Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease.

Parkinson disease basal ganglia thalamocortical network beta oscillations local field potential self-initiated movements

Journal

Frontiers in systems neuroscience
ISSN: 1662-5137
Titre abrégé: Front Syst Neurosci
Pays: Switzerland
ID NLM: 101477946

Informations de publication

Date de publication:
2020
Historique:
received: 24 04 2020
accepted: 06 07 2020
entrez: 15 8 2020
pubmed: 15 8 2020
medline: 15 8 2020
Statut: epublish

Résumé

Parkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements. We investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity. We compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation. SI movements in PD are associated with greater low-beta (13-20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements. These findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD.

Sections du résumé

BACKGROUND BACKGROUND
Parkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements.
OBJECTIVES OBJECTIVE
We investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity.
METHODS METHODS
We compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation.
RESULTS RESULTS
SI movements in PD are associated with greater low-beta (13-20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements.
CONCLUSION CONCLUSIONS
These findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD.

Identifiants

pubmed: 32792918
doi: 10.3389/fnsys.2020.00054
pmc: PMC7390921
doi:

Types de publication

Journal Article

Langues

eng

Pagination

54

Informations de copyright

Copyright © 2020 Choi, Malekmohammadi, Sparks, Kashanian, Cross, Bordelon and Pouratian.

Références

Clin Neurophysiol. 2016 Apr;127(4):2010-9
pubmed: 26971483
Brain Stimul. 2018 May - Jun;11(3):607-617
pubmed: 29422442
J Neurosci. 2008 Jun 11;28(24):6165-73
pubmed: 18550758
J Neuroradiol. 2018 Jul;45(4):249-255
pubmed: 29273534
Neuroimage. 2013 Jan 1;64:416-24
pubmed: 22986076
Eur J Neurosci. 2005 Mar;21(5):1403-12
pubmed: 15813950
Comput Intell Neurosci. 2011;2011:156869
pubmed: 21253357
Neuroimage. 2018 Aug 15;177:20-29
pubmed: 29738912
J Neural Eng. 2018 Oct;15(5):056016
pubmed: 29972146
Neurobiol Dis. 2013 Jun;54:464-74
pubmed: 23388190
Brain. 2016 Aug;139(Pt 8):2211-23
pubmed: 27329771
J Neurosci. 2018 May 9;38(19):4556-4568
pubmed: 29661966
Electroencephalogr Clin Neurophysiol. 1979 Feb;46(2):138-46
pubmed: 86421
Neurol Sci. 2002 Sep;23(3):91-7
pubmed: 12391492
Nat Rev Neurosci. 2010 Nov;11(11):760-72
pubmed: 20944662
Anesthesiology. 2018 Feb;128(2):305-316
pubmed: 29068830
Front Psychol. 2011 Sep 30;2:236
pubmed: 21994498
Behav Neurosci. 2013 Apr;127(2):222-36
pubmed: 23244290
J Neurosci. 2010 May 12;30(19):6667-77
pubmed: 20463229
J Neurol Neurosurg Psychiatry. 2008 Oct;79(10):1110-6
pubmed: 18356249
Motor Control. 1998 Apr;2(2):125-32
pubmed: 9644283
Front Hum Neurosci. 2015 Sep 22;9:512
pubmed: 26441609
Clin Neurophysiol. 2017 Nov;128(11):2165-2178
pubmed: 28942154
Trends Neurosci. 1991 Nov;14(11):480-2
pubmed: 1726761
Brain Res. 2013 May 28;1512:45-59
pubmed: 23548595
Exp Neurol. 2009 Feb;215(2):380-7
pubmed: 19070616
Exp Neurol. 2012 Aug;236(2):383-8
pubmed: 22572590
Neuroimage. 2017 Oct 1;159:1-8
pubmed: 28712991
Sci Rep. 2016 Oct 11;6:34930
pubmed: 27725721
Brain. 1995 Aug;118 ( Pt 4):913-33
pubmed: 7655888
Brain. 2016 May;139(Pt 5):1482-96
pubmed: 27017189
Neuropsychologia. 2016 Jun;86:38-44
pubmed: 27090103
Curr Opin Neurobiol. 2010 Apr;20(2):156-65
pubmed: 20359884
Brain. 2012 Feb;135(Pt 2):615-30
pubmed: 22252995
Neuroimage. 2011 Mar 1;55(1):204-15
pubmed: 21126588
J Neurosci Methods. 2004 Mar 15;134(1):9-21
pubmed: 15102499

Auteurs

Jeong Woo Choi (JW)

Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United States.

Mahsa Malekmohammadi (M)

Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United States.

Hiro Sparks (H)

Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United States.

Alon Kashanian (A)

Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United States.

Katy A Cross (KA)

Department of Neurology, University of California, Los Angeles, Los Angeles, CA, United States.

Yvette Bordelon (Y)

Department of Neurology, University of California, Los Angeles, Los Angeles, CA, United States.

Nader Pouratian (N)

Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United States.
Department of Bioengineering, University of California, Los Angeles, Los Angeles, CA, United States.
Brain Research Institute, University of California, Los Angeles, Los Angeles, CA, United States.

Classifications MeSH