Cortical dynamics during preparation and execution of reactive balance responses with distinct postural demands

Teodoro Solis-Escalante (Corresponding Author), Joris van der Cruijsen, Digna de Kam, Joost van Kordelaar, Vivian Weerdesteyn, Alfred C. Schouten

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)
37 Downloads (Pure)

Abstract

The contributions of the cerebral cortex to human balance control are clearly demonstrated by the profound impact of cortical lesions on the ability to maintain standing balance. The cerebral cortex is thought to regulate subcortical postural centers to maintain upright balance and posture under varying environmental conditions and task demands. However, the cortical mechanisms that support standing balance remain elusive. Here, we present an EEG-based analysis of cortical oscillatory dynamics during the preparation and execution of balance responses with distinct postural demands. In our experiment, participants responded to backward movements of the support surface either with one forward step or by keeping their feet in place. To challenge the postural control system, we applied participant-specific high accelerations of the support surface such that the postural demand was low for stepping responses and high for feet-in-place responses. We expected that postural demand modulated the power of intrinsic cortical oscillations. Independent component analysis and time-frequency domain statistics revealed stronger suppression of alpha (9–13 Hz) and low-gamma (31–34 Hz) rhythms in the supplementary motor area (SMA) when preparing for feet-in-place responses (i.e., high postural demand). Irrespective of the response condition, support-surface movements elicited broadband (3–17 Hz) power increase in the SMA and enhancement of the theta (3–7 Hz) rhythm in the anterior prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral sensorimotor cortices (M1/S1). Although the execution of reactive responses resulted in largely similar cortical dynamics, comparison between the bilateral M1/S1 showed that stepping responses corresponded with stronger suppression of the beta (13–17 Hz) rhythm in the M1/S1 contralateral to the support leg. Comparison between response conditions showed that feet-in-place responses corresponded with stronger enhancement of the theta (3–7 Hz) rhythm in the PFC. Our results provide novel insights into the cortical dynamics of SMA, PFC, and M1/S1 during the control of human balance.

Original languageEnglish
Pages (from-to)557-571
Number of pages15
JournalNeuroImage
Volume188
DOIs
Publication statusPublished - 1 Mar 2019

Fingerprint

Foot
Motor Cortex
Prefrontal Cortex
Cerebral Cortex
Gyrus Cinguli
Posture
Electroencephalography
Leg

Keywords

  • UT-Hybrid-D
  • Electroencephalogram (EEG)
  • Independent component analysis (ICA)
  • Mobile brain/body imaging (MOBI)
  • Posture
  • Balance

Cite this

Solis-Escalante, Teodoro ; van der Cruijsen, Joris ; de Kam, Digna ; van Kordelaar, Joost ; Weerdesteyn, Vivian ; Schouten, Alfred C. / Cortical dynamics during preparation and execution of reactive balance responses with distinct postural demands. In: NeuroImage. 2019 ; Vol. 188. pp. 557-571.
@article{cf88f284f087418181a0783264d35dfd,
title = "Cortical dynamics during preparation and execution of reactive balance responses with distinct postural demands",
abstract = "The contributions of the cerebral cortex to human balance control are clearly demonstrated by the profound impact of cortical lesions on the ability to maintain standing balance. The cerebral cortex is thought to regulate subcortical postural centers to maintain upright balance and posture under varying environmental conditions and task demands. However, the cortical mechanisms that support standing balance remain elusive. Here, we present an EEG-based analysis of cortical oscillatory dynamics during the preparation and execution of balance responses with distinct postural demands. In our experiment, participants responded to backward movements of the support surface either with one forward step or by keeping their feet in place. To challenge the postural control system, we applied participant-specific high accelerations of the support surface such that the postural demand was low for stepping responses and high for feet-in-place responses. We expected that postural demand modulated the power of intrinsic cortical oscillations. Independent component analysis and time-frequency domain statistics revealed stronger suppression of alpha (9–13 Hz) and low-gamma (31–34 Hz) rhythms in the supplementary motor area (SMA) when preparing for feet-in-place responses (i.e., high postural demand). Irrespective of the response condition, support-surface movements elicited broadband (3–17 Hz) power increase in the SMA and enhancement of the theta (3–7 Hz) rhythm in the anterior prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral sensorimotor cortices (M1/S1). Although the execution of reactive responses resulted in largely similar cortical dynamics, comparison between the bilateral M1/S1 showed that stepping responses corresponded with stronger suppression of the beta (13–17 Hz) rhythm in the M1/S1 contralateral to the support leg. Comparison between response conditions showed that feet-in-place responses corresponded with stronger enhancement of the theta (3–7 Hz) rhythm in the PFC. Our results provide novel insights into the cortical dynamics of SMA, PFC, and M1/S1 during the control of human balance.",
keywords = "UT-Hybrid-D, Electroencephalogram (EEG), Independent component analysis (ICA), Mobile brain/body imaging (MOBI), Posture, Balance",
author = "Teodoro Solis-Escalante and {van der Cruijsen}, Joris and {de Kam}, Digna and {van Kordelaar}, Joost and Vivian Weerdesteyn and Schouten, {Alfred C.}",
note = "Elsevier deal",
year = "2019",
month = "3",
day = "1",
doi = "10.1016/j.neuroimage.2018.12.045",
language = "English",
volume = "188",
pages = "557--571",
journal = "NeuroImage",
issn = "1053-8119",
publisher = "Academic Press Inc.",

}

Cortical dynamics during preparation and execution of reactive balance responses with distinct postural demands. / Solis-Escalante, Teodoro (Corresponding Author); van der Cruijsen, Joris; de Kam, Digna; van Kordelaar, Joost; Weerdesteyn, Vivian; Schouten, Alfred C.

In: NeuroImage, Vol. 188, 01.03.2019, p. 557-571.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Cortical dynamics during preparation and execution of reactive balance responses with distinct postural demands

AU - Solis-Escalante, Teodoro

AU - van der Cruijsen, Joris

AU - de Kam, Digna

AU - van Kordelaar, Joost

AU - Weerdesteyn, Vivian

AU - Schouten, Alfred C.

N1 - Elsevier deal

PY - 2019/3/1

Y1 - 2019/3/1

N2 - The contributions of the cerebral cortex to human balance control are clearly demonstrated by the profound impact of cortical lesions on the ability to maintain standing balance. The cerebral cortex is thought to regulate subcortical postural centers to maintain upright balance and posture under varying environmental conditions and task demands. However, the cortical mechanisms that support standing balance remain elusive. Here, we present an EEG-based analysis of cortical oscillatory dynamics during the preparation and execution of balance responses with distinct postural demands. In our experiment, participants responded to backward movements of the support surface either with one forward step or by keeping their feet in place. To challenge the postural control system, we applied participant-specific high accelerations of the support surface such that the postural demand was low for stepping responses and high for feet-in-place responses. We expected that postural demand modulated the power of intrinsic cortical oscillations. Independent component analysis and time-frequency domain statistics revealed stronger suppression of alpha (9–13 Hz) and low-gamma (31–34 Hz) rhythms in the supplementary motor area (SMA) when preparing for feet-in-place responses (i.e., high postural demand). Irrespective of the response condition, support-surface movements elicited broadband (3–17 Hz) power increase in the SMA and enhancement of the theta (3–7 Hz) rhythm in the anterior prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral sensorimotor cortices (M1/S1). Although the execution of reactive responses resulted in largely similar cortical dynamics, comparison between the bilateral M1/S1 showed that stepping responses corresponded with stronger suppression of the beta (13–17 Hz) rhythm in the M1/S1 contralateral to the support leg. Comparison between response conditions showed that feet-in-place responses corresponded with stronger enhancement of the theta (3–7 Hz) rhythm in the PFC. Our results provide novel insights into the cortical dynamics of SMA, PFC, and M1/S1 during the control of human balance.

AB - The contributions of the cerebral cortex to human balance control are clearly demonstrated by the profound impact of cortical lesions on the ability to maintain standing balance. The cerebral cortex is thought to regulate subcortical postural centers to maintain upright balance and posture under varying environmental conditions and task demands. However, the cortical mechanisms that support standing balance remain elusive. Here, we present an EEG-based analysis of cortical oscillatory dynamics during the preparation and execution of balance responses with distinct postural demands. In our experiment, participants responded to backward movements of the support surface either with one forward step or by keeping their feet in place. To challenge the postural control system, we applied participant-specific high accelerations of the support surface such that the postural demand was low for stepping responses and high for feet-in-place responses. We expected that postural demand modulated the power of intrinsic cortical oscillations. Independent component analysis and time-frequency domain statistics revealed stronger suppression of alpha (9–13 Hz) and low-gamma (31–34 Hz) rhythms in the supplementary motor area (SMA) when preparing for feet-in-place responses (i.e., high postural demand). Irrespective of the response condition, support-surface movements elicited broadband (3–17 Hz) power increase in the SMA and enhancement of the theta (3–7 Hz) rhythm in the anterior prefrontal cortex (PFC), anterior cingulate cortex (ACC), and bilateral sensorimotor cortices (M1/S1). Although the execution of reactive responses resulted in largely similar cortical dynamics, comparison between the bilateral M1/S1 showed that stepping responses corresponded with stronger suppression of the beta (13–17 Hz) rhythm in the M1/S1 contralateral to the support leg. Comparison between response conditions showed that feet-in-place responses corresponded with stronger enhancement of the theta (3–7 Hz) rhythm in the PFC. Our results provide novel insights into the cortical dynamics of SMA, PFC, and M1/S1 during the control of human balance.

KW - UT-Hybrid-D

KW - Electroencephalogram (EEG)

KW - Independent component analysis (ICA)

KW - Mobile brain/body imaging (MOBI)

KW - Posture

KW - Balance

UR - http://www.scopus.com/inward/record.url?scp=85059128266&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2018.12.045

DO - 10.1016/j.neuroimage.2018.12.045

M3 - Article

VL - 188

SP - 557

EP - 571

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -