Resting-State Phase-Amplitude Coupling Between the Human Subthalamic Nucleus and Cortical Activity: A Simultaneous Intracranial and Scalp EEG Study

Damborská, Alena; Lamoš, Martin; Brunet, Denis; Vulliemoz, Serge; Bočková, Martina; Deutschová, Barbora; Baláž, Marek; Rektor, Ivan

doi:10.1007/s10548-021-00822-8

Original Paper
Published: 29 January 2021

Resting-State Phase-Amplitude Coupling Between the Human Subthalamic Nucleus and Cortical Activity: A Simultaneous Intracranial and Scalp EEG Study

Alena Damborská ORCID: orcid.org/0000-0002-9714-7441^1,2,6,
Martin Lamoš¹,
Denis Brunet^2,3,
Serge Vulliemoz^3,4,
Martina Bočková^1,5,
Barbora Deutschová^1,5,
Marek Baláž⁵ &
Ivan Rektor^1,5

Brain Topography volume 34, pages 272–282 (2021)Cite this article

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Abstract

It has been suggested that slow oscillations in the subthalamic nucleus (STN) reflect top-down inputs from the medial prefrontal cortex, thus implementing behavior control. It is unclear, however, whether the STN oscillations are related to cortical activity in a bottom-up manner. To assess resting-state subcortico-cortical interactions, we recorded simultaneous scalp electroencephalographic activity and local field potentials in the STN (LFP-STN) in 11 patients with Parkinson’s disease implanted with deep brain stimulation electrodes in the on-medication state during rest. We assessed the cross-structural phase-amplitude coupling (PAC) between the STN and cortical activity within a wide frequency range of 1 to 100 Hz. The PAC was dominant between the δ/θ STN phase and β/γ cortical amplitude in most investigated scalp regions and between the δ cortical phase and θ/α STN amplitude in the frontal and temporal regions. The cross-frequency linkage between the slow oscillations of the LFP-STN activity and the amplitude of the scalp-recorded cortical activity at rest was demonstrated, and similar involvement of the left and right STNs in the coupling was observed. Our results suggest that the STN plays a role in both bottom-up and top-down processes within the subcortico-cortical circuitries of the human brain during the resting state. A relative left–right symmetry in the STN-cortex functional linkage was suggested. Practical treatment studies would be necessary to assess whether unilateral stimulation of the STN might be sufficient for treatment of Parkinson’s disease.

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Availability of Data and Material

The data and material that support the findings of this study are available from the corresponding author upon reasonable request.

Code Availability

The custom in-house MATLAB code is available from the corresponding author upon reasonable request. CARTOOL software by Denis Brunet is freely available https://sites.google.com/site/fbmlab/home.

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Acknowledgements

The authors wish to thank Anne Johnson for providing language help.

Funding

The study was financially supported by the Czech Science Foundation Grant 21-25953S, by Grants FNS 192749 and CRSII5_170873, and by the Ministry of Education, Youth and Sports of the Czech Republic within the CEITEC 2020 (LQ1601) project.

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Authors and Affiliations

CEITEC – Central European Institute of Technology, Masaryk University, Brno, Czech Republic
Alena Damborská, Martin Lamoš, Martina Bočková, Barbora Deutschová & Ivan Rektor
Functional Brain Mapping Lab, University of Geneva, Geneva, Switzerland
Alena Damborská & Denis Brunet
CIBM – Center for Biomedical Imaging, Geneva, Switzerland
Denis Brunet & Serge Vulliemoz
EEG and Epilepsy Unit, Neurology, University Hospital and Faculty of Medicine, Geneva, Switzerland
Serge Vulliemoz
First Department of Neurology, St. Anne’s University Hospital, Masaryk University, Brno, Czech Republic
Martina Bočková, Barbora Deutschová, Marek Baláž & Ivan Rektor
CEITEC – Central European Institute of Technology, Brain and Mind Research Program, Masaryk University, Kamenice 753/5, 625 00, Brno, Czech Republic
Alena Damborská

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Alena Damborská
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Martin Lamoš
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Denis Brunet
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Serge Vulliemoz
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Martina Bočková
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Barbora Deutschová
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Marek Baláž
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Ivan Rektor
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Contributions

A.D. designed the study, collected and pre-processed the data, and wrote the initial draft of the manuscript. M.L. analyzed the data. D.B. and S.V. served as consultants for the data analysis and clinical issues, respectively. B.D., M.Ba, and M.Bo collected the data. I.R. developed the initial idea. All authors reviewed the manuscript.

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Correspondence to Alena Damborská.

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All participants gave their written informed consent prior to the experiment and the study received the approval of the ethics committee of St. Anne’s Hospital in Brno. All experiments in this study were performed in accordance with relevant guidelines and regulations.

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10548_2021_822_MOESM1_ESM.png

Supplementary material 1 (PNG 854 kb) Supplementary Figure 1. Organization of selected scalp electrodes into regional sets. The data from 53 electrodes were pooled into 13 regions: Frontal-Left, Temporal-Left, Central-Left, Parietal-Left, Occipital-Left, Frontal-Right, Temporal-Right, Central-Right, Parietal-Right, Occipital-Right, Frontal, Parietal, Occipital

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Damborská, A., Lamoš, M., Brunet, D. et al. Resting-State Phase-Amplitude Coupling Between the Human Subthalamic Nucleus and Cortical Activity: A Simultaneous Intracranial and Scalp EEG Study. Brain Topogr 34, 272–282 (2021). https://doi.org/10.1007/s10548-021-00822-8

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Received: 19 November 2020
Accepted: 18 January 2021
Published: 29 January 2021
Issue Date: May 2021
DOI: https://doi.org/10.1007/s10548-021-00822-8

Keywords

Subthalamic nucleus
Subcortico-cortical interactions
Phase-amplitude coupling
Cross-structural coupling
Simultaneous intracranial and scalp EEG