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      Perceiving What Is Reachable Depends on Motor Representations: Evidence from a Transcranial Magnetic Stimulation Study

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          Abstract

          Background

          Visually determining what is reachable in peripersonal space requires information about the egocentric location of objects but also information about the possibilities of action with the body, which are context dependent. The aim of the present study was to test the role of motor representations in the visual perception of peripersonal space.

          Methodology

          Seven healthy participants underwent a TMS study while performing a right-left decision (control) task or perceptually judging whether a visual target was reachable or not with their right hand. An actual grasping movement task was also included. Single pulse TMS was delivered 80% of the trials on the left motor and premotor cortex and on a control site (the temporo-occipital area), at 90% of the resting motor threshold and at different SOA conditions (50ms, 100ms, 200ms or 300ms).

          Principal Findings

          Results showed a facilitation effect of the TMS on reaction times in all tasks, whatever the site stimulated and until 200ms after stimulus presentation. However, the facilitation effect was on average 34ms lower when stimulating the motor cortex in the perceptual judgement task, especially for stimuli located at the boundary of peripersonal space.

          Conclusion

          This study provides the first evidence that brain motor area participate in the visual determination of what is reachable. We discuss how motor representations may feed the perceptual system with information about possible interactions with nearby objects and thus may contribute to the perception of the boundary of peripersonal space.

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          Most cited references55

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          Functional properties of brain areas associated with motor execution and imagery.

          Imagining motor acts is a cognitive task that engages parts of the executive motor system. While motor imagery has been intensively studied using neuroimaging techniques, most studies lack behavioral observations. Here, we used functional MRI to compare the functional neuroanatomy of motor execution and imagery using a task that objectively assesses imagery performance. With surface electromyographic monitoring within a scanner, 10 healthy subjects performed sequential finger-tapping movements according to visually presented number stimuli in either a movement or an imagery mode of performance. We also examined effects of varied and fixed stimulus types that differ in stimulus dependency of the task. Statistical parametric mapping revealed movement-predominant activity, imagery-predominant activity, and activity common to both movement and imagery modes of performance (movement-and-imagery activity). The movement-predominant activity included the primary sensory and motor areas, parietal operculum, and anterior cerebellum that had little imagery-related activity (-0.1 ~ 0.1%), and the caudal premotor areas and area 5 that had mild-to-moderate imagery-related activity (0.2 ~ 0.7%). Many frontoparietal areas and posterior cerebellum demonstrated movement-and-imagery activity. Imagery-predominant areas included the precentral sulcus at the level of middle frontal gyrus and the posterior superior parietal cortex/precuneus. Moreover, activity of the superior precentral sulcus and intraparietal sulcus areas, predominantly on the left, was associated with accuracy of the imagery task performance. Activity of the inferior precentral sulcus (area 6/44) showed stimulus-type effect particularly for the imagery mode. A time-course analysis of activity suggested a functional gradient, which was characterized by a more "executive" or more "imaginative" property in many areas related to movement and/or imagery. The results from the present study provide new insights into the functional neuroanatomy of motor imagery, including the effects of imagery performance and stimulus-dependency on brain activity.
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            Partially overlapping neural networks for real and imagined hand movements.

            Neuroimagery findings have shown similar cerebral networks associated with imagination and execution of a movement. On the other hand, neuropsychological studies of parietal-lesioned patients suggest that these networks may be at least partly distinct. In the present study, normal subjects were asked to either imagine or execute auditory-cued hand movements. Compared with rest, imagination and execution showed overlapping networks, including bilateral premotor and parietal areas, basal ganglia and cerebellum. However, direct comparison between the two experimental conditions showed that specific cortico-subcortical areas were more engaged in mental simulation, including bilateral premotor, prefrontal, supplementary motor and left posterior parietal areas, and the caudate nuclei. These results suggest that a specific neuronal substrate is involved in the processing of hand motor representations.
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              Role of the posterior parietal cortex in updating reaching movements to a visual target.

              The exact role of posterior parietal cortex (PPC) in visually directed reaching is unknown. We propose that, by building an internal representation of instantaneous hand location, PPC computes a dynamic motor error used by motor centers to correct the ongoing trajectory. With unseen right hands, five subjects pointed to visual targets that either remained stationary or moved during saccadic eye movements. Transcranial magnetic stimulation (TMS) was applied over the left PPC during target presentation. Stimulation disrupted path corrections that normally occur in response to target jumps, but had no effect on those directed at stationary targets. Furthermore, left-hand movement corrections were not blocked, ruling out visual or oculomotor effects of stimulation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                6 August 2008
                : 3
                : 8
                : e2862
                Affiliations
                [1 ]Lab. URECA (EA 1059), Université de Lille–Nord de France, Lille, France
                [2 ]UMR-CNRS 8163 STL, Université de Lille–Nord de France, Lille, France
                [3 ]Département de Neurophysiologie Clinique, Hôpital Roger Salengro, Centre Hospitalier Régional Universitaire, Lille, France
                Harvard Medical School, United States of America
                Author notes

                Conceived and designed the experiments: YC AB BA EH PD. Performed the experiments: YC AB BA EH. Analyzed the data: YC AB BA HD. Contributed reagents/materials/analysis tools: YC AB BA EH PD. Wrote the paper: YC AB HD.

                Article
                08-PONE-RA-04021R2
                10.1371/journal.pone.0002862
                2483935
                18682848
                e7bfb306-e5e8-49f8-bc74-321a2676e769
                Coello et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 20 March 2008
                : 14 July 2008
                Page count
                Pages: 12
                Categories
                Research Article
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Cognitive Neuroscience
                Neuroscience/Experimental Psychology

                Uncategorized
                Uncategorized

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