Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition

Autores
Holschneider, Daniel P.; Guo, Yumei; Wang, Zhuo; Roch, Margareth; Scremin, Oscar Umberto
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
We explored whether cerebral cortical impact injury (CCI) effects extend beyond direct lesion sites to affect remote brain networks, and whether acetylcholinesterase (AChE) inhibition elicits discrete changes in functional activation of motor circuits following CCI. Adult male rats underwent unilateral motor-sensory CCI or sham injury. Physostigmine (AChE inhibitor) or saline were administered subcutaneously continuously via implanted minipumps (1.6 micromoles/kg/day) for 3 weeks, followed by cerebral perfusion mapping during treadmill walking using [14C]-iodoantipyrine. Quantitative autoradiographs were analyzed by statistical parametric mapping and functional connectivity (FC) analysis. CCI resulted in functional deficits in the ipsilesional basal ganglia, with increased activation contralesionally. Recruitment was also observed, especially contralesionally, of the red nucleus, superior colliculus, pedunculopontine tegmental nucleus, thalamus (ventrolateral n., central medial n.), cerebellum, and sensory cortex. FC decreased significantly within ipsi- and contralesional motor circuits and between hemispheres, but increased between midline cerebellum and select regions of the basal ganglia within each hemisphere. Physostigmine significantly increased functional brain activation in the cerebellar thalamocortical pathway (midline cerebellum/ventrolateral thalamus/motor cortex), subthalamic nucleus/zona incerta, and red nucleus and bilateral sensory cortex. In conclusion, CCI resulted in increased functional recruitment of contralesional motor cortex and bilateral subcortical motor regions, as well as recruitment of the cerebellar– thalamocortical circuit and contralesional sensory cortex. This phenomenon, augmented by physostigmine, may partially compensate motor deficits. FC decreased inter-hemispherically and in negative, but not positive, intra-hemispherical FC, and it was not affected by physostigmine. Circuit-based approaches into functional brain reorganization may inform future behavioral or molecular strategies to augment targeted neurorehabilitation.
Fil: Holschneider, Daniel P.. University of California at Los Angeles; Estados Unidos
Fil: Guo, Yumei. University of California at Los Angeles; Estados Unidos
Fil: Wang, Zhuo. University of California at Los Angeles; Estados Unidos
Fil: Roch, Margareth. University of California at Los Angeles; Estados Unidos
Fil: Scremin, Oscar Umberto. University of California at Los Angeles; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
Brain Imaging
Brain Trauma
Rats
Autoradiography
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/21589

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network_name_str CONICET Digital (CONICET)
spelling Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibitionHolschneider, Daniel P.Guo, YumeiWang, ZhuoRoch, MargarethScremin, Oscar UmbertoBrain ImagingBrain TraumaRatsAutoradiographyhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1We explored whether cerebral cortical impact injury (CCI) effects extend beyond direct lesion sites to affect remote brain networks, and whether acetylcholinesterase (AChE) inhibition elicits discrete changes in functional activation of motor circuits following CCI. Adult male rats underwent unilateral motor-sensory CCI or sham injury. Physostigmine (AChE inhibitor) or saline were administered subcutaneously continuously via implanted minipumps (1.6 micromoles/kg/day) for 3 weeks, followed by cerebral perfusion mapping during treadmill walking using [14C]-iodoantipyrine. Quantitative autoradiographs were analyzed by statistical parametric mapping and functional connectivity (FC) analysis. CCI resulted in functional deficits in the ipsilesional basal ganglia, with increased activation contralesionally. Recruitment was also observed, especially contralesionally, of the red nucleus, superior colliculus, pedunculopontine tegmental nucleus, thalamus (ventrolateral n., central medial n.), cerebellum, and sensory cortex. FC decreased significantly within ipsi- and contralesional motor circuits and between hemispheres, but increased between midline cerebellum and select regions of the basal ganglia within each hemisphere. Physostigmine significantly increased functional brain activation in the cerebellar thalamocortical pathway (midline cerebellum/ventrolateral thalamus/motor cortex), subthalamic nucleus/zona incerta, and red nucleus and bilateral sensory cortex. In conclusion, CCI resulted in increased functional recruitment of contralesional motor cortex and bilateral subcortical motor regions, as well as recruitment of the cerebellar– thalamocortical circuit and contralesional sensory cortex. This phenomenon, augmented by physostigmine, may partially compensate motor deficits. FC decreased inter-hemispherically and in negative, but not positive, intra-hemispherical FC, and it was not affected by physostigmine. Circuit-based approaches into functional brain reorganization may inform future behavioral or molecular strategies to augment targeted neurorehabilitation.Fil: Holschneider, Daniel P.. University of California at Los Angeles; Estados UnidosFil: Guo, Yumei. University of California at Los Angeles; Estados UnidosFil: Wang, Zhuo. University of California at Los Angeles; Estados UnidosFil: Roch, Margareth. University of California at Los Angeles; Estados UnidosFil: Scremin, Oscar Umberto. University of California at Los Angeles; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaMary Ann Liebert Inc2013-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/21589Holschneider, Daniel P.; Guo, Yumei; Wang, Zhuo; Roch, Margareth; Scremin, Oscar Umberto; Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition; Mary Ann Liebert Inc; Journal of Neurotrauma; 30; 11; 1-2013; 907-9190897-7151CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1089/neu.2012.2657info:eu-repo/semantics/altIdentifier/url/http://online.liebertpub.com/doi/abs/10.1089/neu.2012.2657info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:37:27Zoai:ri.conicet.gov.ar:11336/21589instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:37:27.27CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
title Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
spellingShingle Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
Holschneider, Daniel P.
Brain Imaging
Brain Trauma
Rats
Autoradiography
title_short Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
title_full Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
title_fullStr Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
title_full_unstemmed Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
title_sort Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition
dc.creator.none.fl_str_mv Holschneider, Daniel P.
Guo, Yumei
Wang, Zhuo
Roch, Margareth
Scremin, Oscar Umberto
author Holschneider, Daniel P.
author_facet Holschneider, Daniel P.
Guo, Yumei
Wang, Zhuo
Roch, Margareth
Scremin, Oscar Umberto
author_role author
author2 Guo, Yumei
Wang, Zhuo
Roch, Margareth
Scremin, Oscar Umberto
author2_role author
author
author
author
dc.subject.none.fl_str_mv Brain Imaging
Brain Trauma
Rats
Autoradiography
topic Brain Imaging
Brain Trauma
Rats
Autoradiography
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv We explored whether cerebral cortical impact injury (CCI) effects extend beyond direct lesion sites to affect remote brain networks, and whether acetylcholinesterase (AChE) inhibition elicits discrete changes in functional activation of motor circuits following CCI. Adult male rats underwent unilateral motor-sensory CCI or sham injury. Physostigmine (AChE inhibitor) or saline were administered subcutaneously continuously via implanted minipumps (1.6 micromoles/kg/day) for 3 weeks, followed by cerebral perfusion mapping during treadmill walking using [14C]-iodoantipyrine. Quantitative autoradiographs were analyzed by statistical parametric mapping and functional connectivity (FC) analysis. CCI resulted in functional deficits in the ipsilesional basal ganglia, with increased activation contralesionally. Recruitment was also observed, especially contralesionally, of the red nucleus, superior colliculus, pedunculopontine tegmental nucleus, thalamus (ventrolateral n., central medial n.), cerebellum, and sensory cortex. FC decreased significantly within ipsi- and contralesional motor circuits and between hemispheres, but increased between midline cerebellum and select regions of the basal ganglia within each hemisphere. Physostigmine significantly increased functional brain activation in the cerebellar thalamocortical pathway (midline cerebellum/ventrolateral thalamus/motor cortex), subthalamic nucleus/zona incerta, and red nucleus and bilateral sensory cortex. In conclusion, CCI resulted in increased functional recruitment of contralesional motor cortex and bilateral subcortical motor regions, as well as recruitment of the cerebellar– thalamocortical circuit and contralesional sensory cortex. This phenomenon, augmented by physostigmine, may partially compensate motor deficits. FC decreased inter-hemispherically and in negative, but not positive, intra-hemispherical FC, and it was not affected by physostigmine. Circuit-based approaches into functional brain reorganization may inform future behavioral or molecular strategies to augment targeted neurorehabilitation.
Fil: Holschneider, Daniel P.. University of California at Los Angeles; Estados Unidos
Fil: Guo, Yumei. University of California at Los Angeles; Estados Unidos
Fil: Wang, Zhuo. University of California at Los Angeles; Estados Unidos
Fil: Roch, Margareth. University of California at Los Angeles; Estados Unidos
Fil: Scremin, Oscar Umberto. University of California at Los Angeles; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description We explored whether cerebral cortical impact injury (CCI) effects extend beyond direct lesion sites to affect remote brain networks, and whether acetylcholinesterase (AChE) inhibition elicits discrete changes in functional activation of motor circuits following CCI. Adult male rats underwent unilateral motor-sensory CCI or sham injury. Physostigmine (AChE inhibitor) or saline were administered subcutaneously continuously via implanted minipumps (1.6 micromoles/kg/day) for 3 weeks, followed by cerebral perfusion mapping during treadmill walking using [14C]-iodoantipyrine. Quantitative autoradiographs were analyzed by statistical parametric mapping and functional connectivity (FC) analysis. CCI resulted in functional deficits in the ipsilesional basal ganglia, with increased activation contralesionally. Recruitment was also observed, especially contralesionally, of the red nucleus, superior colliculus, pedunculopontine tegmental nucleus, thalamus (ventrolateral n., central medial n.), cerebellum, and sensory cortex. FC decreased significantly within ipsi- and contralesional motor circuits and between hemispheres, but increased between midline cerebellum and select regions of the basal ganglia within each hemisphere. Physostigmine significantly increased functional brain activation in the cerebellar thalamocortical pathway (midline cerebellum/ventrolateral thalamus/motor cortex), subthalamic nucleus/zona incerta, and red nucleus and bilateral sensory cortex. In conclusion, CCI resulted in increased functional recruitment of contralesional motor cortex and bilateral subcortical motor regions, as well as recruitment of the cerebellar– thalamocortical circuit and contralesional sensory cortex. This phenomenon, augmented by physostigmine, may partially compensate motor deficits. FC decreased inter-hemispherically and in negative, but not positive, intra-hemispherical FC, and it was not affected by physostigmine. Circuit-based approaches into functional brain reorganization may inform future behavioral or molecular strategies to augment targeted neurorehabilitation.
publishDate 2013
dc.date.none.fl_str_mv 2013-01
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/21589
Holschneider, Daniel P.; Guo, Yumei; Wang, Zhuo; Roch, Margareth; Scremin, Oscar Umberto; Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition; Mary Ann Liebert Inc; Journal of Neurotrauma; 30; 11; 1-2013; 907-919
0897-7151
CONICET Digital
CONICET
url http://hdl.handle.net/11336/21589
identifier_str_mv Holschneider, Daniel P.; Guo, Yumei; Wang, Zhuo; Roch, Margareth; Scremin, Oscar Umberto; Remote brain network changes after unilateral cortical impact injury and their modulation by Acetylcholinesterase inhibition; Mary Ann Liebert Inc; Journal of Neurotrauma; 30; 11; 1-2013; 907-919
0897-7151
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1089/neu.2012.2657
info:eu-repo/semantics/altIdentifier/url/http://online.liebertpub.com/doi/abs/10.1089/neu.2012.2657
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Mary Ann Liebert Inc
publisher.none.fl_str_mv Mary Ann Liebert Inc
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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