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      Neural encoding and functional interactions underlying pantomimed movements

      research-article
      ,
      Brain Structure & Function
      Springer Berlin Heidelberg
      Motor system, Action, Tool, Goal, Pantomime, fMRI, MVPA, Connectivity

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          Abstract

          Pantomimes are a unique movement category which can convey complex information about our intentions in the absence of any interaction with real objects. Indeed, we can pretend to use the same tool to perform different actions or to achieve the same goal adopting different tools. Nevertheless, how our brain implements pantomimed movements is still poorly understood. In our study, we explored the neural encoding and functional interactions underlying pantomimes adopting multivariate pattern analysis (MVPA) and connectivity analysis of fMRI data. Participants performed pantomimed movements, either grasp-to-move or grasp-to-use, as if they were interacting with two different tools (scissors or axe). These tools share the possibility to achieve the same goal. We adopted MVPA to investigate two levels of representation during the planning and execution of pantomimes: (1) distinguishing different actions performed with the same tool, (2) representing the same final goal irrespective of the adopted tool. We described widespread encoding of action information within regions of the so-called “tool” network. Several nodes of the network—comprising regions within the ventral and the dorsal stream—also represented goal information. The spatial distribution of goal information changed from planning—comprising posterior regions (i.e. parietal and temporal)—to execution—including also anterior regions (i.e. premotor cortex). Moreover, connectivity analysis provided evidence for task-specific bidirectional coupling between the ventral stream and parieto-frontal motor networks. Overall, we showed that pantomimes were characterized by specific patterns of action and goal encoding and by task-dependent cortical interactions.

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          Most cited references71

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          Localization of the motor hand area to a knob on the precentral gyrus. A new landmark.

          Using functional magnetic resonance imaging (fMRI) we have evaluated the anatomical location of the motor hand area. The segment of the precentral gyrus that most often contained motor hand function was a knob-like structure, that is shaped like an omega or epsilon in the axial plane and like a hook in the sagittal plane. On the cortical surface of cadaver specimens this precentral knob corresponded precisely to the characteristic 'middle knee' of the central sulcus that has been described by various anatomists in the last century. We were then able to show that this knob is a reliable landmark for identifying the precentral gyrus directly. We therefore conclude that neural elements involved in motor hand function are located in a characteristic 'precentral knob' which is a reliable landmark for identifying the precentral gyrus under normal and pathological conditions. It faces and forms the 'middle knee' of the central sulcus, is located just at the cross point between the precentral sulcus and the central sulcus, and is therefore also visible on the cortical surface.
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            Representation of manipulable man-made objects in the dorsal stream.

            We used fMRI to examine the neural response in frontal and parietal cortices associated with viewing and naming pictures of different categories of objects. Because tools are commonly associated with specific hand movements, we predicted that pictures of tools, but not other categories of objects, would elicit activity in regions of the brain that store information about motor-based properties. We found that viewing and naming pictures of tools selectively activated the left ventral premotor cortex (BA 6). Single-unit recording studies in monkeys have shown that neurons in the rostral part of the ventral premotor cortex (canonical F5 neurons) respond to the visual presentation of graspable objects, even in the absence of any subsequent motor activity. Thus, the left ventral premotor region that responded selectively to tools in the current study may be the human homolog of the monkey canonical F5 area. Viewing and naming tools also selectively activated the left posterior parietal cortex (BA 40). This response is similar to the firing of monkey anterior intraparietal neurons to the visual presentation of graspable objects. In humans and monkeys, there appears to be a close link between manipulable objects and information about the actions associated with their use. The selective activation of the left posterior parietal and left ventral premotor cortices by pictures of tools suggests that the ability to recognize and identify at least one category of objects (tools) may depend on activity in specific sites of the ventral and dorsal visual processing streams.
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              Connectivity-based approaches in stroke and recovery of function.

              After focal damage, cerebral networks reorganise their structural and functional anatomy to compensate for both the lesion itself and remote effects. Novel developments in the analysis of functional neuroimaging data enable us to assess in vivo the specific contributions of individual brain areas to recovery of function and the effect of treatment on cortical reorganisation. Connectivity analyses can be used to investigate the effect of stroke on cerebral networks, and help us to understand why some patients make a better recovery than others. This systems-level view also provides insights into how neuromodulatory interventions might target pathological network configurations associated with incomplete recovery. In the future, such analyses of connectivity could help to optimise treatment regimens based on the individual network pathology underlying a particular neurological deficit, thereby opening the way for stratification of patients based on the possible response to an intervention. Copyright © 2014 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                luca.turella@gmail.com , luca.turella@unitn.it
                Journal
                Brain Struct Funct
                Brain Struct Funct
                Brain Structure & Function
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1863-2653
                1863-2661
                10 July 2021
                10 July 2021
                2021
                : 226
                : 7
                : 2321-2337
                Affiliations
                GRID grid.11696.39, ISNI 0000 0004 1937 0351, Center for Mind/Brain Sciences (CIMeC), , University of Trento, ; Corso Bettini 31, 38068 Rovereto, Italy
                Author information
                http://orcid.org/0000-0003-1096-2150
                Article
                2332
                10.1007/s00429-021-02332-6
                8354930
                34247268
                84a462ad-c3a2-43da-9e55-e638579fb4e1
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 7 December 2020
                : 21 June 2021
                Funding
                Funded by: MIUR
                Award ID: FIRB 2013, project RBFR132BKP
                Award Recipient :
                Funded by: Università degli Studi di Trento
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2021

                Neurology
                motor system,action,tool,goal,pantomime,fmri,mvpa,connectivity
                Neurology
                motor system, action, tool, goal, pantomime, fmri, mvpa, connectivity

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