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• W2013250864 abstract "Around the last turn of the century, neuroscientists were heatedly debating the associative functions of the large regions of the cerebral cortex that lie between primary sensory and motor areas. Primary areas had recently been identified anatomically, and their functions were being unveiled by lesion and electrical methods. Little or nothing was known, however, about those other areas between them, which in the human included wide expanses of the cortex of the occipital, temporal, and parietal lobes, as well as the prefrontal cortex, by itself making up nearly one-third of the neocortex. 2Flechsig P. Lancet. 1901; 2: 1027-1029Abstract Scopus (281) Google Scholar, noting that those large areas developed late in phylogeny and ontogeny, proposed that they served to mediate new associations of sensation with movement and also certain associative functions of the mind, such as memory. Despite respectable support from clinical observations and animal experiments, those ideas were dismissed, even ridiculed, as unfounded attempts to revitalize, by neurologizing it, a fading doctrine of associationist psychology. For most of this century, the neurophysiologists of the cortex have ignored them. The thalamus has been widely considered the key to cortical physiology, and the sensory and motor cortices the key to the physiology of the areas beyond. That began to change some 30 years ago. Since then, some of the old ideas have come back, this time bolstered by solid anatomical and physiological evidence. We have discovered the previously unsuspected richness and specificity of cortico-cortical axonal connections (10Pandya, D.N., and Yeterian, E.H. (1985). In Cerebral Cortex, A. Peters and E.G. Jones, eds. (New York: Plenum), pp. 3–61.Google Scholar). Even in primary visual cortex, which critically depends on the thalamus, <5% of the terminal axons have been found to be of thalamic—geniculate—origin; the vast majority are of cortical origin, local or remote (11Peters A. Payne B.R. Cereb. Cortex. 1993; 3: 69-78Crossref PubMed Scopus (211) Google Scholar). Highlighting the importance of cortical connectivity for cognitive functions, microelectrode recording studies in the behaving monkey have revealed the widespread cortical activation of neurons during the memorization of an event or an object. We are rapidly making the transition from modular cognition to network cognition. The new perspective is that memory representations are comprised of widely distributed cortical networks that transcend areas and modules by any anatomical definition (reviewed by 4Fuster J.M. Trends Neurosci. 1997; 20 (a): 451-459Abstract Full Text Full Text PDF PubMed Scopus (488) Google Scholar). Memory networks are probably hierarchically organized, overlapping anatomically, and profusely interconnected. Accordingly, any neuron or group of neurons, anywhere in the cortex, can be part of many networks and thus many memories. The making of those networks follows certain principles of synaptic modulation that are not yet fully understood. It appears almost certain, however, that learning and the acquisition of memory are based on the synaptic linkage of elementary cortical representations or nets into complex networks. Those new or expanded networks represent new cognitive structures or gestalts. All memory would, therefore, be associative and the memory code essentially a relational code. According to this view, memory networks, after they have been formed, are defined by their cortico-cortical connectivity, are exquisitely specific with regard to their content, and presumably, to a degree, are topographically idiosyncratic for each individual. In the course of behavior, reasoning, or speech, memory networks are successively activated—ignited, to use Braitenberg’s term (1978)—by recall, recognition, or the need to retain them in short-term memory. Working memory, the kind of short-term memory needed to perform a sequential task, may simply be the temporary activation of a widespread cortical network of long-term memory for prospective action. That prospective action is what determines the role of the prefrontal cortex in that state of memory, for this cortex contains the action-related associations of networks originating in posterior cortex and itself plays a critical role in the organization of sequential actions toward a goal (5Fuster J.M. The Prefrontal Cortex. Lippincott-Raven, Philadelphia1997Google Scholar). To better understand the interactions between the prefrontal and other cortices in behavior, it is useful to view them all in the context of the perception–action cycle. Briefly, this cycle is the circular flow of neural information by which an organism relates to its environment, a basic principle of biological cybernetics. The figure shows very schematically the cortical stages of that cycle and their interconnections (human brain in the inset, arrows symbolizing aggregates of fiber connections demonstrated in the monkey). Those cortical stages are the upper levels of two parallel hierarchies of neural structures, one sensory and the other motor, that extend through the entire length of the nerve axis, from the spinal cord to the highest cortex of association. (The unlabeled stages represent intermediary cortical areas or subareas of adjacent labeled regions.) All connections between stages are bidirectional, providing feedforward as well as feedback. In the course of new or recently acquired behavior, sensory information is processed along the sensory hierarchy—both serially and in parallel. In the cortex, that information translates into action, which is processed down the motor hierarchy to produce change in the environment, which leads to sensory change, which is processed through the sensory hierarchy and then modulates further action, and so on. The prefrontal and posterior association cortices are in the cycle inasmuch and for as long as the behavior contains novelty, uncertainty, or ambiguity and has to bridge time spans with short-term memory. As those constraints disappear and behavior becomes automatic (e.g., walking, skilled routines), the action is integrated in lower structures (e.g., premotor cortex, basal ganglia) and sensory processing shunted at lower levels of the cycle. Asaad et al. (1998 [this issue of Neuron]) take us closer than ever before to understanding how those action-related associations are formed in the prefrontal cortex, at the top of the cycle. Their experimental animal, a monkey, is trained in a delay task, where a particular visual stimulus calls for a particular movement of the eyes after a short delay. This delay makes the task a memory task, requiring the subject to recognize and retain a stimulus for subsequent action. Based on previous research, so-called memory cells are expectedly found, which fire faster during the delay than during intertrial baseline periods; the discharge of some of these cells is stimulus preferential, that is, higher in reaction to a given stimulus than to another. In other cells nearby, the discharge is related to the movement. Most notable is the finding of cells that are related to both the cue and the response, or a particular combination of the two. As the learning of a new association progresses, activity in prefrontal cells related to the direction of impending movement develops progressively earlier. Thus, the authors demonstrate in an elegant manner that prefrontal neurons become part of cortical networks containing and representing associations between visual stimuli and movements. Because memory cells were observed first in the prefrontal cortex and repeatedly reencountered in it (6Fuster J.M. Alexander G.E. Science. 1971; 173: 652-654Crossref PubMed Scopus (1346) Google Scholar, 9Niki H. Brain Res. 1974; 70: 346-349Crossref PubMed Scopus (182) Google Scholar, 3Funahashi S. Bruce C.J. Goldman-Rakic P.S. J. Neurophysiol. 1989; 61: 331-349PubMed Google Scholar), such cells have long been considered the substrate of its specific role in working memory. There is now ample evidence, however, that this state of memory activates also other broad and widely dispersed areas of the cortex with which the prefrontal cortex is connected. In addition to prefrontal neurons, the short-term retention of visual stimuli elicits the sustained activation of neurons in inferotemporal cortex (7Fuster J.M. Jervey J. Science. 1981; 212: 952-955Crossref PubMed Scopus (293) Google Scholar, 8Miller E.K. Li L. Desimone R. J. Neurosci. 1993; 13: 1460-1478PubMed Google Scholar) and even in somatosensory cortex if the task is visuo-haptic (12Zhou Y. Fuster J.M. Exp. Brain Res. 1997; 116: 551-555Crossref PubMed Scopus (90) Google Scholar). In sum, therefore, the memory-active prefrontal cells are part of extensive networks that span posterior as well as frontal cortex. There is evidence that their sustained activation in working memory results from the dynamic interactions between those cortices at or near the top of the perception–action cycle (4Fuster J.M. Trends Neurosci. 1997; 20 (a): 451-459Abstract Full Text Full Text PDF PubMed Scopus (488) Google Scholar). The cells that Asaad et al. describe seem to become part of those networks as they are formed or expanded by learning and thus also to become engaged in the interactions at the summit of the perception–action cycle. In general, however, as sensory–motor associations become routine, they are presumably relegated to lower stages of the cycle. That is probably why, with overlearning, cortical activations disappear from tomographic screens, and the neurons described by Asaad et al. seem to lose their interest in old or familiar associations. The experimental approach of these investigators is uniquely suited to reveal these changes. Indeed, somewhat paradoxically, the microelectrode remains the best tool to explore neural mechanisms in distributed cortical networks with thousands if not millions of neurons." @default.
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• W2013250864 title "Linkage at the Top" @default.
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