Cognitive effects of theta frequency bilateral subthalamic nucleus stimulation in Parkinson's disease: A pilot study.


Journal

Brain stimulation
ISSN: 1876-4754
Titre abrégé: Brain Stimul
Pays: United States
ID NLM: 101465726

Informations de publication

Date de publication:
Historique:
received: 13 06 2020
revised: 12 11 2020
accepted: 28 12 2020
pubmed: 9 1 2021
medline: 5 10 2021
entrez: 8 1 2021
Statut: ppublish

Résumé

There is significant evidence for cognitive decline following deep brain stimulation (DBS). Current stimulation paradigms utilize gamma frequency stimulation for optimal motor benefits; however, little has been done to optimize stimulation parameters for cognition. Recent evidence implicates subthalamic nucleus (STN) theta oscillations in executive function, and theta oscillations are well-known to relate to episodic memory, suggesting that theta frequency stimulation could potentially improve cognition in Parkinson's disease (PD). To evaluate the acute effects of theta frequency bilateral STN stimulation on executive function in PD versus gamma frequency and off, as well as investigate the differential effects on episodic versus nonepisodic verbal fluency. Twelve patients (all males, mean age 60.8) with bilateral STN DBS for PD underwent a double-blinded, randomized cognitive testing during stimulation at (1) 130-135 Hz (gamma), (2) 10 Hz (theta) and (3) off. Executive functions and processing speed were evaluated using verbal fluency tasks (letter, episodic category, nonepisodic category, and category switching), color-word interference task, and random number generation task. Performance at each stimulation frequency was compared within subjects. Theta frequency significantly improved episodic category fluency compared to gamma, but not compared to off. There were no significant differences between stimulation frequencies in other tests. In this pilot trial, our results corroborate the role of theta oscillations in episodic retrieval, although it is unclear whether this reflects direct modulation of the medial temporal lobe and whether similar effects can be found with more canonical memory paradigms. Further work is necessary to corroborate our findings and investigate the possibility of interleaving theta and gamma frequency stimulation for concomitant motor and cognitive effects.

Sections du résumé

BACKGROUND
There is significant evidence for cognitive decline following deep brain stimulation (DBS). Current stimulation paradigms utilize gamma frequency stimulation for optimal motor benefits; however, little has been done to optimize stimulation parameters for cognition. Recent evidence implicates subthalamic nucleus (STN) theta oscillations in executive function, and theta oscillations are well-known to relate to episodic memory, suggesting that theta frequency stimulation could potentially improve cognition in Parkinson's disease (PD).
OBJECTIVE
To evaluate the acute effects of theta frequency bilateral STN stimulation on executive function in PD versus gamma frequency and off, as well as investigate the differential effects on episodic versus nonepisodic verbal fluency.
METHODS
Twelve patients (all males, mean age 60.8) with bilateral STN DBS for PD underwent a double-blinded, randomized cognitive testing during stimulation at (1) 130-135 Hz (gamma), (2) 10 Hz (theta) and (3) off. Executive functions and processing speed were evaluated using verbal fluency tasks (letter, episodic category, nonepisodic category, and category switching), color-word interference task, and random number generation task. Performance at each stimulation frequency was compared within subjects.
RESULTS
Theta frequency significantly improved episodic category fluency compared to gamma, but not compared to off. There were no significant differences between stimulation frequencies in other tests.
CONCLUSION
In this pilot trial, our results corroborate the role of theta oscillations in episodic retrieval, although it is unclear whether this reflects direct modulation of the medial temporal lobe and whether similar effects can be found with more canonical memory paradigms. Further work is necessary to corroborate our findings and investigate the possibility of interleaving theta and gamma frequency stimulation for concomitant motor and cognitive effects.

Identifiants

pubmed: 33418095
pii: S1935-861X(20)30317-X
doi: 10.1016/j.brs.2020.12.014
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

230-240

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest There are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

Auteurs

Jordan Lam (J)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States.

Justin Lee (J)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States.

Marcus Williams (M)

King's College London Medical School, London, United Kingdom.

Melanie Cohn (M)

Department of Psychology, University of Toronto, Toronto, Canada; Krembil Brain Institute, University Health Network, Toronto, Canada.

Melissa Wilson (M)

Department of Preventive Medicine, Keck School of Medicine of USC, Los Angeles, United States.

Catherine Mark (C)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States.

Nasrin Esnaashari (N)

Department of Neurology, Keck School of Medicine of USC, Los Angeles, United States.

Andrew Petkus (A)

Department of Neurology, Keck School of Medicine of USC, Los Angeles, United States.

Jennifer Hui (J)

Department of Neurology, Keck School of Medicine of USC, Los Angeles, United States.

Danielle Feigenbaum (D)

Department of Neurology, Keck School of Medicine of USC, Los Angeles, United States.

Mark Liker (M)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States.

Charles Y Liu (CY)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States.

Brian Lee (B)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States.

Darrin J Lee (DJ)

Department of Neurological Surgery, Keck School of Medicine of USC, Los Angeles, United States; USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, United States. Electronic address: Darrin.lee@med.usc.edu.

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