The effect of salient stimuli on neural oscillations, isometric force, and their coupling
Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly co...
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creator | Novembre, Giacomo Pawar, Vijay M. Kilintari, Marina Bufacchi, Rory J. Guo, Yifei Rothwell, John C. Iannetti, Gian Domenico |
description | Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency region (∼4 Hz) reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency region (beta-band, ∼20 Hz) reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behaviour in response to salient environmental events.
•We delivered salient stimuli to humans exerting a constant isometric force.•The stimuli evoked several modulations of both EEG and Force spectral power.•Some of these modulations were coupled across EEG and Force.•The coupled modulations were both phase-locked (∼4 Hz) and non-phase-locked (∼20 Hz).•Stimulus-induced corticomuscular coupling involves two types of cortical activity. |
doi_str_mv | 10.1016/j.neuroimage.2019.05.032 |
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•We delivered salient stimuli to humans exerting a constant isometric force.•The stimuli evoked several modulations of both EEG and Force spectral power.•Some of these modulations were coupled across EEG and Force.•The coupled modulations were both phase-locked (∼4 Hz) and non-phase-locked (∼20 Hz).•Stimulus-induced corticomuscular coupling involves two types of cortical activity.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2019.05.032</identifier><identifier>PMID: 31085301</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acoustic Stimulation ; Adult ; Auditory ; Auditory Perception - physiology ; Auditory stimuli ; Beta oscillations ; Biomechanical Phenomena ; Brain - physiology ; Brain research ; Brain Waves ; Conflicts of interest ; Cortico-muscular resonance (CMR) ; EEG ; Experiments ; Female ; Force ; Hand ; Humans ; Isometric ; Isometric Contraction ; Male ; Motor Activity ; Oscillations ; Physical Stimulation ; Psychomotor Performance - physiology ; Pyramidal tracts ; Sensorimotor Cortex - physiology ; Somatosensory ; Somatosensory cortex ; Touch Perception - physiology ; Young Adult</subject><ispartof>NeuroImage (Orlando, Fla.), 2019-09, Vol.198, p.221-230</ispartof><rights>2019 The Authors</rights><rights>Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.</rights><rights>2019. The Authors</rights><rights>2019 The Authors 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c507t-dce2d1e8bcc760a174e8eb9f56b43cbfdeb857c5d17c96c3c21c5d4f54f9ebb63</citedby><cites>FETCH-LOGICAL-c507t-dce2d1e8bcc760a174e8eb9f56b43cbfdeb857c5d17c96c3c21c5d4f54f9ebb63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2244078466?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,777,781,882,3537,27905,27906,45976,64364,64366,64368,72218</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31085301$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Novembre, Giacomo</creatorcontrib><creatorcontrib>Pawar, Vijay M.</creatorcontrib><creatorcontrib>Kilintari, Marina</creatorcontrib><creatorcontrib>Bufacchi, Rory J.</creatorcontrib><creatorcontrib>Guo, Yifei</creatorcontrib><creatorcontrib>Rothwell, John C.</creatorcontrib><creatorcontrib>Iannetti, Gian Domenico</creatorcontrib><title>The effect of salient stimuli on neural oscillations, isometric force, and their coupling</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency region (∼4 Hz) reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency region (beta-band, ∼20 Hz) reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behaviour in response to salient environmental events.
•We delivered salient stimuli to humans exerting a constant isometric force.•The stimuli evoked several modulations of both EEG and Force spectral power.•Some of these modulations were coupled across EEG and Force.•The coupled modulations were both phase-locked (∼4 Hz) and non-phase-locked (∼20 Hz).•Stimulus-induced corticomuscular coupling involves two types of cortical activity.</description><subject>Acoustic Stimulation</subject><subject>Adult</subject><subject>Auditory</subject><subject>Auditory Perception - physiology</subject><subject>Auditory stimuli</subject><subject>Beta oscillations</subject><subject>Biomechanical Phenomena</subject><subject>Brain - physiology</subject><subject>Brain research</subject><subject>Brain Waves</subject><subject>Conflicts of interest</subject><subject>Cortico-muscular resonance (CMR)</subject><subject>EEG</subject><subject>Experiments</subject><subject>Female</subject><subject>Force</subject><subject>Hand</subject><subject>Humans</subject><subject>Isometric</subject><subject>Isometric Contraction</subject><subject>Male</subject><subject>Motor Activity</subject><subject>Oscillations</subject><subject>Physical Stimulation</subject><subject>Psychomotor Performance - physiology</subject><subject>Pyramidal tracts</subject><subject>Sensorimotor Cortex - physiology</subject><subject>Somatosensory</subject><subject>Somatosensory cortex</subject><subject>Touch Perception - physiology</subject><subject>Young Adult</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkctu3CAUQFGVqkmm-YUKqZssYhcM2HhTKYnykiJ1ky66Qja-zDCyYQo4Uv--WJOkaTZhA4jDfR2EMCUlJbT-ti0dzMHbqVtDWRHalkSUhFUf0BElrSha0VQHy1mwQlLaHqLjGLeEkJZy-QkdMkqkYIQeoV8PG8BgDOiEvcGxGy24hGOy0zxa7B1eMnUj9lHbceyS9S6eYRv9BClYjY0PGs5w5wacNmAD1n7ejdatP6OPphsjnDztK_Tz-urh8ra4_3Fzd3l-X2hBmlQMGqqBguy1bmrS0YaDhL41ou45070ZoJei0WKgjW5rzXRF84UbwU0LfV-zFfq-j7ub-wlyOJdyvWoX8nTCH-U7q_5_cXaj1v5R1TUlLK8VOn0KEPzvGWJSk40acrMO_BxVVTEqeS15ldGvb9Ctn4PL7WWKc9JkbqlI7ikdfIwBzEsxlKjFn9qqf_7U4k8RobK__PXL62ZePj4Ly8DFHoA80kcLQWUv4DQMNmSHavD2_Sx_AUBVtAQ</recordid><startdate>201909</startdate><enddate>201909</enddate><creator>Novembre, Giacomo</creator><creator>Pawar, Vijay M.</creator><creator>Kilintari, Marina</creator><creator>Bufacchi, Rory J.</creator><creator>Guo, Yifei</creator><creator>Rothwell, John C.</creator><creator>Iannetti, Gian Domenico</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><general>Academic Press</general><scope>6I.</scope><scope>AAFTH</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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201909</creationdate><title>The effect of salient stimuli on neural oscillations, isometric force, and their coupling</title><author>Novembre, Giacomo ; Pawar, Vijay M. ; Kilintari, Marina ; Bufacchi, Rory J. ; Guo, Yifei ; Rothwell, John C. ; Iannetti, Gian Domenico</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c507t-dce2d1e8bcc760a174e8eb9f56b43cbfdeb857c5d17c96c3c21c5d4f54f9ebb63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Acoustic Stimulation</topic><topic>Adult</topic><topic>Auditory</topic><topic>Auditory Perception - physiology</topic><topic>Auditory stimuli</topic><topic>Beta oscillations</topic><topic>Biomechanical Phenomena</topic><topic>Brain - physiology</topic><topic>Brain research</topic><topic>Brain Waves</topic><topic>Conflicts of interest</topic><topic>Cortico-muscular resonance (CMR)</topic><topic>EEG</topic><topic>Experiments</topic><topic>Female</topic><topic>Force</topic><topic>Hand</topic><topic>Humans</topic><topic>Isometric</topic><topic>Isometric Contraction</topic><topic>Male</topic><topic>Motor Activity</topic><topic>Oscillations</topic><topic>Physical Stimulation</topic><topic>Psychomotor Performance - physiology</topic><topic>Pyramidal tracts</topic><topic>Sensorimotor Cortex - physiology</topic><topic>Somatosensory</topic><topic>Somatosensory cortex</topic><topic>Touch Perception - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Novembre, Giacomo</creatorcontrib><creatorcontrib>Pawar, Vijay M.</creatorcontrib><creatorcontrib>Kilintari, Marina</creatorcontrib><creatorcontrib>Bufacchi, Rory J.</creatorcontrib><creatorcontrib>Guo, Yifei</creatorcontrib><creatorcontrib>Rothwell, John C.</creatorcontrib><creatorcontrib>Iannetti, Gian Domenico</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Novembre, Giacomo</au><au>Pawar, Vijay M.</au><au>Kilintari, Marina</au><au>Bufacchi, Rory J.</au><au>Guo, Yifei</au><au>Rothwell, John C.</au><au>Iannetti, Gian Domenico</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The effect of salient stimuli on neural oscillations, isometric force, and their coupling</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2019-09</date><risdate>2019</risdate><volume>198</volume><spage>221</spage><epage>230</epage><pages>221-230</pages><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency region (∼4 Hz) reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency region (beta-band, ∼20 Hz) reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behaviour in response to salient environmental events.
•We delivered salient stimuli to humans exerting a constant isometric force.•The stimuli evoked several modulations of both EEG and Force spectral power.•Some of these modulations were coupled across EEG and Force.•The coupled modulations were both phase-locked (∼4 Hz) and non-phase-locked (∼20 Hz).•Stimulus-induced corticomuscular coupling involves two types of cortical activity.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31085301</pmid><doi>10.1016/j.neuroimage.2019.05.032</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic Stimulation Adult Auditory Auditory Perception - physiology Auditory stimuli Beta oscillations Biomechanical Phenomena Brain - physiology Brain research Brain Waves Conflicts of interest Cortico-muscular resonance (CMR) EEG Experiments Female Force Hand Humans Isometric Isometric Contraction Male Motor Activity Oscillations Physical Stimulation Psychomotor Performance - physiology Pyramidal tracts Sensorimotor Cortex - physiology Somatosensory Somatosensory cortex Touch Perception - physiology Young Adult |
title | The effect of salient stimuli on neural oscillations, isometric force, and their coupling |
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