Cargando…

Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control

Ipsilateral sensorimotor (iSM1) cortex negative BOLD responses (NBR) are observed to unilateral tasks and are thought to reflect a functionally relevant component of sensorimotor inhibition. Evidence suggests that sensorimotor inhibitory mechanisms degrade with age, along with aspects of motor abili...

Descripción completa

Detalles Bibliográficos
Autores principales: Mayhew, Stephen D., Coleman, Sebastian C., Mullinger, Karen J., Can, Cam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9130740/
https://www.ncbi.nlm.nih.gov/pubmed/35278710
http://dx.doi.org/10.1016/j.neuroimage.2022.119081
_version_ 1784713036247859200
author Mayhew, Stephen D.
Coleman, Sebastian C.
Mullinger, Karen J.
Can, Cam
author_facet Mayhew, Stephen D.
Coleman, Sebastian C.
Mullinger, Karen J.
Can, Cam
author_sort Mayhew, Stephen D.
collection PubMed
description Ipsilateral sensorimotor (iSM1) cortex negative BOLD responses (NBR) are observed to unilateral tasks and are thought to reflect a functionally relevant component of sensorimotor inhibition. Evidence suggests that sensorimotor inhibitory mechanisms degrade with age, along with aspects of motor ability and dexterity. However, understanding of age-related changes to NBR is restricted by limited comparisons between young vs old adults groups with relatively small samples sizes. Here we analysed a BOLD fMRI dataset (obtained from the CamCAN repository) of 581 healthy subjects, gender-balanced, sampled from the whole adult lifespan performing a motor response task to an audiovisual stimulus. We aimed to investigate how sensorimotor and default-mode NBR characteristics of magnitude, spatial extent and response shape alter at every decade of the aging process. We observed a linear decrease in iSM1 NBR magnitude across the whole lifespan, whereas the contralateral sensorimotor (cSM1) PBR magnitude was unchanged. An age-related decrease in the spatial extent of NBR and an increase in the ipsilateral positive BOLD response (PBR) was observed. This occurred alongside an increasing negative correlation between subject's iSM1 NBR and cSM1 PBR magnitude, reflecting a change in the balance between cortical excitation and inhibition. Conventional GLM analysis, using a canonical haemodynamic response (HR) function, showed disappearance of iSM1 NBR in subjects over 50 years of age. However, a deconvolution analysis showed that the shape of the iSM1 HR altered throughout the lifespan, with significantly delayed time-to-peak and decreased magnitude. The most significant decreases in iSM1 HR magnitude occurred in older age (>60 years) but the first changes in HR shape and timing occurred as early as 30 years, suggesting the possibility of separate mechanisms underlying these alterations. Reanalysis using data-driven HRs for each decade detected significant sensorimotor NBR into late older age, showing the importance of taking changes in HR morphology into account in fMRI aging studies. These results may reflect fMRI measures of the age-related decreases in transcollosal inhibition exerted upon ipsilateral sensorimotor cortex and alterations to the excitatory-inhibitory balance in the sensorimotor network.
format Online
Article
Text
id pubmed-9130740
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Academic Press
record_format MEDLINE/PubMed
spelling pubmed-91307402022-06-14 Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control Mayhew, Stephen D. Coleman, Sebastian C. Mullinger, Karen J. Can, Cam Neuroimage Article Ipsilateral sensorimotor (iSM1) cortex negative BOLD responses (NBR) are observed to unilateral tasks and are thought to reflect a functionally relevant component of sensorimotor inhibition. Evidence suggests that sensorimotor inhibitory mechanisms degrade with age, along with aspects of motor ability and dexterity. However, understanding of age-related changes to NBR is restricted by limited comparisons between young vs old adults groups with relatively small samples sizes. Here we analysed a BOLD fMRI dataset (obtained from the CamCAN repository) of 581 healthy subjects, gender-balanced, sampled from the whole adult lifespan performing a motor response task to an audiovisual stimulus. We aimed to investigate how sensorimotor and default-mode NBR characteristics of magnitude, spatial extent and response shape alter at every decade of the aging process. We observed a linear decrease in iSM1 NBR magnitude across the whole lifespan, whereas the contralateral sensorimotor (cSM1) PBR magnitude was unchanged. An age-related decrease in the spatial extent of NBR and an increase in the ipsilateral positive BOLD response (PBR) was observed. This occurred alongside an increasing negative correlation between subject's iSM1 NBR and cSM1 PBR magnitude, reflecting a change in the balance between cortical excitation and inhibition. Conventional GLM analysis, using a canonical haemodynamic response (HR) function, showed disappearance of iSM1 NBR in subjects over 50 years of age. However, a deconvolution analysis showed that the shape of the iSM1 HR altered throughout the lifespan, with significantly delayed time-to-peak and decreased magnitude. The most significant decreases in iSM1 HR magnitude occurred in older age (>60 years) but the first changes in HR shape and timing occurred as early as 30 years, suggesting the possibility of separate mechanisms underlying these alterations. Reanalysis using data-driven HRs for each decade detected significant sensorimotor NBR into late older age, showing the importance of taking changes in HR morphology into account in fMRI aging studies. These results may reflect fMRI measures of the age-related decreases in transcollosal inhibition exerted upon ipsilateral sensorimotor cortex and alterations to the excitatory-inhibitory balance in the sensorimotor network. Academic Press 2022-06 /pmc/articles/PMC9130740/ /pubmed/35278710 http://dx.doi.org/10.1016/j.neuroimage.2022.119081 Text en © 2022 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Mayhew, Stephen D.
Coleman, Sebastian C.
Mullinger, Karen J.
Can, Cam
Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title_full Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title_fullStr Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title_full_unstemmed Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title_short Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
title_sort across the adult lifespan the ipsilateral sensorimotor cortex negative bold response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9130740/
https://www.ncbi.nlm.nih.gov/pubmed/35278710
http://dx.doi.org/10.1016/j.neuroimage.2022.119081
work_keys_str_mv AT mayhewstephend acrosstheadultlifespantheipsilateralsensorimotorcortexnegativeboldresponseexhibitsdecreasesinmagnitudeandspatialextentsuggestingdeclininginhibitorycontrol
AT colemansebastianc acrosstheadultlifespantheipsilateralsensorimotorcortexnegativeboldresponseexhibitsdecreasesinmagnitudeandspatialextentsuggestingdeclininginhibitorycontrol
AT mullingerkarenj acrosstheadultlifespantheipsilateralsensorimotorcortexnegativeboldresponseexhibitsdecreasesinmagnitudeandspatialextentsuggestingdeclininginhibitorycontrol
AT cancam acrosstheadultlifespantheipsilateralsensorimotorcortexnegativeboldresponseexhibitsdecreasesinmagnitudeandspatialextentsuggestingdeclininginhibitorycontrol