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      Posterior parietal cortex contains a command apparatus for hand movements

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          Significance

          The primate hand has evolved into a specialized sensorimotor device that can grasp, explore, and manipulate objects with extraordinary skill. The frontal lobe is generally thought to be the exclusive source of descending commands to the spinal cord to control hand movements. Here, we identify a region within the parietal lobe that could also contribute commands to control hand movements directly at spinal levels. Intracortical stimulation in a lateral region in area 5 of posterior parietal cortex reliably evokes hand movements. Corticospinal neurons in this region make disynaptic connections with hand motoneurons. These observations suggest that a region within lateral area 5 contains a unique command apparatus that could assist in generating dexterous finger movements required during haptic behavior.

          Abstract

          Mountcastle and colleagues proposed that the posterior parietal cortex contains a “command apparatus” for the operation of the hand in immediate extrapersonal space [Mountcastle et al. (1975) J Neurophysiol 38(4):871–908]. Here we provide three lines of converging evidence that a lateral region within area 5 has corticospinal neurons that are directly linked to the control of hand movements. First, electrical stimulation in a lateral region of area 5 evokes finger and wrist movements. Second, corticospinal neurons in the same region of area 5 terminate at spinal locations that contain last-order interneurons that innervate hand motoneurons. Third, this lateral region of area 5 contains many neurons that make disynaptic connections with hand motoneurons. The disynaptic input to motoneurons from this portion of area 5 is as direct and prominent as that from any of the premotor areas in the frontal lobe. Thus, our results establish that a region within area 5 contains a motor area with corticospinal neurons that could function as a command apparatus for operation of the hand.

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          Most cited references31

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          The organization of the cortical motor system: new concepts.

          A series of recent anatomical and functional data has radically changed our view on the organization of the motor cortex in primates. In the present article we present this view and discuss its fundamental principles. The basic principles are the following: (a) the motor cortex, defined as the agranular frontal cortex, is formed by a mosaic of separate areas, each of which contains an independent body movement representation, (b) each motor area plays a specific role in motor control, based on the specificity of its cortical afferents and descending projections, (c) in analogy to the motor cortex, the posterior parietal cortex is formed by a multiplicity of areas, each of which is involved in the analysis of particular aspects of sensory information. There are no such things as multipurpose areas for space or body schema and (d) the parieto-frontal connections form a series of segregated anatomical circuits devoted to specific sensorimotor transformations. These circuits transform sensory information into action. They represent the basic functional units of the motor system. Although these conclusions mostly derive from monkey experiments, anatomical and brain-imaging evidence suggest that the organization of human motor cortex is based on the same principles. Possible homologies between the motor cortices of humans and non-human primates are discussed.
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            Motor areas in the frontal lobe of the primate.

            There has been a substantial change in our concepts about the cortical motor areas. It is now clear that the frontal lobe of primates contains at least six premotor areas that project directly to the primary motor cortex (M1). Two premotor areas, the ventral premotor area (PMv) and the dorsal premotor area (PMd), are located on the lateral surface of the hemisphere. Four premotor areas are located on the medial wall of the hemisphere and include the supplementary motor area (SMA) and three cingulate motor areas. Each of these premotor areas has substantial direct projections to the spinal cord. Corticospinal axons from the premotor areas terminate in the intermediate zone of the spinal cord, and some also terminate in the ventral horn around motoneurons. In this respect, the premotor areas are like M1 and appear to have direct connections with spinal motoneurons, particularly those innervating hand muscles. Furthermore, it is possible to evoke movements of the distal and proximal forelimb using intracortical stimulation at relatively low currents in the premotor areas. Thus, the premotor areas appear to have the potential to influence the control of movement not only at the level of M1, but also more directly at the level of the spinal cord. For these reasons, we have suggested that the premotor areas may operate at a hierarchical level comparable to M1. We propose that each premotor area is a functionally distinct efferent system that differentially generates and/or controls specific aspects of motor behavior.
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              Muscle representation in the macaque motor cortex: an anatomical perspective.

              How are the neurons that directly influence the motoneurons of a muscle distributed in the primary motor cortex (M1)? To answer this classical question we used retrograde transneuronal transport of rabies virus from single muscles of macaques. This enabled us to define cortico-motoneuronal (CM) cells that make monosynaptic connections with the motoneurons of the injected muscle. We examined the distribution of CM cells that project to motoneurons of three thumb and finger muscles. We found that the CM cells for these digit muscles are restricted to the caudal portion of M1, which is buried in the central sulcus. Within this region of M1, CM cells for one muscle display a remarkably widespread distribution and fill the entire mediolateral extent of the arm area. In fact, CM cells for digit muscles are found in regions of M1 that are known to contain the shoulder representation. The cortical territories occupied by CM cells for different muscles overlap extensively. Thus, we found no evidence for a focal representation of single muscles in M1. Instead, the overlap and intermingling among the different populations of CM cells may be the neural substrate to create a wide variety of muscle synergies. We found two additional surprising results. First, 15-16% of the CM cells originate from area 3a, a region of primary somatosensory cortex. Second, the size range of CM cells includes both "fast" and "slow" pyramidal tract neurons. These observations are likely to lead to dramatic changes in views about the function of the CM system.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                18 April 2017
                3 April 2017
                3 April 2017
                : 114
                : 16
                : 4255-4260
                Affiliations
                [1] aUniversity of Pittsburgh Brain Institute, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [2] bSystems Neuroscience Institute, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [3] cCenter for the Neural Basis of Cognition, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [4] dDepartment of Neurobiology, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261
                Author notes
                1To whom correspondence should be addressed. Email: strickp@ 123456pitt.edu .

                Edited by Mortimer Mishkin, National Institute for Mental Health, Bethesda, MD, and approved February 7, 2017 (received for review May 20, 2016)

                Author contributions: J.-A.R., R.P.D., and P.L.S. designed research, performed research, analyzed data, and wrote the paper.

                Article
                PMC5402465 PMC5402465 5402465 201608132
                10.1073/pnas.1608132114
                5402465
                28373554
                6078853d-be5b-4292-8dea-3ef4fbc2ec46

                Freely available online through the PNAS open access option.

                History
                Page count
                Pages: 6
                Funding
                Funded by: HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) 100000065
                Award ID: R01 NS24328
                Funded by: HHS | NIH | NIH Office of the Director (OD) 100000052
                Award ID: P40 OD010996
                Funded by: HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) 100000065
                Award ID: P30 NS076405
                Categories
                Biological Sciences
                Neuroscience
                From the Cover

                cerebral cortex,movement control,motor systems,motor control

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