Daniel J. Felleman

Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex

This report provides an overview of the functional organization of cortex immediately anterior to area V2 in extrastriate visual cortex of the macaque monkey. Contrary to previous suggestions that a single area, V3, lies anterior to V2, we have obtained evidence that this strip of cortex includes two separate areas, V3 and the ventral posterior area, VP. The evidence supporting this conclusion is based on dorso-ventral asymmetries in cortico-cortical connections, myeloarchitecture, and single-unit physiological properties relating to the processing of information about color and motion.

Indeterminate Organization of the Visual System

The classic view of how the brain areas that control vision are connected is a complicated wiring diagram devised by manual sorting on the basis of existing anatomical data [D. J. Felleman and D. C. Van Essen, Cereb. Cortex 1, 1 (1991)]. Now, in this issues Enhanced Perspective, Hilgetag and co-workers have used a computer algorithm to test whether there is a better way to organize the connections. They find that the brain is surprisingly indeterminate, and that no single hierarchy can satisfactorily represent the order implied by the anatomical data. A more detailed explanation of their analysis and a list of predictions derived from their hierarchies that will be particularly informative to test experimentally can be found on the home page of the authors.

Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex

The cortical connections of visual area 3 (V3) and the ventral posterior area (VP) in the macaque monkey were studied by using combinations of retrograde and anterograde tracers. Tracer injections were made into V3 or VP following electrophysiological recording in and near the target area. The pattern of ipsilateral cortical connections was analyzed in relation to the pattern of interhemispheric connections identified after transection of the corpus callosum. Both V3 and VP have major connections with areas V2, V3A, posterior intraparietal area (PIP), V4, middle temporal area (MT), medial superior temporal area (dorsal) (MSTd), and ventral intraparietal area (VIP). Their connections differ in several respects. Specifically, V3 has connections with areas V1 and V4 transitional area (V4t) that are absent for VP; VP has connections with areas ventral occipitotemporal area (VOT), dorsal prelunate area (DP), and visually responsive portion of temporal visual area F (VTF) that are absent or occur only rarely for V3. The laminar pattern of labeled terminals and retrogradely labeled cell bodies allowed assessment of the hierarchical relationships between areas V3 and VP and their various targets. Areas V1 and V2 are at a lower hierarchical level than V3 and VP; all of the remaining areas are at a higher level. V3 receives major inputs from layer 4B of V1, suggesting an association with the magnocellular‐dominated processing stream and a role in routing magnocellular‐dominated information along pathways leading to both parietal and temporal lobes. The convergence and divergence of pathways involving V3 and VP underscores the distributed nature of hierarchical processing in the visual system. J. Comp. Neurol. 379:21‐47, 1997.

Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of cebus monkeys

The somatotopic organization of postcentral parietal cortex was determined with microelectrode mapping methods in a New World monkey, Cebus albifrons. As in previous studies in macaque, squirrel and owl monkeys, two separate representations of the body surface were found in regions corresponding to the architectonic fields 3b and 1. The two representations were roughly mirror-images of each other, with receptive field locations matched for recording sites along the common border. As in other monkeys, the glabrous digit tips of the hand and foot pointed rostrally in the Area 3b representation and caudally in the Area 1 representation. Both representations proceeded in parallel from the tail on the medial wall of the cerebral hemisphere to the teeth and tongue in lateral cortex along the Sylvian fissure. Compared with the other monkeys, the tail of the cebus monkey, which is prehensile, was represented in a very large region of cortex in Areas 3b and 1. Like its close relative, the squirrel monkey, the representation of the trunk and parts of the limbs were reversed in orientation in both Area 3b and Area 1 in cebus monkeys as compared to owl and macaque monkeys. The reversals of organization for some but not all parts of the representations in cebus and squirrel monkeys suggest that one line of New World monkeys acquired a unique but functionally adequate pattern of somatotopic organization for the two adjoining fields.

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. NEUROSCIENTIST 13(5):416—421, 2007. DOI: 10.1177/1073858407305201

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.

Probing the Primate Visual Cortex: Pathways and Perspectives

Most primates are highly visual creatures, capable of a wide variety of difficult tasks that must be carried out in a complex visual environment. It is therefore hardly surprising that a very large expanse of cerebral cortex is devoted to analyzing and interpreting the relatively raw messages transmitted from the retina. Over the past three decades, much progress has been made in elucidating the organization and function of visual cortex. In this chapter we briefly review recent progress in understanding several aspects of visual processing in the macaque monkey, as revealed by both anatomical and physiological studies. The first topic concerns the nature of information flow through the visual cortex as revealed by analysis of the numerous pathways that interconnect different visual areas. The guiding hypothesis is that the cortex is arranged as a distributed hierarchical system, in which there are many distinct levels of analysis. The second topic concerns parallel processing streams and their relationship to the M and P pathways established within the retina. The third topic deals with the functional significance of the feedback pathways that form a prominent characteristic of the cortical hierarchy. The function of feedback pathways in sensory processing has been an intriguing but elusive issue. There are probably many such functions, and here we emphasize their possible role in modulating neural responses according to the broader context of the visual environment.

The popout in some conjunction searches is due to perceptual grouping.

The target in a visual search task usually pops out if it can be distinguished from its background on the basis of only one visual feature but not if the target represents a conjunction of two or more features. However, several recent reports suggest that in certain cases, search targets defined by a conjunction of two features also pop out. We have reinvestigated three pairs of such features to determine whether the popout in these cases can be attributed to perceptual grouping. We find that that in all three cases, popout no longer occurs when perceptual grouping is degraded, suggesting that the popout is the result of perceptual grouping and not of novel mechanism/s of conjunction search.

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.

Radiation-induced micrencephaly in guinea pigs

The effect of X rays on brain weight of guinea pig pups at birth was studied in 21-day-old embryos exposed in utero to doses of 75 and 100 mGy. When compared to controls and when corrected for body weight, gestation time, litter size, sex, and examiner differences, the brains of irradiated pups weighed approximately 46 mg less than those of controls (P < 0.001) for the 75-mGy group and about 55 mg less for the 100-mGy group. Brains of females weighed 51 mg less than those of males of the same body weight. Dam weight and caging conditions had no observed effect on brain weight.