A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination
Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To addres...
Gespeichert in:
Veröffentlicht in: | Neuropsychologia 2021-09, Vol.160, p.107969-107969, Article 107969 |
---|---|
Hauptverfasser: | , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 107969 |
---|---|
container_issue | |
container_start_page | 107969 |
container_title | Neuropsychologia |
container_volume | 160 |
creator | Schaffer, Jacob E. Sarlegna, Fabrice R. Sainburg, Robert L. |
description | Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.
•We examined bimanual coordination in a deafferented participant, and in age-matched control participants.•Significant differences were seen in the trajectories of the dominant and non-dominant hands in the deafferented participant.•The dominant arm of the deafferented participant showed more drift than the non-dominant arm at the end of movement.•Even without proprioception, lateralized mechanisms persist, resulting in asymmetrical control of position and trajectory. |
doi_str_mv | 10.1016/j.neuropsychologia.2021.107969 |
format | Article |
fullrecord | <record><control><sourceid>proquest_webof</sourceid><recordid>TN_cdi_proquest_miscellaneous_2555636942</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0028393221002220</els_id><sourcerecordid>2555636942</sourcerecordid><originalsourceid>FETCH-LOGICAL-c537t-fc09b4e8597ad343a6b693faafcec115b8cd1f414b4221eb5bcb58e25c217c9c3</originalsourceid><addsrcrecordid>eNqNkc2O0zAUhS0EYsrAK6CsEAil-CdO4g1SVQEdqRKbYW3ZzvXUVWoXOymat8dtOoWZ1axs-X7n-FwdhD4QPCeY1F-2cw9jDPt0bzahD3dOzSmmJA8bUYsXaEbahpWMk-olmmFM25IJRq_Qm5S2GOOK0_Y1umIVI1g0ZIa6RRFVhMKoBEWwRQfKWojgBzW44IsIB1B9KpQvIKX87FRfxNCf4H0OEl0wsD-xzhfa9WqAmBkTQuycP7m8Ra9sNoF35_Ma_fr-7Xa5Ktc_f9wsF-vScNYMpTVY6ApaLhrV5Yiq1rVgVilrwBDCdWs6YitS6YpSAppro3kLlBtKGiMMu0ZfJ9_9qHfQmRw3R5E5407FexmUk48n3m3kXThIgTkXosoGnyaDzRPZarGWxzfMGMWipgeS2Y_nz2L4PUIa5M4lA32vPIQxSco5r1ktKvovl4khpQj24k2wPNYqt_JprfJYq5xqzQbv_1_sIn_oMQPtBPwBHWwyDryBC5aLrwXOLMs3QpZuKncZRj9k6efnSzO9mmjIPR4cRHlWdC6CGWQX3HOX-gt0KeJA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2555636942</pqid></control><display><type>article</type><title>A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination</title><source>MEDLINE</source><source>Web of Science - Science Citation Index Expanded - 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /></source><source>Access via ScienceDirect (Elsevier)</source><source>Web of Science - Social Sciences Citation Index – 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /></source><creator>Schaffer, Jacob E. ; Sarlegna, Fabrice R. ; Sainburg, Robert L.</creator><creatorcontrib>Schaffer, Jacob E. ; Sarlegna, Fabrice R. ; Sainburg, Robert L.</creatorcontrib><description>Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.
•We examined bimanual coordination in a deafferented participant, and in age-matched control participants.•Significant differences were seen in the trajectories of the dominant and non-dominant hands in the deafferented participant.•The dominant arm of the deafferented participant showed more drift than the non-dominant arm at the end of movement.•Even without proprioception, lateralized mechanisms persist, resulting in asymmetrical control of position and trajectory.</description><identifier>ISSN: 0028-3932</identifier><identifier>ISSN: 1873-3514</identifier><identifier>EISSN: 1873-3514</identifier><identifier>DOI: 10.1016/j.neuropsychologia.2021.107969</identifier><identifier>PMID: 34310971</identifier><language>eng</language><publisher>OXFORD: Elsevier Ltd</publisher><subject>Arm ; Behavioral Sciences ; Bimanual coordination ; Cognitive science ; Cognitive Sciences ; Hand ; Handedness ; Humans ; Large-fiber sensory neuropathy ; Life Sciences ; Life Sciences & Biomedicine ; Motor lateralization ; Movement ; Neurons and Cognition ; Neuroscience ; Neurosciences ; Neurosciences & Neurology ; Proprioception ; Psychology ; Psychology, Experimental ; Psychomotor Performance ; Science & Technology ; Social Sciences</subject><ispartof>Neuropsychologia, 2021-09, Vol.160, p.107969-107969, Article 107969</ispartof><rights>2021 Elsevier Ltd</rights><rights>Copyright © 2021 Elsevier Ltd. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>9</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000690431300011</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c537t-fc09b4e8597ad343a6b693faafcec115b8cd1f414b4221eb5bcb58e25c217c9c3</citedby><cites>FETCH-LOGICAL-c537t-fc09b4e8597ad343a6b693faafcec115b8cd1f414b4221eb5bcb58e25c217c9c3</cites><orcidid>0000-0002-7718-7286</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuropsychologia.2021.107969$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,315,781,785,886,3551,27929,27930,39262,39263,46000</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34310971$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03320962$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Schaffer, Jacob E.</creatorcontrib><creatorcontrib>Sarlegna, Fabrice R.</creatorcontrib><creatorcontrib>Sainburg, Robert L.</creatorcontrib><title>A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination</title><title>Neuropsychologia</title><addtitle>NEUROPSYCHOLOGIA</addtitle><addtitle>Neuropsychologia</addtitle><description>Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.
•We examined bimanual coordination in a deafferented participant, and in age-matched control participants.•Significant differences were seen in the trajectories of the dominant and non-dominant hands in the deafferented participant.•The dominant arm of the deafferented participant showed more drift than the non-dominant arm at the end of movement.•Even without proprioception, lateralized mechanisms persist, resulting in asymmetrical control of position and trajectory.</description><subject>Arm</subject><subject>Behavioral Sciences</subject><subject>Bimanual coordination</subject><subject>Cognitive science</subject><subject>Cognitive Sciences</subject><subject>Hand</subject><subject>Handedness</subject><subject>Humans</subject><subject>Large-fiber sensory neuropathy</subject><subject>Life Sciences</subject><subject>Life Sciences & Biomedicine</subject><subject>Motor lateralization</subject><subject>Movement</subject><subject>Neurons and Cognition</subject><subject>Neuroscience</subject><subject>Neurosciences</subject><subject>Neurosciences & Neurology</subject><subject>Proprioception</subject><subject>Psychology</subject><subject>Psychology, Experimental</subject><subject>Psychomotor Performance</subject><subject>Science & Technology</subject><subject>Social Sciences</subject><issn>0028-3932</issn><issn>1873-3514</issn><issn>1873-3514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>GIZIO</sourceid><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><recordid>eNqNkc2O0zAUhS0EYsrAK6CsEAil-CdO4g1SVQEdqRKbYW3ZzvXUVWoXOymat8dtOoWZ1axs-X7n-FwdhD4QPCeY1F-2cw9jDPt0bzahD3dOzSmmJA8bUYsXaEbahpWMk-olmmFM25IJRq_Qm5S2GOOK0_Y1umIVI1g0ZIa6RRFVhMKoBEWwRQfKWojgBzW44IsIB1B9KpQvIKX87FRfxNCf4H0OEl0wsD-xzhfa9WqAmBkTQuycP7m8Ra9sNoF35_Ma_fr-7Xa5Ktc_f9wsF-vScNYMpTVY6ApaLhrV5Yiq1rVgVilrwBDCdWs6YitS6YpSAppro3kLlBtKGiMMu0ZfJ9_9qHfQmRw3R5E5407FexmUk48n3m3kXThIgTkXosoGnyaDzRPZarGWxzfMGMWipgeS2Y_nz2L4PUIa5M4lA32vPIQxSco5r1ktKvovl4khpQj24k2wPNYqt_JprfJYq5xqzQbv_1_sIn_oMQPtBPwBHWwyDryBC5aLrwXOLMs3QpZuKncZRj9k6efnSzO9mmjIPR4cRHlWdC6CGWQX3HOX-gt0KeJA</recordid><startdate>20210917</startdate><enddate>20210917</enddate><creator>Schaffer, Jacob E.</creator><creator>Sarlegna, Fabrice R.</creator><creator>Sainburg, Robert L.</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>17B</scope><scope>BLEPL</scope><scope>DTL</scope><scope>DVR</scope><scope>EGQ</scope><scope>GIZIO</scope><scope>HGBXW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7718-7286</orcidid></search><sort><creationdate>20210917</creationdate><title>A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination</title><author>Schaffer, Jacob E. ; Sarlegna, Fabrice R. ; Sainburg, Robert L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c537t-fc09b4e8597ad343a6b693faafcec115b8cd1f414b4221eb5bcb58e25c217c9c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arm</topic><topic>Behavioral Sciences</topic><topic>Bimanual coordination</topic><topic>Cognitive science</topic><topic>Cognitive Sciences</topic><topic>Hand</topic><topic>Handedness</topic><topic>Humans</topic><topic>Large-fiber sensory neuropathy</topic><topic>Life Sciences</topic><topic>Life Sciences & Biomedicine</topic><topic>Motor lateralization</topic><topic>Movement</topic><topic>Neurons and Cognition</topic><topic>Neuroscience</topic><topic>Neurosciences</topic><topic>Neurosciences & Neurology</topic><topic>Proprioception</topic><topic>Psychology</topic><topic>Psychology, Experimental</topic><topic>Psychomotor Performance</topic><topic>Science & Technology</topic><topic>Social Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schaffer, Jacob E.</creatorcontrib><creatorcontrib>Sarlegna, Fabrice R.</creatorcontrib><creatorcontrib>Sainburg, Robert L.</creatorcontrib><collection>Web of Knowledge</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Social Sciences Citation Index</collection><collection>Web of Science Primary (SCIE, SSCI & AHCI)</collection><collection>Web of Science - Social Sciences Citation Index – 2021</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schaffer, Jacob E.</au><au>Sarlegna, Fabrice R.</au><au>Sainburg, Robert L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination</atitle><jtitle>Neuropsychologia</jtitle><stitle>NEUROPSYCHOLOGIA</stitle><addtitle>Neuropsychologia</addtitle><date>2021-09-17</date><risdate>2021</risdate><volume>160</volume><spage>107969</spage><epage>107969</epage><pages>107969-107969</pages><artnum>107969</artnum><issn>0028-3932</issn><issn>1873-3514</issn><eissn>1873-3514</eissn><abstract>Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.
•We examined bimanual coordination in a deafferented participant, and in age-matched control participants.•Significant differences were seen in the trajectories of the dominant and non-dominant hands in the deafferented participant.•The dominant arm of the deafferented participant showed more drift than the non-dominant arm at the end of movement.•Even without proprioception, lateralized mechanisms persist, resulting in asymmetrical control of position and trajectory.</abstract><cop>OXFORD</cop><pub>Elsevier Ltd</pub><pmid>34310971</pmid><doi>10.1016/j.neuropsychologia.2021.107969</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-7718-7286</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0028-3932 |
ispartof | Neuropsychologia, 2021-09, Vol.160, p.107969-107969, Article 107969 |
issn | 0028-3932 1873-3514 1873-3514 |
language | eng |
recordid | cdi_proquest_miscellaneous_2555636942 |
source | MEDLINE; Web of Science - Science Citation Index Expanded - 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; Access via ScienceDirect (Elsevier); Web of Science - Social Sciences Citation Index – 2021<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /> |
subjects | Arm Behavioral Sciences Bimanual coordination Cognitive science Cognitive Sciences Hand Handedness Humans Large-fiber sensory neuropathy Life Sciences Life Sciences & Biomedicine Motor lateralization Movement Neurons and Cognition Neuroscience Neurosciences Neurosciences & Neurology Proprioception Psychology Psychology, Experimental Psychomotor Performance Science & Technology Social Sciences |
title | A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-16T03%3A03%3A26IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_webof&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20rare%20case%20of%20deafferentation%20reveals%20an%20essential%20role%20of%20proprioception%20in%20bilateral%20coordination&rft.jtitle=Neuropsychologia&rft.au=Schaffer,%20Jacob%20E.&rft.date=2021-09-17&rft.volume=160&rft.spage=107969&rft.epage=107969&rft.pages=107969-107969&rft.artnum=107969&rft.issn=0028-3932&rft.eissn=1873-3514&rft_id=info:doi/10.1016/j.neuropsychologia.2021.107969&rft_dat=%3Cproquest_webof%3E2555636942%3C/proquest_webof%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2555636942&rft_id=info:pmid/34310971&rft_els_id=S0028393221002220&rfr_iscdi=true |