Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation

Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedfo...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Journal of neurophysiology 2019-04, Vol.121 (4), p.1162-1170
Hauptverfasser: Davare, Marco, Parikh, Pranav J, Santello, Marco
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1170
container_issue 4
container_start_page 1162
container_title Journal of neurophysiology
container_volume 121
creator Davare, Marco
Parikh, Pranav J
Santello, Marco
description Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW & NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.
doi_str_mv 10.1152/jn.00800.2018
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6485741</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2197888577</sourcerecordid><originalsourceid>FETCH-LOGICAL-c387t-aa04a199bd3f9ac1918016757f56f9294b9dbf4d20bc28846107b399cba567e33</originalsourceid><addsrcrecordid>eNpVkU1PHDEMhqOqqGy3PXJFc-xltk7mI8kFqVpBW2klDsA5JJnMkiWTLEmmgn9PtlBUTrbsx69tvQidYFhh3JHvO78CYAArAph9QItSIzXuOPuIFgAlb4DSY_Q5pR0A0A7IJ3RcaqTHHVug2yvjU4h2CjnEavbaxCytz0_VFIbZyWxSpUPMVoe0t166yjxqm6WyzhZomKP12yrdW-fMUAW1MzpXk_R2fxi2wX9BR6N0yXx9jUt0c3F-vf5Vby5__l7_2NS6YTTXUkIrMedqaEYuNeaYAe5pR8euHznhreKDGtuBgNKEsbbHQFXDuVay66lpmiU6e9Hdz2oygzY-R-nEvrwm45MI0or3HW_vxDb8EX3LOtriIvDtVSCGh9mkLCabtHFOehPmJAjmlLHC0oLWL6iOIaVoxrc1GMTBFbHz4q8r4uBK4U__v-2N_mdD8ww_xovw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2197888577</pqid></control><display><type>article</type><title>Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation</title><source>MEDLINE</source><source>American Physiological Society</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Alma/SFX Local Collection</source><creator>Davare, Marco ; Parikh, Pranav J ; Santello, Marco</creator><creatorcontrib>Davare, Marco ; Parikh, Pranav J ; Santello, Marco</creatorcontrib><description>Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW &amp; NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00800.2018</identifier><identifier>PMID: 30726158</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Adult ; Feedback, Sensory ; Female ; Fingers - physiology ; Hand Strength ; Humans ; Male ; Motor Skills ; Pyramidal Tracts - physiology ; Sensorimotor Cortex - physiology ; Touch Perception ; Uncertainty ; Visual Perception</subject><ispartof>Journal of neurophysiology, 2019-04, Vol.121 (4), p.1162-1170</ispartof><rights>Copyright © 2019 the American Physiological Society 2019 American Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c387t-aa04a199bd3f9ac1918016757f56f9294b9dbf4d20bc28846107b399cba567e33</citedby><cites>FETCH-LOGICAL-c387t-aa04a199bd3f9ac1918016757f56f9294b9dbf4d20bc28846107b399cba567e33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,3025,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30726158$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Davare, Marco</creatorcontrib><creatorcontrib>Parikh, Pranav J</creatorcontrib><creatorcontrib>Santello, Marco</creatorcontrib><title>Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW &amp; NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.</description><subject>Adult</subject><subject>Feedback, Sensory</subject><subject>Female</subject><subject>Fingers - physiology</subject><subject>Hand Strength</subject><subject>Humans</subject><subject>Male</subject><subject>Motor Skills</subject><subject>Pyramidal Tracts - physiology</subject><subject>Sensorimotor Cortex - physiology</subject><subject>Touch Perception</subject><subject>Uncertainty</subject><subject>Visual Perception</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU1PHDEMhqOqqGy3PXJFc-xltk7mI8kFqVpBW2klDsA5JJnMkiWTLEmmgn9PtlBUTrbsx69tvQidYFhh3JHvO78CYAArAph9QItSIzXuOPuIFgAlb4DSY_Q5pR0A0A7IJ3RcaqTHHVug2yvjU4h2CjnEavbaxCytz0_VFIbZyWxSpUPMVoe0t166yjxqm6WyzhZomKP12yrdW-fMUAW1MzpXk_R2fxi2wX9BR6N0yXx9jUt0c3F-vf5Vby5__l7_2NS6YTTXUkIrMedqaEYuNeaYAe5pR8euHznhreKDGtuBgNKEsbbHQFXDuVay66lpmiU6e9Hdz2oygzY-R-nEvrwm45MI0or3HW_vxDb8EX3LOtriIvDtVSCGh9mkLCabtHFOehPmJAjmlLHC0oLWL6iOIaVoxrc1GMTBFbHz4q8r4uBK4U__v-2N_mdD8ww_xovw</recordid><startdate>20190401</startdate><enddate>20190401</enddate><creator>Davare, Marco</creator><creator>Parikh, Pranav J</creator><creator>Santello, Marco</creator><general>American Physiological Society</general><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>5PM</scope></search><sort><creationdate>20190401</creationdate><title>Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation</title><author>Davare, Marco ; Parikh, Pranav J ; Santello, Marco</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c387t-aa04a199bd3f9ac1918016757f56f9294b9dbf4d20bc28846107b399cba567e33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Feedback, Sensory</topic><topic>Female</topic><topic>Fingers - physiology</topic><topic>Hand Strength</topic><topic>Humans</topic><topic>Male</topic><topic>Motor Skills</topic><topic>Pyramidal Tracts - physiology</topic><topic>Sensorimotor Cortex - physiology</topic><topic>Touch Perception</topic><topic>Uncertainty</topic><topic>Visual Perception</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Davare, Marco</creatorcontrib><creatorcontrib>Parikh, Pranav J</creatorcontrib><creatorcontrib>Santello, Marco</creatorcontrib><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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Davare, Marco</au><au>Parikh, Pranav J</au><au>Santello, Marco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2019-04-01</date><risdate>2019</risdate><volume>121</volume><issue>4</issue><spage>1162</spage><epage>1170</epage><pages>1162-1170</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>Sensorimotor memory built through previous hand-object interactions allows subjects to plan grasp forces. The memory-based mechanism is particularly effective when contact points on the object do not change across multiple manipulations, thus allowing subjects to generate the same forces in a feedforward fashion. However, allowing subjects to choose where to grasp an object causes trial-to-trial variability in fingertip positioning, suggesting a decreased ability to predict where the object will be grasped. In this scenario, subjects modulate forces on a trial-to-trial basis as a function of fingertip positioning. We suggested that this fingertip force-to-position modulation could be implemented by transforming feedback of digit placement into an accurate distribution of fingertip forces. Thus, decreasing certainty of fingertip position on an object would cause a shift from predominantly memory- to feedback-based force control mechanisms. To gain further insight into these sensorimotor transformation mechanisms, we asked subjects to grasp and lift an object with an asymmetrical center of mass while preventing it from tilting. To isolate the effect of digit placement uncertainty, we designed two experimental conditions that differed in terms of predictability of fingertip position but had similar average fingertip positioning and force distribution. We measured corticospinal excitability to probe possible changes in sensorimotor processing associated with digit placement uncertainty. We found a differential effect of sensorimotor uncertainty after but not before object contact. Our results suggest that sensorimotor integration is rapidly tuned after object contact based on different processing demands for memory versus feedback mechanisms underlying the control of manipulative forces. NEW &amp; NOTEWORTHY The relative contribution of predictive and feedback mechanisms for scaling digit forces to position during dexterous manipulation depends on the predictability of where the object will be grasped. We found that corticospinal excitability shortly after contact was sensitive to digit position predictability. This supports the proposition that distinct sensorimotor integration processes are engaged, depending on the role of feedback about digit placement versus sensorimotor memory in controlling manipulative forces.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>30726158</pmid><doi>10.1152/jn.00800.2018</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0022-3077
ispartof Journal of neurophysiology, 2019-04, Vol.121 (4), p.1162-1170
issn 0022-3077
1522-1598
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6485741
source MEDLINE; American Physiological Society; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
subjects Adult
Feedback, Sensory
Female
Fingers - physiology
Hand Strength
Humans
Male
Motor Skills
Pyramidal Tracts - physiology
Sensorimotor Cortex - physiology
Touch Perception
Uncertainty
Visual Perception
title Sensorimotor uncertainty modulates corticospinal excitability during skilled object manipulation
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-27T01%3A17%3A02IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Sensorimotor%20uncertainty%20modulates%20corticospinal%20excitability%20during%20skilled%20object%20manipulation&rft.jtitle=Journal%20of%20neurophysiology&rft.au=Davare,%20Marco&rft.date=2019-04-01&rft.volume=121&rft.issue=4&rft.spage=1162&rft.epage=1170&rft.pages=1162-1170&rft.issn=0022-3077&rft.eissn=1522-1598&rft_id=info:doi/10.1152/jn.00800.2018&rft_dat=%3Cproquest_pubme%3E2197888577%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2197888577&rft_id=info:pmid/30726158&rfr_iscdi=true