Nonlinear interactions in the thalamocortical loop in essential tremor: A model-based frequency domain analysis

F. He, P. G. Sarrigiannis, S. A. Billings, H. Wei, J. Rowe, C. Romanowski, N. Hoggard, M. Hadjivassilliou, D. G. Rao, R. Grünewald, A. Khan, J. Yianni

Research output: Contribution to journalArticle

6 Citations (Scopus)
20 Downloads (Pure)

Abstract

There is increasing evidence to suggest that essential tremor has a central origin. Different structures appear to be part of the central tremorogenic network, including the motor cortex, the thalamus and the cerebellum. Some studies using electroencephalogram (EEG) and magnetoencephalography (MEG) show linear association in the tremor frequency between the motor cortex and the contralateral tremor electromyography (EMG). Additionally, high thalamomuscular coherence is found with the use of thalamic local field potential (LFP) recordings and tremulous EMG in patients undergoing surgery for deep brain stimulation (DBS). Despite a well-established reciprocal anatomical connection between the thalamus and cortex, the functional association between the two structures during "tremor-on" periods remains elusive. Thalamic (Vim) LFPs, ipsilateral scalp EEG from the sensorimotor cortex and contralateral tremor arm EMG recordings were obtained from two patients with essential tremor who had undergone successful surgery for DBS. Coherence analysis shows a strong linear association between thalamic LFPs and contralateral tremor EMG, but the relationship between the EEG and the thalamus is much less clear. These measurements were then analyzed by constructing a novel parametric nonlinear autoregressive with exogenous input (NARX) model. This new approach uncovered two distinct and not overlapping frequency "channels" of communication between Vim thalamus and the ipsilateral motor cortex, defining robustly "tremor-on" versus "tremor-off" states. The associated estimated nonlinear time lags also showed non-overlapping values between the two states, with longer corticothalamic lags (exceeding 50 ms) in the tremor active state, suggesting involvement of an indirect multisynaptic loop. The results reveal the importance of the nonlinear interactions between cortical and subcortical areas in the central motor network of essential tremor. This work is important because it demonstrates for the first time that in essential tremor the functional interrelationships between the cortex and thalamus should not be sought exclusively within individual frequencies but more importantly between cross-frequency nonlinear interactions. Should our results be successfully reproduced on a bigger cohort of patients with essential tremor, our approach could be used to create an on-demand closed-loop DBS device, able to automatically activate when the tremor is on.

Original languageEnglish
Pages (from-to)377-389
Number of pages13
JournalNeuroscience
Volume324
Early online date14 Mar 2016
DOIs
Publication statusPublished - 2 Jun 2016
Externally publishedYes

Fingerprint

Essential Tremor
Tremor
Thalamus
Electromyography
Deep Brain Stimulation
Motor Cortex
Electroencephalography
Magnetoencephalography
Scalp
Cerebellum
Arm
Communication
Equipment and Supplies

Bibliographical note

© 2017, Elsevier. Licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/

Copyright © and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders.

Keywords

  • Coherence
  • EEG
  • Essential tremor
  • Local field potentials
  • Nonlinear modeling
  • Spectral analysis

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Nonlinear interactions in the thalamocortical loop in essential tremor : A model-based frequency domain analysis. / He, F.; Sarrigiannis, P. G.; Billings, S. A.; Wei, H.; Rowe, J.; Romanowski, C.; Hoggard, N.; Hadjivassilliou, M.; Rao, D. G.; Grünewald, R.; Khan, A.; Yianni, J.

In: Neuroscience, Vol. 324, 02.06.2016, p. 377-389.

Research output: Contribution to journalArticle

He, F, Sarrigiannis, PG, Billings, SA, Wei, H, Rowe, J, Romanowski, C, Hoggard, N, Hadjivassilliou, M, Rao, DG, Grünewald, R, Khan, A & Yianni, J 2016, 'Nonlinear interactions in the thalamocortical loop in essential tremor: A model-based frequency domain analysis' Neuroscience, vol. 324, pp. 377-389. https://doi.org/10.1016/j.neuroscience.2016.03.028
He, F. ; Sarrigiannis, P. G. ; Billings, S. A. ; Wei, H. ; Rowe, J. ; Romanowski, C. ; Hoggard, N. ; Hadjivassilliou, M. ; Rao, D. G. ; Grünewald, R. ; Khan, A. ; Yianni, J. / Nonlinear interactions in the thalamocortical loop in essential tremor : A model-based frequency domain analysis. In: Neuroscience. 2016 ; Vol. 324. pp. 377-389.
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