In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31% of the possible number of pathways if each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somatosensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas V1 and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainities in the reported assignment.

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Distributed Hierarchical Processing in the Primate Cerebral Cortex

Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.

The organization of the human cerebral cortex estimated by intrinsic functional connectivity

We recorded electrical activity from 532 neurons in the rostral part of inferior area 6 (area F5) of two macaque monkeys. Previous data had shown that neurons of this area discharge during goal-directed hand and mouth movements. We describe here the properties of a newly discovered set of F5 neurons ("mirror neurons', n = 92) all of which became active both when the monkey performed a given action and when it observed a similar action performed by the experimenter. Mirror neurons, in order to be visually triggered, required an interaction between the agent of the action and the object of it. The sight of the agent alone or of the object alone (three-dimensional objects, food) were ineffective. Hand and the mouth were by far the most effective agents. The actions most represented among those activating mirror neurons were grasping, manipulating and placing. In most mirror neurons (92%) there was a clear relation between the visual action they responded to and the motor response they coded. In approximately 30% of mirror neurons the congruence was very strict and the effective observed and executed actions corresponded both in terms of general action (e.g. grasping) and in terms of the way in which that action was executed (e.g. precision grip). We conclude by proposing that mirror neurons form a system for matching observation and execution of motor actions. We discuss the possible role of this system in action recognition and, given the proposed homology between F5 and human Brocca's region, we posit that a matching system, similar to that of mirror neurons exists in humans and could be involved in recognition of actions as well as phonetic gestures.

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Action recognition in the premotor cortex

http://www.fulminiesaette.it/_uploads/foto/legame/Rizzolatti1996.pdf

Premotor cortex and the recognition of motor actions.

In area F5 of the monkey premotor cortex there are neurons that discharge both when the monkey performs an action and when he observes a similar action made by another monkey or by the experimenter. We report here some of the properties of these 'mirror' neurons and we propose that their activity 'represents' the observed action. We posit, then, that this motor representation is at the basis of the understanding of motor events. Finally, on the basis of some recent data showing that, in man, the observation of motor actions activate the posterior part of inferior frontal gyrus, we suggest that the development of the lateral verbal communication system in man derives from a more ancient communication system based on recognition of hand and face gestures.

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Research report Premotor cortex and the recognition of motor actions

The anatomy of the cerebellum

The classically conditioned nictitating membrane response (NMR) of the rabbit, a simple form of associative motor learning, is crucially dependent upon the cerebellum. Discrete unilateral lesions of the cerebellar nuclei were made in 20 rabbits. Lesions of the anterior interpositus nucleus (IA) abolished NMR conditioning to light and white noise stimuli on the side of the lesion without affecting unconditional responses. Lesions of the posterior interpositus nucleus, fastigial and dentate nuclei were without effect upon NMR conditioning.

Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei.

The distribution of cortical cells projecting to the pontine nuclei in rats was studied by making large injections of horseradish peroxidase that filled the basilar pons and measuring the density of labelled cells in each cortical area. All retrogradely labelled cells were layer V pyramidal cells. The highest densities of labelled cells were observed in the motor areas. The lowest densities were in temporal association cortex and perirhinal cortex. Visual cortical areas, including the primary visual cortex, provided a major source of pontine projections. The distribution of corticopontine cells within the primary visual cortex was studied in more detail. In all cases the highest density of labelled cells was observed in the region of cortex that represents the nasal visual field. Control injections into brainstem regions adjacent to the pontine nuclei produced a much lower absolute density of retrogradely labelled cortical cells and the distribution of those cells was different from that observed following pontine injections. We conclude that every area of the rat's cerebral cortex projects to the pontine nuclei and that there are consistent variations in the density of the projections both between and within areas.

Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei

Mathematicians, control engineers and information technologists are beginning to take a greater interest in neuroscience. They are perhaps starting to realize that they may be able to learn a few tricks from nature with which to improve their machines. At the same time there is a good chance that neuroscientists will benefit from their input of fresh ideas and techniques with which to attack the problems of understanding neural processing. One area of the brain which seems particularly promising in these respects is the cerebellum.

Role of the cerebellum in visual guidance of movement

The rostral part of the agranular frontal cortex (area 6) can be subdivided on the basis of its cytoarchitecture, enzymatic properties, and connections into two large sectors: a superior region, lying medial to the spur of the arcuate sulcus, and an inferior region, lying lateral to it. In this study we traced the afferent and efferent connections of the inferior region of area 6 by injecting small amounts of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) and fluorescent tracers (fast blue and diamidino yellow) into restricted parts of inferior area 6 and in physiologically determined fields of area 4. There is an ordered topographic pattern of connections between inferior area 6 and area 4. The region near the spur of the arcuate sulcus (hand field) projects to the area 4 hand field while the lateral part of inferior area 6 (mouth field) is connected with the corresponding field in area 4. The organization of the connections between the two fields is, however, different. The hand fields in area 6 and 4 have direct reciprocal projections, whereas the mouth field in the postarcuate cortex relays information to area 4 via a zone intermediate between the arcuate and the central sulcus. This zone corresponds to the cytochrome oxidase area F4 (Matelli, Luppino, and Rizzolatti: Behav. Brain Res. 18: 125-137, '85). The inferior area 6 also has topographically organized connections with the supplementary motor area. The inferior area 6 receives and sends fibers to a series of discrete cortical areas located in the lower cortical moiety (Sanides: The Structure and Function of the Nervous Tissue, Vol. 5. New York: Academic Press, pp 329-453, '72). These areas that form a broad ring around the central sulcus are the ventral bank of the principal sulcus and the adjacent area 46, the precentral operculum (PrOC), area SII (Jones and Burton: J. Comp. Neurol. 168:197-248, '76), the parietal operculum, and the rostral part of the inferior parietal lobule including the lower bank of the intraparietal sulcus. Finally, the inferior area 6 has sparse but consistent connections with insular and cingulate cortices. The functional significance of this complex pattern of connections is discussed.

Mitchell Glickstein

Papers

The anatomy of the cerebellum

Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei.

Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei

Role of the cerebellum in visual guidance of movement

Afferent and efferent projections of the inferior area 6 in the macaque monkey.