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Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin
Cervical dystonia is characterized by involuntary, abnormal movements and postures of the head and neck. Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explor...
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Published in: | PloS one 2013-05, Vol.8 (5), p.e62877 |
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description | Cervical dystonia is characterized by involuntary, abnormal movements and postures of the head and neck. Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explored whether cervical dystonia patients have altered functional brain connectivity compared to healthy controls, by investigating 10 resting state networks. Scans were repeated immediately before and some weeks after botulinum toxin injections to see whether connectivity abnormalities were restored. We here show that cervical dystonia patients have reduced connectivity in selected regions of the prefrontal cortex, premotor cortex and superior parietal lobule within a distributed network that comprises the premotor cortex, supplementary motor area, primary sensorimotor cortex, and secondary somatosensory cortex (sensorimotor network). With regard to a network originating from the occipital cortex (primary visual network), selected regions in the prefrontal and premotor cortex, superior parietal lobule, and middle temporal gyrus areas have reduced connectivity. In selected regions of the prefrontal, premotor, primary motor and early visual cortex increased connectivity was found within a network that comprises the prefrontal cortex including the anterior cingulate cortex and parietal cortex (executive control network). Botulinum toxin treatment resulted in a partial restoration of connectivity abnormalities in the sensorimotor and primary visual network. These findings demonstrate the involvement of multiple neural networks in cervical dystonia. The reduced connectivity within the sensorimotor and primary visual networks may provide the neural substrate to expect defective motor planning and disturbed spatial cognition. Increased connectivity within the executive control network suggests excessive attentional control and while this may be a primary trait, perhaps contributing to abnormal motor control, this may alternatively serve a compensatory function in order to reduce the consequences of the motor planning defect inflicted by the other network abnormalities. |
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Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explored whether cervical dystonia patients have altered functional brain connectivity compared to healthy controls, by investigating 10 resting state networks. Scans were repeated immediately before and some weeks after botulinum toxin injections to see whether connectivity abnormalities were restored. We here show that cervical dystonia patients have reduced connectivity in selected regions of the prefrontal cortex, premotor cortex and superior parietal lobule within a distributed network that comprises the premotor cortex, supplementary motor area, primary sensorimotor cortex, and secondary somatosensory cortex (sensorimotor network). With regard to a network originating from the occipital cortex (primary visual network), selected regions in the prefrontal and premotor cortex, superior parietal lobule, and middle temporal gyrus areas have reduced connectivity. In selected regions of the prefrontal, premotor, primary motor and early visual cortex increased connectivity was found within a network that comprises the prefrontal cortex including the anterior cingulate cortex and parietal cortex (executive control network). Botulinum toxin treatment resulted in a partial restoration of connectivity abnormalities in the sensorimotor and primary visual network. These findings demonstrate the involvement of multiple neural networks in cervical dystonia. The reduced connectivity within the sensorimotor and primary visual networks may provide the neural substrate to expect defective motor planning and disturbed spatial cognition. Increased connectivity within the executive control network suggests excessive attentional control and while this may be a primary trait, perhaps contributing to abnormal motor control, this may alternatively serve a compensatory function in order to reduce the consequences of the motor planning defect inflicted by the other network abnormalities.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0062877</identifier><identifier>PMID: 23650536</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Adult ; Aged ; Aged, 80 and over ; Anti-Dyskinesia Agents - pharmacology ; Anti-Dyskinesia Agents - therapeutic use ; Biology ; Botulinum toxin ; Botulinum Toxins - pharmacology ; Botulinum Toxins - therapeutic use ; Brain ; Brain Mapping ; Care and treatment ; Case-Control Studies ; Cerebellum - physiopathology ; Cognition ; Cognition & reasoning ; Computer networks ; Cortex (cingulate) ; Cortex (motor) ; Cortex (occipital) ; Cortex (parietal) ; Cortex (premotor) ; Cortex (somatosensory) ; Cortex (temporal) ; Defects ; Development and progression ; Dystonia ; Executive function ; Female ; Functional magnetic resonance imaging ; Head and neck ; Health aspects ; Humans ; Magnetic Resonance Imaging ; Male ; Medicine ; Middle Aged ; Motor Cortex - physiopathology ; Motor task performance ; Nerve Net - physiopathology ; Neural networks ; Neurology ; Occipital lobe ; Patients ; Perceptual-motor processes ; Prefrontal cortex ; Restoration ; Sensorimotor integration ; Social and Behavioral Sciences ; Somatosensory cortex ; Spatial distribution ; Studies ; Substrates ; Superior parietal lobule ; Supplementary motor area ; Temporal cortex ; Temporal gyrus ; Testing ; Torticollis - drug therapy ; Torticollis - physiopathology ; Visual cortex ; Visual Cortex - physiopathology</subject><ispartof>PloS one, 2013-05, Vol.8 (5), p.e62877</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Delnooz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Delnooz et al 2013 Delnooz et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-9bb4bb62b6421882551bb8a4b5254b1c2e14ef939c47592f75826d8175db08e83</citedby><cites>FETCH-LOGICAL-c692t-9bb4bb62b6421882551bb8a4b5254b1c2e14ef939c47592f75826d8175db08e83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1348121814/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1348121814?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,25734,27905,27906,36993,44571,53772,53774,74875</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23650536$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Barton, Jason Jeremy Sinclair</contributor><creatorcontrib>Delnooz, Cathérine C S</creatorcontrib><creatorcontrib>Pasman, Jaco W</creatorcontrib><creatorcontrib>Beckmann, Christian F</creatorcontrib><creatorcontrib>van de Warrenburg, Bart P C</creatorcontrib><title>Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Cervical dystonia is characterized by involuntary, abnormal movements and postures of the head and neck. Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explored whether cervical dystonia patients have altered functional brain connectivity compared to healthy controls, by investigating 10 resting state networks. Scans were repeated immediately before and some weeks after botulinum toxin injections to see whether connectivity abnormalities were restored. We here show that cervical dystonia patients have reduced connectivity in selected regions of the prefrontal cortex, premotor cortex and superior parietal lobule within a distributed network that comprises the premotor cortex, supplementary motor area, primary sensorimotor cortex, and secondary somatosensory cortex (sensorimotor network). 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Current views on its pathophysiology, such as faulty sensorimotor integration and impaired motor planning, are largely based on studies of focal hand dystonia. Using resting state fMRI, we explored whether cervical dystonia patients have altered functional brain connectivity compared to healthy controls, by investigating 10 resting state networks. Scans were repeated immediately before and some weeks after botulinum toxin injections to see whether connectivity abnormalities were restored. We here show that cervical dystonia patients have reduced connectivity in selected regions of the prefrontal cortex, premotor cortex and superior parietal lobule within a distributed network that comprises the premotor cortex, supplementary motor area, primary sensorimotor cortex, and secondary somatosensory cortex (sensorimotor network). With regard to a network originating from the occipital cortex (primary visual network), selected regions in the prefrontal and premotor cortex, superior parietal lobule, and middle temporal gyrus areas have reduced connectivity. In selected regions of the prefrontal, premotor, primary motor and early visual cortex increased connectivity was found within a network that comprises the prefrontal cortex including the anterior cingulate cortex and parietal cortex (executive control network). Botulinum toxin treatment resulted in a partial restoration of connectivity abnormalities in the sensorimotor and primary visual network. These findings demonstrate the involvement of multiple neural networks in cervical dystonia. The reduced connectivity within the sensorimotor and primary visual networks may provide the neural substrate to expect defective motor planning and disturbed spatial cognition. Increased connectivity within the executive control network suggests excessive attentional control and while this may be a primary trait, perhaps contributing to abnormal motor control, this may alternatively serve a compensatory function in order to reduce the consequences of the motor planning defect inflicted by the other network abnormalities.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23650536</pmid><doi>10.1371/journal.pone.0062877</doi><tpages>e62877</tpages><oa>free_for_read</oa></addata></record> |
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recordid | cdi_plos_journals_1348121814 |
source | Publicly Available Content Database; PubMed Central |
subjects | Abnormalities Adult Aged Aged, 80 and over Anti-Dyskinesia Agents - pharmacology Anti-Dyskinesia Agents - therapeutic use Biology Botulinum toxin Botulinum Toxins - pharmacology Botulinum Toxins - therapeutic use Brain Brain Mapping Care and treatment Case-Control Studies Cerebellum - physiopathology Cognition Cognition & reasoning Computer networks Cortex (cingulate) Cortex (motor) Cortex (occipital) Cortex (parietal) Cortex (premotor) Cortex (somatosensory) Cortex (temporal) Defects Development and progression Dystonia Executive function Female Functional magnetic resonance imaging Head and neck Health aspects Humans Magnetic Resonance Imaging Male Medicine Middle Aged Motor Cortex - physiopathology Motor task performance Nerve Net - physiopathology Neural networks Neurology Occipital lobe Patients Perceptual-motor processes Prefrontal cortex Restoration Sensorimotor integration Social and Behavioral Sciences Somatosensory cortex Spatial distribution Studies Substrates Superior parietal lobule Supplementary motor area Temporal cortex Temporal gyrus Testing Torticollis - drug therapy Torticollis - physiopathology Visual cortex Visual Cortex - physiopathology |
title | Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-17T17%3A36%3A30IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Task-free%20functional%20MRI%20in%20cervical%20dystonia%20reveals%20multi-network%20changes%20that%20partially%20normalize%20with%20botulinum%20toxin&rft.jtitle=PloS%20one&rft.au=Delnooz,%20Cath%C3%A9rine%20C%20S&rft.date=2013-05-01&rft.volume=8&rft.issue=5&rft.spage=e62877&rft.pages=e62877-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0062877&rft_dat=%3Cgale_plos_%3EA478448763%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c692t-9bb4bb62b6421882551bb8a4b5254b1c2e14ef939c47592f75826d8175db08e83%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1348121814&rft_id=info:pmid/23650536&rft_galeid=A478448763&rfr_iscdi=true |