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      Seeing Your Foot Move Changes Muscle Proprioceptive Feedback

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          Abstract

          Multisensory effects are found when the input from single senses combines, and this has been well researched in the brain. Presently, we examined in humans the potential impact of visuo-proprioceptive interactions at the peripheral level, using microneurography, and compared it with a similar behavioral task. We used a paradigm where participants had either proprioceptive information only (no vision) or combined visual and proprioceptive signals (vision). We moved the foot to measure changes in the sensitivity of single muscle afferents, which can be altered by the descending fusimotor drive. Visual information interacted with proprioceptive information, where we found that for the same passive movement, the response of muscle afferents increased when the proprioceptive channel was the only source of information, as compared with when visual cues were added, regardless of the attentional level. Behaviorally, when participants looked at their foot moving, they more accurately judged differences between movement amplitudes, than in the absence of visual cues. These results impact our understanding of multisensory interactions throughout the nervous system, where the information from different senses can modify the sensitivity of peripheral receptors. This has clinical implications, where future strategies may modulate such visual signals during sensorimotor rehabilitation.

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          Most cited references49

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          Imaging the premotor areas.

          Recent imaging studies of motor function provide new insights into the organization of the premotor areas of the frontal lobe. The pre-supplementary motor area and the rostral portion of the dorsal premotor cortex, the 'pre-PMd', are, in many respects, more like prefrontal areas than motor areas. Recent data also suggest the existence of separate functional divisions in the rostral cingulate zone.
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            The origin of corticospinal projections from the premotor areas in the frontal lobe.

            We determined the origin of corticospinal neurons in the frontal lobe. These neurons were labeled by retrograde transport of tracers after injections into either the dorsolateral funiculus at the second cervical segment or the gray matter of the spinal cord throughout the cervical enlargement. Using retrograde transport of tracer from the arm area of the primary motor cortex, we defined the arm representation in each premotor area in another set of animals. We found that corticospinal projections to cervical segments of the spinal cord originate from the primary motor cortex and from the 6 premotor areas in the frontal lobe. These are the same premotor areas that project directly to the arm area of the primary motor cortex. The premotor areas are located in parts of cytoarchitectonic area 6 on the lateral surface and medial wall of the hemisphere, as well as in subfields of areas 23 and 24 in the cingulate sulcus. The total number of corticospinal neurons in the arm representations of the premotor areas equals or exceeds the total number in the arm representation of the primary motor cortex. The premotor areas collectively comprise more than 60% of the cortical area in the frontal lobe that projects to the spinal cord. Like the primary motor cortex, each of the premotor areas contains local regions that have a high density of corticospinal neurons. These observations indicate that a substantial component of the corticospinal system originates from the premotor areas in the frontal lobe. Each of the premotor areas has direct access to the spinal cord, and as a consequence, each has the potential to influence the generation and control of movement independently of the primary motor cortex. These findings raise serious questions about the utility of viewing the primary motor cortex as the "upper motoneuron" or "final common pathway" for the central control of movement.
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              Movement, posture and equilibrium: interaction and coordination.

              J Massion (1991)
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                4 March 2019
                22 March 2019
                Mar-Apr 2019
                : 6
                : 2
                : ENEURO.0341-18.2019
                Affiliations
                [1 ]Aix-Marseille Université, Centre National de la Recherche Scientifique, Laboratoire de Neurosciences Sensorielles et Cognitives - UMR 7260 , Marseille 13331, France
                [2 ]Department of Physiology, University of Gothenburg , Göteborg 40530, Sweden
                [3 ]Department of Neuroscience, Karolinska Institutet , Stockholm 17177, Sweden
                Author notes

                The authors declare no competing financial interests.

                Author contributions: R.A., M.C., J.-M.A., and E.R.-C. performed research; R.A., M.C., and A.K. contributed unpublished reagents/analytic tools; R.A., M.C., J.-M.A., E.R.-C., and A.K. analyzed data; R.A., M.C., J.-M.A., E.R.-C., and A.K. wrote the paper; E.R.-C. and A.K. designed research.

                This work was supported by the Agence Nationale de la Recherche, France Grant ANR12-JSH2-0005-01- Project: MULTISENSE (to A.K.). R.A. was supported by a grant from the FP7-People-COFUND (Marie Curie Actions) of the European Union, under Research Executive Agency Grant Agreement 608743. This publication reflects only the view of the authors and the European Union is not liable for any use that may be made of the information contained herein.

                [*]

                E.R.-C. and A.K. contributed equally to this work.

                Correspondence should be addressed to Anne Kavounoudias at anne.kavounoudias@ 123456univ-amu.fr .
                Author information
                https://orcid.org/0000-0003-4621-7929
                https://orcid.org/0000-0002-6678-1466
                https://orcid.org/0000-0003-4501-832X
                https://orcid.org/0000-0002-2712-8739
                Article
                eN-NWR-0341-18
                10.1523/ENEURO.0341-18.2019
                6437656
                30923738
                67fb77ac-0b86-415c-b704-db217c3b622d
                Copyright © 2019 Ackerley et al.

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

                History
                : 30 August 2018
                : 13 February 2019
                : 14 February 2019
                Page count
                Figures: 3, Tables: 3, Equations: 4, References: 57, Pages: 11, Words: 8673
                Funding
                Funded by: http://doi.org/10.13039/501100001665Agence Nationale de la Recherche (ANR)
                Award ID: #ANR12-JSH2-0005-01- Project: MULTISENSE
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                March/April 2019

                fusimotor drive,human,kinesthesia,movement perception,muscle proprioception

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