Anna W. Roe

Cross-modal plasticity in cortical development: differentiation and specification of sensory neocortex

Early developmental manipulations can induce sensory afferents of one modality to project to central targets of a different sensory modality. We and other investigators have used such cross-modal plasticity to examine the role of afferent inputs and their patterns of activity in the development of sensory neocortex. We suggest that the afferent rewiring can significantly influence the internal connectivity or microcircuitry of sensory cortex, aspects of which appear to be determined or specified relatively late in development, but that they cannot influence, or influence only to a minor extent, the laminar characteristics and external connectivity patterns of cortex, which appear to be specified earlier.

Toward a Unified Theory of Visual Area V4

Visual area V4 is a midtier cortical area in the ventral visual pathway. It is crucial for visual object recognition and has been a focus of many studies on visual attention. However, there is no unifying view of V4s role in visual processing. Neither is there an understanding of how its role in feature processing interfaces with its role in visual attention. This review captures our current knowledge of V4, largely derived from electrophysiological and imaging studies in the macaque monkey. Based on recent discovery of functionally specific domains in V4, we propose that the unifying function of V4 circuitry is to enable selective extraction of specific functional domain-based networks, whether it be by bottom-up specification of object features or by top-down attentionally driven selection.

A hierarchy of the functional organization for color, form and disparity in primate visual area V2

By combining optical imaging, single unit electrophysiology and cytochrome oxidase (CO) histology, we sought to reveal in greater detail the functional organization within the CO stripes of visual area V2 of primates. To visualize the disparity selective regions of V2, the imaging of binocular interaction was employed. These imaging maps guided single unit penetrations that then revealed a columnar organization for disparity. Our studies also showed a pattern of intermixing between the color and disparity pathways of V2, including the existence of single cells tuned for both color and disparity. While previous studies have suggested that the CO stripes of V2 constitute the fundamental organizational unit within V2, our results show a further level of organization consisting of functionally distinct subcompartments, 0.7-1.5 mm in diameter, within individual stripes. These subcompartments, which are not clearly revealed by CO histochemistry, lie within each of the thin, pale, and thick CO dense stripes in V2 and are specific for aspects of color, orientation and retinal disparity, respectively. The present results favor an architectural view of V2, not unlike that of V1, as a collection of functionally distinct subcompartments or modules situated within each of the V2 stripes. These modules also support the notion that for each cortical area (e.g. V1, V2, V4), there exists a stereotyped cortical module with a geometry that is characteristic for each area. These modules exist as a middle tier in a hierarchy of functional organization within V2.

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.

Pulsed infrared light alters neural activity in rat somatosensory cortex in vivo

Pulsed infrared light has shown promise as an alternative to electrical stimulation in applications where contact free or high spatial precision stimulation is desired. Infrared neural stimulation (INS) is well characterized in the peripheral nervous system; however, to date, research has been limited in the central nervous system. In this study, pulsed infrared light (λ=1.875 μm, pulse width=250 μs, radiant exposure=0.01-0.55 J/cm(2), fiber size=400 μm, repetition rate=50-200 Hz) was used to stimulate the somatosensory cortex of anesthetized rats, and its efficacy was assessed using intrinsic optical imaging and electrophysiology techniques. INS was found to evoke an intrinsic response of similar magnitude to that evoked by tactile stimulation (0.3-0.4% change in intrinsic signal magnitude). A maximum deflection in the intrinsic signal was measured to range from 0.05% to 0.4% in response to INS, and the activated region of cortex measured approximately 2mm in diameter. The intrinsic signal magnitude increased with faster laser repetition rates and increasing radiant exposures. Single unit recordings indicated a statistically significant decrease in neuronal firing that was observed at the onset of INS stimulation (0.5s stimulus) and continued up to 1s after stimulation onset. The pattern of neuronal firing differed from that observed during tactile stimulation, potentially due to a different spatial integration field of the pulsed infrared light compared to tactile stimulation. The results demonstrate that INS can be used safely and effectively to manipulate neuronal firing.

Optical Imaging of SI Topography in Anesthetized and Awake Squirrel Monkeys

Orderly topographic maps in the primary somatosensory cortex (SI) serve as an anchor for our understanding of somatosensory cortical organization. However, this view is mostly based on data collected in the anesthetized animal. Less is known about these topographies in the awake primate. Even less is known about the relative activations of different subdivisions of SI (areas 3a, 3b, 1, and 2). Toward the goal of understanding the functional activation of SI, we conducted intrinsic signal optical imaging of areas 3b and 1 in awake squirrel monkeys. Monkeys were imaged repeatedly for a period of >2 years in awake and anesthetized states in response to vibrotactile and electrocutaneous stimuli presented to individual fingerpads. During this period, we found stable somatotopic maps in both the anesthetized and awake states, consistent with electrophysiologically recorded maps in areas 3b and 1 in the anesthetized state. In the awake animal, signal sizes were larger, but variability was greater, leading to decreased signal-to-noise ratios. Topographic activations were larger (in both area and amplitude) in the awake animal, suggesting either a less precise topography and/or more complex integration. This brings into question the role of a precise topographic map during behavior. In addition, whereas in the anesthetized animal strongest imaging signals were obtained from area 3b, in the awake animal, area 1 activation dominated over that in area 3b. Differences in relative dominance of area 3b versus area 1 suggest that inter-areal interactions in the alert animal differ substantially from that in the anesthetized animal.

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.

High-Resolution Maps of Real and Illusory Tactile Activation in Primary Somatosensory Cortex in Individual Monkeys with Functional Magnetic Resonance Imaging and Optical Imaging

Although blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) has been widely used to explore human brain function, questions remain regarding the ultimate spatial resolution of positive BOLD fMRI, and indeed the extent to which functional maps revealed by positive BOLD correlate spatially with maps obtained with other high-spatial-resolution mapping techniques commonly used in animals, such as optical imaging of intrinsic signal (OIS) and single-unit electrophysiology. Here, we demonstrate that the positive BOLD signal at 9.4T can reveal the fine topography of individual fingerpads in single-condition activation maps in nonhuman primates. These digit maps are similar to maps obtained from the same animal using intrinsic optical imaging. Furthermore, BOLD fMRI reliably resolved submillimeter spatial shifts in activation in area 3b previously identified with OIS (Chen et al., 2003) as neural correlates of the “funneling illusion.” These data demonstrate that at high field, high-spatial-resolution topographic maps can be achieved using the positive BOLD signal, weakening previous notions regarding the spatial specificity of the positive BOLD signal.

Disparity Channels in Early Vision

The past decade has seen a dramatic increase in our knowledge of the neural basis of stereopsis. New cortical areas have been found to represent binocular disparities, new representations of disparity information (e.g., relative disparity signals) have been uncovered, the first topographic maps of disparity have been measured, and the first causal links between neural activity and depth perception have been established. Equally exciting is the finding that training and experience affects how signals are channeled through different brain areas, a flexibility that may be crucial for learning, plasticity, and recovery of function. The collective efforts of several laboratories have established stereo vision as one of the most productive model systems for elucidating the neural basis of perception. Much remains to be learned about how the disparity signals that are initially encoded in primary visual cortex are routed to and processed by extrastriate areas to mediate the diverse capacities of three-dimensional vision that enhance our daily experience of the world.

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.