Hypersynchrony despite pathologically reduced beta oscillations in patients with Parkinson’s disease

A pharmaco-magnetoencephalography study

Elizabeth C Heinrichs-Graham, Max J Kurz, Katherine M. Becker, Pamela M. Santamaria, Howard Eliot Gendelman, Tony W Wilson

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Parkinson’s disease (PD) is a progressive debilitating neurodegenerative disorder clinically manifest by motor, posture and gait abnormalities. Human neurophysiological studies recording local field potentials within the subthalamic nucleus and scalp-based electroencephalography have shown pathological beta synchrony throughout the basal ganglia-thalamic-cortical motor network in PD. Notably, suppression of this pathological beta synchrony by dopamine replacement therapy or deep-brain stimulation has been associated with improved motor function. However, due to the invasive nature of these studies, it remains unknown whether this “pathological beta” is actually stronger than that observed in healthy demographically matched controls. We used magnetoencephalography to investigate neuronal synchrony and oscillatory amplitude in the beta range and lower frequencies during the resting state in patients with PD and a matched group of patients without neurological disease. Patients with PD were studied both in the practically defined drug “OFF” state, and after administration of dopamine replacements. We found that beta oscillatory amplitude was reduced bilaterally in the primary motor regions of unmedicated patients with PD compared with controls. Administration of dopaminergic medications significantly increased beta oscillatory activity, thus having a normalizing effect. Interestingly, we also found significantly stronger beta synchrony (i.e., hypersynchrony) between the primary motor regions in unmedicated patients with PD compared with controls, and that medication reduced this coupling which is in agreement with the intraoperative studies. These results are consistent with the known functionality of the basal ganglia-thalamic-cortical motor circuit and the likely consequences of beta hypersynchrony in the subthalamic nucleus of patients with PD.

Original languageEnglish (US)
Pages (from-to)1739-1747
Number of pages9
JournalJournal of Neurophysiology
Volume112
Issue number7
DOIs
StatePublished - Oct 1 2014

Fingerprint

Magnetoencephalography
Parkinson Disease
Subthalamic Nucleus
Basal Ganglia
Dopamine
Deep Brain Stimulation
Scalp
Posture
Gait
Neurodegenerative Diseases
Electroencephalography
Research Design
Pharmaceutical Preparations

Keywords

  • Cortex
  • MEG
  • Magnetoencephalography
  • Oscillations
  • Resting state

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

Cite this

@article{1ecc44c0f63044069c45a353b33e2859,
title = "Hypersynchrony despite pathologically reduced beta oscillations in patients with Parkinson’s disease: A pharmaco-magnetoencephalography study",
abstract = "Parkinson’s disease (PD) is a progressive debilitating neurodegenerative disorder clinically manifest by motor, posture and gait abnormalities. Human neurophysiological studies recording local field potentials within the subthalamic nucleus and scalp-based electroencephalography have shown pathological beta synchrony throughout the basal ganglia-thalamic-cortical motor network in PD. Notably, suppression of this pathological beta synchrony by dopamine replacement therapy or deep-brain stimulation has been associated with improved motor function. However, due to the invasive nature of these studies, it remains unknown whether this “pathological beta” is actually stronger than that observed in healthy demographically matched controls. We used magnetoencephalography to investigate neuronal synchrony and oscillatory amplitude in the beta range and lower frequencies during the resting state in patients with PD and a matched group of patients without neurological disease. Patients with PD were studied both in the practically defined drug “OFF” state, and after administration of dopamine replacements. We found that beta oscillatory amplitude was reduced bilaterally in the primary motor regions of unmedicated patients with PD compared with controls. Administration of dopaminergic medications significantly increased beta oscillatory activity, thus having a normalizing effect. Interestingly, we also found significantly stronger beta synchrony (i.e., hypersynchrony) between the primary motor regions in unmedicated patients with PD compared with controls, and that medication reduced this coupling which is in agreement with the intraoperative studies. These results are consistent with the known functionality of the basal ganglia-thalamic-cortical motor circuit and the likely consequences of beta hypersynchrony in the subthalamic nucleus of patients with PD.",
keywords = "Cortex, MEG, Magnetoencephalography, Oscillations, Resting state",
author = "Heinrichs-Graham, {Elizabeth C} and Kurz, {Max J} and Becker, {Katherine M.} and Santamaria, {Pamela M.} and Gendelman, {Howard Eliot} and Wilson, {Tony W}",
year = "2014",
month = "10",
day = "1",
doi = "10.1152/jn.00383.2014",
language = "English (US)",
volume = "112",
pages = "1739--1747",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "7",

}

TY - JOUR

T1 - Hypersynchrony despite pathologically reduced beta oscillations in patients with Parkinson’s disease

T2 - A pharmaco-magnetoencephalography study

AU - Heinrichs-Graham, Elizabeth C

AU - Kurz, Max J

AU - Becker, Katherine M.

AU - Santamaria, Pamela M.

AU - Gendelman, Howard Eliot

AU - Wilson, Tony W

PY - 2014/10/1

Y1 - 2014/10/1

N2 - Parkinson’s disease (PD) is a progressive debilitating neurodegenerative disorder clinically manifest by motor, posture and gait abnormalities. Human neurophysiological studies recording local field potentials within the subthalamic nucleus and scalp-based electroencephalography have shown pathological beta synchrony throughout the basal ganglia-thalamic-cortical motor network in PD. Notably, suppression of this pathological beta synchrony by dopamine replacement therapy or deep-brain stimulation has been associated with improved motor function. However, due to the invasive nature of these studies, it remains unknown whether this “pathological beta” is actually stronger than that observed in healthy demographically matched controls. We used magnetoencephalography to investigate neuronal synchrony and oscillatory amplitude in the beta range and lower frequencies during the resting state in patients with PD and a matched group of patients without neurological disease. Patients with PD were studied both in the practically defined drug “OFF” state, and after administration of dopamine replacements. We found that beta oscillatory amplitude was reduced bilaterally in the primary motor regions of unmedicated patients with PD compared with controls. Administration of dopaminergic medications significantly increased beta oscillatory activity, thus having a normalizing effect. Interestingly, we also found significantly stronger beta synchrony (i.e., hypersynchrony) between the primary motor regions in unmedicated patients with PD compared with controls, and that medication reduced this coupling which is in agreement with the intraoperative studies. These results are consistent with the known functionality of the basal ganglia-thalamic-cortical motor circuit and the likely consequences of beta hypersynchrony in the subthalamic nucleus of patients with PD.

AB - Parkinson’s disease (PD) is a progressive debilitating neurodegenerative disorder clinically manifest by motor, posture and gait abnormalities. Human neurophysiological studies recording local field potentials within the subthalamic nucleus and scalp-based electroencephalography have shown pathological beta synchrony throughout the basal ganglia-thalamic-cortical motor network in PD. Notably, suppression of this pathological beta synchrony by dopamine replacement therapy or deep-brain stimulation has been associated with improved motor function. However, due to the invasive nature of these studies, it remains unknown whether this “pathological beta” is actually stronger than that observed in healthy demographically matched controls. We used magnetoencephalography to investigate neuronal synchrony and oscillatory amplitude in the beta range and lower frequencies during the resting state in patients with PD and a matched group of patients without neurological disease. Patients with PD were studied both in the practically defined drug “OFF” state, and after administration of dopamine replacements. We found that beta oscillatory amplitude was reduced bilaterally in the primary motor regions of unmedicated patients with PD compared with controls. Administration of dopaminergic medications significantly increased beta oscillatory activity, thus having a normalizing effect. Interestingly, we also found significantly stronger beta synchrony (i.e., hypersynchrony) between the primary motor regions in unmedicated patients with PD compared with controls, and that medication reduced this coupling which is in agreement with the intraoperative studies. These results are consistent with the known functionality of the basal ganglia-thalamic-cortical motor circuit and the likely consequences of beta hypersynchrony in the subthalamic nucleus of patients with PD.

KW - Cortex

KW - MEG

KW - Magnetoencephalography

KW - Oscillations

KW - Resting state

UR - http://www.scopus.com/inward/record.url?scp=84907540570&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84907540570&partnerID=8YFLogxK

U2 - 10.1152/jn.00383.2014

DO - 10.1152/jn.00383.2014

M3 - Article

VL - 112

SP - 1739

EP - 1747

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 7

ER -