Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation

Kyle Joseph Edmunds, Hannes Petersen, Mahmoud Hassan, Sahar Yassine, Antonella Olivieri, Fabio Barollo, Rún Friðriksdóttir, Patricia Edmunds, Magnús Gíslason, Antonio Fratini, Paolo Gargiulo

Research output: Contribution to journalArticle

Abstract

Objective. Maintaining upright posture is a complex task governed by the integration of afferent sensorimotor and visual information with compensatory neuromuscular reactions. The objective of the present work was to characterize the visual dependency and functional dynamics of cortical activation during postural control. Approach. Proprioceptic vibratory stimulation of calf muscles at 85 Hz was performed to evoke postural perturbation in open-eye (OE) and closed-eye (CE) experimental trials, with pseudorandom binary stimulation phases divided into four segments of 16 stimuli. 64-channel EEG was recorded at 512 Hz, with perturbation epochs defined using bipolar electrodes placed proximal to each vibrator. Power spectra variation and linearity analysis was performed via fast Fourier transformation into six frequency bands (Δ, 0.5–3.5 Hz; θ, 3.5–7.5 Hz; α, 7.5–12.5 Hz; β, 12.5–30 Hz; γlow, 30–50 Hz; and γhigh, 50–80 Hz). Finally, functional connectivity assessment was explored via network segregation and integration analyses. Main results. Spectra variation showed waveform and vision-dependent activation within cortical regions specific to both postural adaptation and habituation. Generalized spectral variation yielded significant shifts from low to high frequencies in CE adaptation trials, with overall activity suppressed in habituation; OE trials showed the opposite phenomenon, with both adaptation and habituation yielding increases in spectral power. Finally, our analysis of functional dynamics reveals novel cortical networks implicated in postural control using EEG source-space brain networks. In particular, our reported significant increase in local θ connectivity May signify the planning of corrective steps and/or the analysis of falling consequences, while α band network integration results reflect an inhibition of error detection within the cingulate cortex, likely due to habituation. Significance. Our findings principally suggest that specific cortical waveforms are dependent upon the availability of visual feedback, and we furthermore present the first evidence that local and global brain networks undergo characteristic modification during postural control.

Original languageEnglish
Article number026037
JournalJournal of Neural Engineering
Volume16
Issue number2
Early online date12 Feb 2019
DOIs
Publication statusPublished - 13 Mar 2019

Fingerprint

Electroencephalography
Brain
Functional assessment
Chemical activation
Vibrators
Error detection
Power spectrum
Sensory Feedback
Frequency bands
Muscle
Gyrus Cinguli
Posture
Availability
Feedback
Planning
Electrodes
Muscles
Dependency (Psychology)
Power (Psychology)
Inhibition (Psychology)

Bibliographical note

©2019 IOP Publishing Ltd. After the Embargo Period, the full text of the Accepted Manuscript may be made available on the non-commercial repository for anyone with an internet connection to read and download. After the Embargo Period a CC BY-NC-ND 3.0 licence applies to the Accepted Manuscript, in which case it may then only be posted under that CC BY-NC-ND licence provided that all the terms of the licence are adhered to, and any copyright notice and any cover sheet applied by IOP is not deleted or modified.

Keywords

  • EEG
  • Functional connectivity
  • Power spectral density
  • Proprioceptive stimulation
  • Vertical posture

Cite this

Edmunds, Kyle Joseph ; Petersen, Hannes ; Hassan, Mahmoud ; Yassine, Sahar ; Olivieri, Antonella ; Barollo, Fabio ; Friðriksdóttir, Rún ; Edmunds, Patricia ; Gíslason, Magnús ; Fratini, Antonio ; Gargiulo, Paolo. / Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation. In: Journal of Neural Engineering. 2019 ; Vol. 16, No. 2.
@article{1027a1f9e13a42f694352a44b0fbda82,
title = "Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation",
abstract = "Objective. Maintaining upright posture is a complex task governed by the integration of afferent sensorimotor and visual information with compensatory neuromuscular reactions. The objective of the present work was to characterize the visual dependency and functional dynamics of cortical activation during postural control. Approach. Proprioceptic vibratory stimulation of calf muscles at 85 Hz was performed to evoke postural perturbation in open-eye (OE) and closed-eye (CE) experimental trials, with pseudorandom binary stimulation phases divided into four segments of 16 stimuli. 64-channel EEG was recorded at 512 Hz, with perturbation epochs defined using bipolar electrodes placed proximal to each vibrator. Power spectra variation and linearity analysis was performed via fast Fourier transformation into six frequency bands (Δ, 0.5–3.5 Hz; θ, 3.5–7.5 Hz; α, 7.5–12.5 Hz; β, 12.5–30 Hz; γlow, 30–50 Hz; and γhigh, 50–80 Hz). Finally, functional connectivity assessment was explored via network segregation and integration analyses. Main results. Spectra variation showed waveform and vision-dependent activation within cortical regions specific to both postural adaptation and habituation. Generalized spectral variation yielded significant shifts from low to high frequencies in CE adaptation trials, with overall activity suppressed in habituation; OE trials showed the opposite phenomenon, with both adaptation and habituation yielding increases in spectral power. Finally, our analysis of functional dynamics reveals novel cortical networks implicated in postural control using EEG source-space brain networks. In particular, our reported significant increase in local θ connectivity May signify the planning of corrective steps and/or the analysis of falling consequences, while α band network integration results reflect an inhibition of error detection within the cingulate cortex, likely due to habituation. Significance. Our findings principally suggest that specific cortical waveforms are dependent upon the availability of visual feedback, and we furthermore present the first evidence that local and global brain networks undergo characteristic modification during postural control.",
keywords = "EEG, Functional connectivity, Power spectral density, Proprioceptive stimulation, Vertical posture",
author = "Edmunds, {Kyle Joseph} and Hannes Petersen and Mahmoud Hassan and Sahar Yassine and Antonella Olivieri and Fabio Barollo and R{\'u}n Fri{\dh}riksd{\'o}ttir and Patricia Edmunds and Magn{\'u}s G{\'i}slason and Antonio Fratini and Paolo Gargiulo",
note = "{\circledC}2019 IOP Publishing Ltd. After the Embargo Period, the full text of the Accepted Manuscript may be made available on the non-commercial repository for anyone with an internet connection to read and download. After the Embargo Period a CC BY-NC-ND 3.0 licence applies to the Accepted Manuscript, in which case it may then only be posted under that CC BY-NC-ND licence provided that all the terms of the licence are adhered to, and any copyright notice and any cover sheet applied by IOP is not deleted or modified.",
year = "2019",
month = "3",
day = "13",
doi = "10.1088/1741-2552/ab0678",
language = "English",
volume = "16",
journal = "Journal of Neural Engineering",
issn = "1741-2560",
publisher = "IOP Publishing Ltd.",
number = "2",

}

Edmunds, KJ, Petersen, H, Hassan, M, Yassine, S, Olivieri, A, Barollo, F, Friðriksdóttir, R, Edmunds, P, Gíslason, M, Fratini, A & Gargiulo, P 2019, 'Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation', Journal of Neural Engineering, vol. 16, no. 2, 026037. https://doi.org/10.1088/1741-2552/ab0678

Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation. / Edmunds, Kyle Joseph; Petersen, Hannes; Hassan, Mahmoud; Yassine, Sahar; Olivieri, Antonella; Barollo, Fabio; Friðriksdóttir, Rún; Edmunds, Patricia; Gíslason, Magnús; Fratini, Antonio; Gargiulo, Paolo.

In: Journal of Neural Engineering, Vol. 16, No. 2, 026037, 13.03.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Cortical recruitment and functional dynamics in postural control adaptation and habituation during vibratory proprioceptive stimulation

AU - Edmunds, Kyle Joseph

AU - Petersen, Hannes

AU - Hassan, Mahmoud

AU - Yassine, Sahar

AU - Olivieri, Antonella

AU - Barollo, Fabio

AU - Friðriksdóttir, Rún

AU - Edmunds, Patricia

AU - Gíslason, Magnús

AU - Fratini, Antonio

AU - Gargiulo, Paolo

N1 - ©2019 IOP Publishing Ltd. After the Embargo Period, the full text of the Accepted Manuscript may be made available on the non-commercial repository for anyone with an internet connection to read and download. After the Embargo Period a CC BY-NC-ND 3.0 licence applies to the Accepted Manuscript, in which case it may then only be posted under that CC BY-NC-ND licence provided that all the terms of the licence are adhered to, and any copyright notice and any cover sheet applied by IOP is not deleted or modified.

PY - 2019/3/13

Y1 - 2019/3/13

N2 - Objective. Maintaining upright posture is a complex task governed by the integration of afferent sensorimotor and visual information with compensatory neuromuscular reactions. The objective of the present work was to characterize the visual dependency and functional dynamics of cortical activation during postural control. Approach. Proprioceptic vibratory stimulation of calf muscles at 85 Hz was performed to evoke postural perturbation in open-eye (OE) and closed-eye (CE) experimental trials, with pseudorandom binary stimulation phases divided into four segments of 16 stimuli. 64-channel EEG was recorded at 512 Hz, with perturbation epochs defined using bipolar electrodes placed proximal to each vibrator. Power spectra variation and linearity analysis was performed via fast Fourier transformation into six frequency bands (Δ, 0.5–3.5 Hz; θ, 3.5–7.5 Hz; α, 7.5–12.5 Hz; β, 12.5–30 Hz; γlow, 30–50 Hz; and γhigh, 50–80 Hz). Finally, functional connectivity assessment was explored via network segregation and integration analyses. Main results. Spectra variation showed waveform and vision-dependent activation within cortical regions specific to both postural adaptation and habituation. Generalized spectral variation yielded significant shifts from low to high frequencies in CE adaptation trials, with overall activity suppressed in habituation; OE trials showed the opposite phenomenon, with both adaptation and habituation yielding increases in spectral power. Finally, our analysis of functional dynamics reveals novel cortical networks implicated in postural control using EEG source-space brain networks. In particular, our reported significant increase in local θ connectivity May signify the planning of corrective steps and/or the analysis of falling consequences, while α band network integration results reflect an inhibition of error detection within the cingulate cortex, likely due to habituation. Significance. Our findings principally suggest that specific cortical waveforms are dependent upon the availability of visual feedback, and we furthermore present the first evidence that local and global brain networks undergo characteristic modification during postural control.

AB - Objective. Maintaining upright posture is a complex task governed by the integration of afferent sensorimotor and visual information with compensatory neuromuscular reactions. The objective of the present work was to characterize the visual dependency and functional dynamics of cortical activation during postural control. Approach. Proprioceptic vibratory stimulation of calf muscles at 85 Hz was performed to evoke postural perturbation in open-eye (OE) and closed-eye (CE) experimental trials, with pseudorandom binary stimulation phases divided into four segments of 16 stimuli. 64-channel EEG was recorded at 512 Hz, with perturbation epochs defined using bipolar electrodes placed proximal to each vibrator. Power spectra variation and linearity analysis was performed via fast Fourier transformation into six frequency bands (Δ, 0.5–3.5 Hz; θ, 3.5–7.5 Hz; α, 7.5–12.5 Hz; β, 12.5–30 Hz; γlow, 30–50 Hz; and γhigh, 50–80 Hz). Finally, functional connectivity assessment was explored via network segregation and integration analyses. Main results. Spectra variation showed waveform and vision-dependent activation within cortical regions specific to both postural adaptation and habituation. Generalized spectral variation yielded significant shifts from low to high frequencies in CE adaptation trials, with overall activity suppressed in habituation; OE trials showed the opposite phenomenon, with both adaptation and habituation yielding increases in spectral power. Finally, our analysis of functional dynamics reveals novel cortical networks implicated in postural control using EEG source-space brain networks. In particular, our reported significant increase in local θ connectivity May signify the planning of corrective steps and/or the analysis of falling consequences, while α band network integration results reflect an inhibition of error detection within the cingulate cortex, likely due to habituation. Significance. Our findings principally suggest that specific cortical waveforms are dependent upon the availability of visual feedback, and we furthermore present the first evidence that local and global brain networks undergo characteristic modification during postural control.

KW - EEG

KW - Functional connectivity

KW - Power spectral density

KW - Proprioceptive stimulation

KW - Vertical posture

UR - http://iopscience.iop.org/article/10.1088/1741-2552/ab0678

UR - http://www.scopus.com/inward/record.url?scp=85062848033&partnerID=8YFLogxK

U2 - 10.1088/1741-2552/ab0678

DO - 10.1088/1741-2552/ab0678

M3 - Article

VL - 16

JO - Journal of Neural Engineering

JF - Journal of Neural Engineering

SN - 1741-2560

IS - 2

M1 - 026037

ER -