potentials from the neocortex. A removable, external case of the wireless device is attached to a titanium pedestal placed in the animal skull. Broadband neural signals are amplified, multiplexed, and continuously transmitted as TCP/IP data at a sustained rate of 24 Mbps. A Xilinx Spartan 6 FPGA assembles the digital signals into serial data frames for transmission at 20 kHz though an 802.11n wireless data link on a frequency-shift key-modulated signal at 5.7-5.8 GHz to a receiver up to 10 m away. The system is powered by two CR123A, 3 V batteries for 2 h of operation. MAIN RESULTS: We implanted a multi-electrode array in visual area V4 of one anesthetized monkey (Macaca fascicularis) and in the dorsolateral prefrontal cortex (dlPFC) of a freely moving monkey (Macaca mulatta). The implanted recording arrays were electrically stable and delivered broadband neural data over a year of testing. For the first time, we compared dlPFC neuronal responses to the same set of stimuli (food reward) in restrained and freely moving conditions. Although we did not find differences in neuronal responses as a function of reward type in the restrained and unrestrained conditions, there were significant differences in correlated activity. This demonstrates that measuring neural responses in freely moving animals can capture phenomena that are absent in the traditional head-fixed paradigm. SIGNIFICANCE: We implemented a wireless neural interface for multi-electrode recordings in freely moving non-human primates, which can potentially move systems neuroscience to a new direction by allowing one to record neural signals while animals interact with their environment.

The Representation of Orientation in Macaque V2: Four Stripes Not Three.

Area V2 of macaque monkeys is traditionally thought to consist of 3 distinct functional compartments with characteristic cortical connections and functional properties. Orientation selectivity is one property that has frequently been used to distinguish V2 stripes, however, this receptive field property has been found in a high percentage of neurons across V2 compartments. Using quantitative intrinsic cortical imaging, we derived maps of preferred orientation, orientation selectivity, and orientation gradient in thin stripes, thick stripes, and interstripes in area V2. Orientation-selective responses were found in each V2 stripe, but the magnitude and organization of orientation selectivity differed significantly from stripe to stripe. Remarkably, the 2 pale stripes flanking each cytochrome oxidase dense stripe differed significantly in their representation of orientation resulting in their distinction as type-I and type-II interstripes. V2 orientation maps are characterized by clockwise and anticlockwise "orientation pinwheels", but unlike V1, they are not homogeneously distributed across V2. Furthermore, V2 stripes contain large-scale sequences of preferred orientation. These analyses demonstrate that V2 consists of 4 distinct functional compartments; thick stripes and type-II interstripes, which are strongly orientation selective and thin stripes and type-I interstripes, which are significantly less selective for orientation and exhibit larger orientation gradient magnitudes.

Mutual information of local field potentials distinguishes area-V2 stripe compartments.

PURPOSE: Determining how information is represented by populations of neurons in different cortical areas is critical to our understanding of the brain mechanisms of visual perception. Recently, information-theoretical approaches have been applied to the analysis of spike trains of multiple neurons. However, other neurophysiological signals, such as local field potentials (LFPs), offer a different source of information worthy of investigating in this way. In this study, we investigate how the modular organization of area V2 of macaque monkeys impacts the information represented in LFPs. MATERIALS AND METHODS: LFPs were recorded from a 32-channel microelectrode array implanted in area V2 of an anesthetized macaque monkey. The electrode positions were recovered in histological tissue stained for cytochrome oxidase (CO) to reveal the modular organization of V2. Visual stimuli consisted of a variety of moving gratings that differed in orientation, direction, spatial frequency, and chromatic content. RESULTS: LFPs were separated into different frequency bands for analysis of mutual information as a function of stimulus type and CO-stripe location. High-γ-band LFPs revealed the highest information content across the electrode array. The distributions of total mutual information as well as mutual information due to correlations varied greatly by CO stripe. This analysis indicates that local correlations within each CO stripe generally reduce mutual information, whereas correlations between stripes greatly increase mutual information. CONCLUSION: The decomposition mutual information based on the power of different frequency bands of LFPs provides new insight into the impact of modular architecture on population coding in area V2. Unlike other cortical areas, such as V1, where mutual information based on LFP correlations is largely determined by cortical separation, mutual information in V2 is also fundamentally determined by the CO-stripe architecture.

Organization of hue selectivity in macaque V2 thin stripes.

V2 has long been recognized to contain functionally distinguishable compartments that are correlated with the stripelike pattern of cytochrome oxidase activity. Early electrophysiological studies suggested that color, direction/disparity, and orientation selectivity were largely segregated in the thin, thick, and interstripes, respectively. Subsequent studies revealed a greater degree of homogeneity in the distribution of response properties across stripes, yet color-selective cells were still found to be most prevalent in the thin stripes. Optical recording studies have demonstrated that thin stripes contain both color-preferring and luminance-preferring modules. These thin stripe color-preferring modules contain spatially organized hue maps, whereas the luminance-preferring modules contain spatially organized luminance-change maps. In this study, the neuronal basis of these hue maps was determined by characterizing the selectivity of neurons for isoluminant hues in multiple penetrations within previously characterized V2 thin stripe hue maps. The results indicate that neurons within the superficial layers of V2 thin stripe hue maps are organized into columns whose aggregated hue selectivity is closely related to the hue selectivity of the optically defined hue maps. These data suggest that thin stripes contain hue maps not simply because of their moderate percentage of hue-selective neurons, but because of the columnar and tangential organization of hue selectivity.

Reappraising the functional implications of the primate visual anatomical hierarchy.

The primate visual system has been shown to be organized into an anatomical hierarchy by the application of a few principled criteria. It has been widely assumed that cortical visual processing is also hierarchical, with the anatomical hierarchy providing a defined substrate for clear levels of hierarchical function. A large body of empirical evidence seemed to support this assumption, including the general observations that functional properties of visual neurons grow progressively more complex at progressively higher levels of the anatomical hierarchy. However, a growing body of evidence, including recent direct experimental comparisons of functional properties at two or more levels of the anatomical hierarchy, indicates that visual processing neither is hierarchical nor parallels the anatomical hierarchy. Recent results also indicate that some of the pathways of visual information flow are not hierarchical, so that the anatomical hierarchy cannot be taken as a strict flowchart of visual information either. Thus, while the sustaining strength of the notion of hierarchical processing may be that it is rather simple, its fatal flaw is that it is overly simplistic.

V2 thin stripes contain spatially organized representations of achromatic luminance change.

A considerable amount of research over the last decades has focused on the apparent specialization of V2 thin stripes for the processing of color in diurnal primates. However, because V2 thin stripes are functionally heterogeneous in that they consist of largely separate color- and luminance-preferring domains and because the color-preferring domains contain a systematic representation of hue, we hypothesized that they contained functional maps that subserve luminance processing. Here we show, using optical imaging of intrinsic cortical signals and microelectrode recording, that the V2 thin stripe luminance-preferring domains contain spatially segregated modules that encode the direction of relative luminance change. Quantitative analysis of the cortical responses to luminance increments or decrements indicates that these luminance-sensitive modules also encode the magnitude of the luminance change by the magnitude of the evoked cortical response. These results demonstrate an important role of V2 thin stripes in the processing of luminance and thus suggest that thin stripes are involved in the overall processing of the surface properties of objects rather than simply the processing of color.

Projections from primary visual cortex to cytochrome oxidase thin stripes and interstripes of macaque visual area 2.

It has been controversial whether the cytochrome oxidase (CO)-dense blobs in primate primary visual cortex (V1) and CO-dense thin stripes in visual area 2 (V2) are parts of a cortical color-processing stream that is segregated from other functional streams. One of the key pieces of evidence for the segregated color stream is the previous report of specific connections between blobs and thin stripes, which is parallel to the connections between interblobs and interstripes. To study the degree of the segregation between the proposed different streams, in the current study, anatomical tracers were injected into different V2 compartments with the functional guidance of optical imaging. The spatial relationship between each labeled cell and the CO blobs in V1 were analyzed quantitatively. After tracer injections in the color-preferring modules in CO thin stripes, equal amounts of labeled cells were found in the blobs and interblobs. However, the density of the labeled cells was more than twice as high in the blobs as that in the interblobs, and most of the clusters of labeled cells partially overlapped with the blobs. Tracer injections in the interstripes labeled cells predominantly in the interblobs. Our results suggest that both the blobs and interblobs project to the thin stripes and call into question the proposition that different CO compartments in V1 and V2 are connected in parallel to form highly segregated functional streams.

How selective are V1 cells for pop-out stimuli?

Many neurons in visual area V1 respond better to a pop-out stimulus, such as a single vertical bar among many horizontal bars, than to a homogeneous stimulus, such as a stimulus with all vertical bars. Many studies have suggested such cells represent neural correlates of pop-out, or more generally figure-ground segregation. However, preference for pop-out stimuli over homogeneous stimuli could also arise from a nonspecific selectivity for feature discontinuities between the target and the background, without any specificity for pop-out per se. To distinguish between these two confounding scenarios, we compared the responses of V1 neurons to pop-out stimuli with the responses to "conjunction-target" stimuli, which have more complex feature discontinuities between the target and the surround, as in a stimulus with a blue vertical bar among blue horizontal bars and yellow vertical bars. The target in conjunction-target stimuli does not pop out, which we psychophysically verified. V1 cells in general responded similarly to pop-out and conjunction-target stimuli, and only a small minority of cells (approximately 2% by one measure) distinguished the pop-out and conjunction-target stimuli from each other and from homogeneous stimuli. Nevertheless, the responses of approximately 50% of the cells were significantly modulated across all center-surround stimuli, indicating that V1 cells can convey information about the feature discontinuities between the center and the surround as part of a network of neurons, although individual cells by themselves fail to explicitly represent pop-out. In light of our results, unambiguous pop-out selectivity at the level of individual cells remains to be demonstrated in V1 or elsewhere in the visual cortex.

A spatially organized representation of colour in macaque cortical area V2.

Neurons responding selectively to different colours have been found in various cortical areas in macaque monkeys; however, little is known about whether and how the representation of colour is spatially organized in any cortical area. Cortical area V2 contains modules that respond preferentially to chromatic modulation, which are located in thin cytochrome oxidase stripes. Here we show that within and beyond these modules, gratings of different colours produce activations that peak at different locations. Optical recording of intrinsic signals revealed that the peak regions of the responses to different colours were spatially organized in the same order as colour stimuli are arranged in the DIN (German standard colour chart) colour system. Nearby regions represented colours of a similar hue. We found that the set of colour-specific regions formed 0.07-0.32-mm-wide and approximately 1.3-mm long bands that varied in shape from linear to nearly circular. Our finding suggests that thin stripes in V2 contain functional maps where the colour of a stimulus is represented by the location of its response activation peak.