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      Top-down signals transmitted from prefrontal to parietal neurons reflect the executive control of cognition

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          Abstract

          Prefrontal cortex influences behavior largely through its connections with other association cortices; however the nature of the information conveyed by prefrontal output signals and what effect these signals have on computations performed by target structures is largely unknown. To address these questions, we simultaneously recorded the activity of neurons in prefrontal and posterior parietal cortex of monkeys performing a rule-based spatial categorization task. Parietal cortex receives direct prefrontal input, and parietal neurons, like their prefrontal counterparts, exhibit signals that reflect rule-based cognitive processing in this task. By analyzing rapid fluctuations in the cognitive information encoded by activity in the two areas, we obtained evidence that signals reflecting rule-dependent categories were selectively transmitted in a top-down direction from prefrontal to parietal neurons, suggesting prefrontal output is important for the executive control of distributed cognitive processing.

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          Most cited references28

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          High-frequency, long-range coupling between prefrontal and visual cortex during attention.

          Electrical recordings in humans and monkeys show attentional enhancement of evoked responses and gamma synchrony in ventral stream cortical areas. Does this synchrony result from intrinsic activity in visual cortex or from inputs from other structures? Using paired recordings in the frontal eye field (FEF) and area V4, we found that attention to a stimulus in their joint receptive field leads to enhanced oscillatory coupling between the two areas, particularly at gamma frequencies. This coupling appeared to be initiated by FEF and was time-shifted by about 8 to 13 milliseconds across a range of frequencies. Considering the expected conduction and synaptic delays between the areas, this time-shifted coupling at gamma frequencies may optimize the postsynaptic impact of spikes from one area upon the other, improving cross-area communication with attention.
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            Neural correlates of decision variables in parietal cortex.

            Decision theory proposes that humans and animals decide what to do in a given situation by assessing the relative value of each possible response. This assessment can be computed, in part, from the probability that each action will result in a gain and the magnitude of the gain expected. Here we show that the gain (or reward) a monkey can expect to realize from an eye-movement response modulates the activity of neurons in the lateral intraparietal area, an area of primate cortex that is thought to transform visual signals into eye-movement commands. We also show that the activity of these neurons is sensitive to the probability that a particular response will result in a gain. When animals can choose freely between two alternative responses, the choices subjects make and neuronal activation in this area are both correlated with the relative amount of gain that the animal can expect from each response. Our data indicate that a decision-theoretic model may provide a powerful new framework for studying the neural processes that intervene between sensation and action.
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              Matching behavior and the representation of value in the parietal cortex.

              Psychologists and economists have long appreciated the contribution of reward history and expectation to decision-making. Yet we know little about how specific histories of choice and reward lead to an internal representation of the "value" of possible actions. We approached this problem through an integrated application of behavioral, computational, and physiological techniques. Monkeys were placed in a dynamic foraging environment in which they had to track the changing values of alternative choices through time. In this context, the monkeys' foraging behavior provided a window into their subjective valuation. We found that a simple model based on reward history can duplicate this behavior and that neurons in the parietal cortex represent the relative value of competing actions predicted by this model.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                29 November 2013
                01 September 2013
                October 2013
                18 February 2019
                : 16
                : 10
                : 1484-1491
                Affiliations
                [1 ]Department of Neuroscience, University of Minnesota, Minneapolis, MN, USA
                [2 ]Brain Sciences Center, VA Medical Center, Minneapolis, MN, USA
                [3 ]Department of Biology, Augsburg College, Minneapolis, MN, USA
                [4 ]Medical Scientist Training Program (MD/PhD), University of Minnesota, Minneapolis, MN, USA
                [5 ]Center for Cognitive Sciences, University of Minnesota, Minneapolis, MN, USA
                [6 ]Department of Psychiatry, University of Minnesota, Minneapolis, MN, USA
                [7 ]Department of Psychology, University of Minnesota, Minneapolis, MN, USA
                Author notes
                [* ]Correspondence to: Matthew V. Chafee, chafe001@ 123456umn.edu
                Article
                NIHMS512104
                10.1038/nn.3509
                6379206
                23995071
                9dd62797-18a3-4ed0-b66a-5702348c727f

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                Neurosciences
                Neurosciences

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