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      Computational Architecture of the Parieto-Frontal Network Underlying Cognitive-Motor Control in Monkeys

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          Abstract

          The statistical structure of intrinsic parietal and parieto-frontal connectivity in monkeys was studied through hierarchical cluster analysis. Based on their inputs, parietal and frontal areas were grouped into different clusters, including a variable number of areas that in most instances occupied contiguous architectonic fields. Connectivity tended to be stronger locally: that is, within areas of the same cluster. Distant frontal and parietal areas were targeted through connections that in most instances were reciprocal and often of different strength. These connections linked parietal and frontal clusters formed by areas sharing basic functional properties. This led to five different medio-laterally oriented pillar domains spanning the entire extent of the parieto-frontal system, in the posterior parietal, anterior parietal, cingulate, frontal, and prefrontal cortex. Different information processing streams could be identified thanks to inter-domain connectivity. These streams encode fast hand reaching and its control, complex visuomotor action spaces, hand grasping, action/intention recognition, oculomotor intention and visual attention, behavioral goals and strategies, and reward and decision value outcome. Most of these streams converge on the cingulate domain, the main hub of the system. All of them are embedded within a larger eye–hand coordination network, from which they can be selectively set in motion by task demands.

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          Neural population dynamics during reaching

          Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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            Neurons in the orbitofrontal cortex encode economic value.

            Economic choice is the behaviour observed when individuals select one among many available options. There is no intrinsically 'correct' answer: economic choice depends on subjective preferences. This behaviour is traditionally the object of economic analysis and is also of primary interest in psychology. However, the underlying mental processes and neuronal mechanisms are not well understood. Theories of human and animal choice have a cornerstone in the concept of 'value'. Consider, for example, a monkey offered one raisin versus one piece of apple: behavioural evidence suggests that the animal chooses by assigning values to the two options. But where and how values are represented in the brain is unclear. Here we show that, during economic choice, neurons in the orbitofrontal cortex (OFC) encode the value of offered and chosen goods. Notably, OFC neurons encode value independently of visuospatial factors and motor responses. If a monkey chooses between A and B, neurons in the OFC encode the value of the two goods independently of whether A is presented on the right and B on the left, or vice versa. This trait distinguishes the OFC from other brain areas in which value modulates activity related to sensory or motor processes. Our results have broad implications for possible psychological models, suggesting that economic choice is essentially choice between goods rather than choice between actions. In this framework, neurons in the OFC seem to be a good candidate network for value assignment underlying economic choice.
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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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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                14 February 2017
                27 February 2017
                Jan-Feb 2017
                : 4
                : 1
                : ENEURO.0306-16.2017
                Affiliations
                [1 ]Department of Physiology and Pharmacology, University of Rome SAPIENZA , Rome, 00185, Italy
                [2 ]Department of Anatomy, Histology, Forensic Medicine, and Orthopedics, University of Rome SAPIENZA , Rome, 00185, Italy
                [3 ]Department of Medicine and Surgery, Section of Neuroscience, University of Parma , Parma, 43125, Italy
                [4 ]Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health , Bethesda, MD 20892
                Author notes

                Authors report no conflict of interest.

                Author contributions: R.C. and A.B.M. designed study; B.A., A.B.M., E.B., G.L., F.V.C., and R.C. analyzed data; R.C. and G.L. wrote the paper.

                This study was supported by grants from the University of Rome SAPIENZA (to ABM), from MIUR of Italy (protocol 2015AWSW2Y_002, to RC), and from the Intramural Research Program of the National Insitute of Mental Health (to BA).

                Correspondence should be addressed to Roberto Caminiti, Department of Physiology and Pharmacology, University of Rome SAPIENZA, Piazzale Aldo Moro 5, 00185 Rome, Italy. E-mail: roberto.caminiti@ 123456uniroma1.it .
                Author information
                http://orcid.org/0000-0001-6565-357X
                http://orcid.org/0000-0002-0220-0618
                Article
                eN-NWR-0306-16
                10.1523/ENEURO.0306-16.2017
                5329620
                28275714
                3204235f-66f4-4498-bf99-3c85960287e0
                Copyright © 2017 Caminiti et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 10 October 2016
                : 31 January 2017
                : 1 February 2017
                Page count
                Figures: 10, Tables: 1, Equations: 1, References: 441, Pages: 35, Words: 28492
                Funding
                Funded by: MIUR of Italy
                Award ID: 2015AWSW2Y_002
                Funded by: Intramural Research Program of NIMH
                Categories
                8
                New Research
                Sensory and Motor Systems
                Custom metadata
                January/February 2017

                cluster analysis,cognitive-motor behavior,cortico-cortical connectivity,frontal lobe,macaque monkey,parietal lobe

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