Basal ganglia theta power indexes trait anxiety in people with Parkinson's disease

Bart E K S Swinnen; Colin W Hoy; Elena Pegolo; Bryony Ishihara; Elena Ubeda Matzilevich; Julia Sun; Francesca Morgante; Erlick Pereira; Fahd Baig; Michael Hart; Huiling Tan; Zimi Sawacha; Martijn Beudel; Sarah Wang; Philip Starr; Simon Little; Lucia Ricciardi

doi:10.1093/brain/awae313

journal article Open Access Oct 21, 2024

Basal ganglia theta power indexes trait anxiety in people with Parkinson's disease

Bart E K S Swinnen

Colin W Hoy Elena Pegolo Bryony Ishihara Elena Ubeda Matzilevich Julia Sun Francesca Morgante

Erlick Pereira Fahd Baig

Michael Hart

Huiling Tan

Zimi Sawacha Martijn Beudel

Sarah Wang Philip Starr Simon Little

Lucia Ricciardi

Brain Vol. 148 No. 4 pp. 1228-1241 · Oxford University Press (OUP)

View at Publisher Save 10.1093/brain/awae313

Abstract

Abstract
Neuropsychiatric symptoms are common and disabling in Parkinson's disease, with troublesome anxiety occurring in one-third of patients. Management of anxiety in Parkinson's disease is challenging, hampered by insufficient insight into underlying mechanisms, lack of objective anxiety measurements and largely ineffective treatments.
In this study, we assessed the intracranial neurophysiological correlates of anxiety in patients with Parkinson's disease treated with deep brain stimulation (DBS) in the laboratory and at home. We hypothesized that low-frequency (theta–alpha) activity would be associated with anxiety.
We recorded local field potentials from subthalamic nucleus or globus pallidus pars interna DBS implants in three Parkinson's disease cohorts: (i) patients with recordings (subthalamic nucleus) performed in hospital at rest via perioperatively externalized leads, without active stimulation, both ON and OFF dopaminergic medication; (ii) patients with recordings (subthalamic nucleus or globus pallidus pars interna) performed at home while resting, via a chronically implanted commercially available sensing-enabled neurostimulator (Medtronic Percept™ device), ON dopaminergic medication, with stimulation both on and off; and (iii) patients with recordings performed at home while engaging in a behavioural task via subthalamic nucleus and globus pallidus pars interna leads and electrocorticography paddles over the premotor cortex connected to an investigational sensing-enabled neurostimulator, ON dopaminergic medication, with stimulation both on and off.
Trait anxiety was measured with validated clinical scales in all participants, and state anxiety was measured with momentary assessment scales at multiple time points in the two at-home cohorts. Power in theta (4–8 Hz) and alpha (8–12 Hz) ranges was extracted from the local field potential recordings, and its relationship with anxiety ratings was assessed using linear mixed-effects models.
In total, 33 patients with Parkinson's disease (59 hemispheres) were included. Across three independent cohorts, with stimulation off, basal ganglia theta power was positively related to trait anxiety (all P &lt; 0.05). Also in a naturalistic setting, with individuals at home, at rest, with stimulation and medication ON, basal ganglia theta power was positively related to trait anxiety (P &lt; 0.05). This relationship held regardless of the hemisphere and DBS target. There was no correlation between trait anxiety and premotor cortical theta–alpha power. There was no within-patient association between basal ganglia theta–alpha power and state anxiety.
We showed that basal ganglia theta activity indexes trait anxiety in Parkinson's disease. Our data suggest that theta could be a possible physiomarker of neuropsychiatric symptoms and specifically of anxiety in Parkinson's disease, potentially suitable for guiding advanced DBS treatment tailored to the needs of the individual patient, including non-motor symptoms.

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References

73

[1]

Weintraub "The neuropsychiatry of Parkinson’s disease: Advances and challenges" Lancet Neurol (2022) 10.1016/s1474-4422(21)00330-6

[2]

Bock "Association of motor and nonmotor symptoms with health-related quality of life in a large online cohort of people with Parkinson disease" Neurology (2022) 10.1212/wnl.0000000000200113

[3]

Jacob "Occurrence of depression and anxiety prior to Parkinson’s disease" Parkinsonism Relat Disord (2010) 10.1016/j.parkreldis.2010.06.014

[4]

Weintraub "The neuropsychiatry of Parkinson disease: A perfect storm" Am J Geriatr Psychiatry (2019) 10.1016/j.jagp.2019.03.002

[5]

Rodriguez-Blazquez "Prevalence of non-motor symptoms and non-motor fluctuations in Parkinson’s disease using the MDS-NMS" Mov Disord Clin Pract (2021) 10.1002/mdc3.13122

[6]

Forbes "Defining atypical anxiety in Parkinson’s disease" Mov Disord Clin Pract (2021) 10.1002/mdc3.13193

[7]

Hirsch "Improving detection of psychiatric disturbances in Parkinson’s disease: The role of informants" J Parkinsons Dis (2013) 10.3233/jpd-120170

[8]

Rizos "Characterizing motor and non-motor aspects of early-morning off periods in Parkinson’s disease: An international multicenter study" Parkinsonism Relat Disord (2014) 10.1016/j.parkreldis.2014.09.013

[9]

Kua "How well do caregivers detect depression and anxiety in patients with Parkinson disease?" J Geriatr Psychiatry Neurol (2018) 10.1177/0891988718788641

[10]

Hu "How well do we recognise non-motor symptoms in a British Parkinson’s disease population?" J Neurol (2011) 10.1007/s00415-011-5972-6

[11]

Pontone "Report from a multidisciplinary meeting on anxiety as a non-motor manifestation of Parkinson’s disease" NPJ Parkinsons Dis (2019) 10.1038/s41531-019-0102-8

[12]

Spielberger "The state-trait anxiety inventory" RIP/IJP (1971)

[13]

Saviola "Trait and state anxiety are mapped differently in the human brain" Sci Rep (2020) 10.1038/s41598-020-68008-z

[14]

Goodarzi "Barriers and facilitators for guidelines with depression and anxiety in Parkinson’s disease or dementia" Can J Aging (2018) 10.1017/s0714980818000053

[15]

Dobkin "Barriers to mental health care utilization in Parkinson’s disease" J Geriatr Psychiatry Neurol (2013) 10.1177/0891988713481269

[16]

Seppi "Update on treatments for nonmotor symptoms of Parkinson’s disease—an evidence-based medicine review" Mov Disord (2019) 10.1002/mds.27602

[17]

Goldman "Treatment of nonmotor symptoms associated with Parkinson disease" Neurol Clin (2020) 10.1016/j.ncl.2019.12.003

[18]

Deuschl "European academy of neurology/movement disorder society-European section guideline on the treatment of Parkinson’s disease: I. Invasive therapies" Mov Disord (2022) 10.1002/mds.29066

[19]

Kurtis "The effect of deep brain stimulation on the non-motor symptoms of Parkinson’s disease: A critical review of the current evidence" NPJ Parkinsons Dis (2017) 10.1038/npjparkd.2016.24

[20]

Mosley "Neuropsychiatric effects of subthalamic deep brain stimulation" Handb Clin Neurol (2021) 10.1016/b978-0-12-820107-7.00026-4

[21]

Cartmill "Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: A meta-analysis of mood effects" Neuropsychol Rev (2021) 10.1007/s11065-020-09467-z

[22]

Swinnen "Diving into the subcortex: The potential of chronic subcortical sensing for unravelling basal ganglia function and optimization of deep brain stimulation" Neuroimage (2022) 10.1016/j.neuroimage.2022.119147

[23]

Little "Adaptive deep brain stimulation in advanced Parkinson disease" Ann Neurol (2013) 10.1002/ana.23951

[24]

Schmidt "At home adaptive dual target deep brain stimulation in Parkinson’s disease with proportional control" Brain (2024) 10.1093/brain/awad429

[25]

Busch "Single threshold adaptive deep brain stimulation in Parkinson’s disease depends on parameter selection, movement state and controllability of subthalamic beta activity" Brain Stimul (2024) 10.1016/j.brs.2024.01.007

[26]

van Wijk "A systematic review of local field potential physiomarkers in Parkinsons disease: From clinical correlations to adaptive deep brain stimulation algorithms" J Neurol (2023) 10.1007/s00415-022-11388-1

[27]

Maltête "Microsubthalamotomy: An immediate predictor of long-term subthalamic stimulation efficacy in Parkinson disease" Mov Disord (2008) 10.1002/mds.22054

[28]

Wang "Micro lesion effect of the globus pallidus internus with deep brain stimulation in Parkinson’s disease patients" Acta Neurochir (Wien) (2017) 10.1007/s00701-017-3271-4

[29]

Ricciardi "Uncovering the neurophysiology of mood, motivation and behavioral symptoms in Parkinson’s disease through intracranial recordings" NPJ Parkinson’s Disease (2023) 10.1038/s41531-023-00567-0

[30]

Rodriguez-Oroz "Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson’s disease" Brain (2011) 10.1093/brain/awq301

[31]

Sun "α and θ oscillations in the subthalamic nucleus are potential biomarkers for Parkinson’s disease with depressive symptoms" Parkinsonism Relat Disord (2021) 10.1016/j.parkreldis.2021.07.023

[32]

Ricciardi "Neurophysiological correlates of trait impulsivity in Parkinson’s disease" Mov Disord (2021) 10.1002/mds.28625

[33]

Defer "Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD)" Mov Disord (1999) 10.1002/1531-8257(199907)14:4<572::aid-mds1005>3.0.co;2-c

[34]

Stanslaski "A chronically implantable neural coprocessor for investigating the treatment of neurological disorders" IEEE Trans Biomed Circuits Syst (2018) 10.1109/tbcas.2018.2880148

[35]

Hamilton "The assessment of anxiety states by rating" Br J Med Psychol (1959) 10.1111/j.2044-8341.1959.tb00467.x

[36]

Hamilton "A rating scale for depression" J Neurol Neurosurg Psychiatry (1960) 10.1136/jnnp.23.1.56

[37]

An inventory for measuring clinical anxiety: Psychometric properties.

Aaron T. Beck, Norman Epstein, Gary Brown et al.

Journal of Consulting and Clinical Psychology 1988 10.1037/0022-006x.56.6.893

[38]

Beck "Psychometric properties of the Beck depression inventory: Twenty-five years of evaluation" Clin Psychol Rev (1988) 10.1016/0272-7358(88)90050-5

[39]

Kool "When does model-based control pay off?" PLoS Comput Biol (2016) 10.1371/journal.pcbi.1005090

[40]

Sellers "Analysis-rcs-data: Open-source toolbox for the ingestion, time-alignment, and visualization of sense and stimulation data from the Medtronic Summit RC+S system" Front Hum Neurosci (2021) 10.3389/fnhum.2021.714256

[41]

Dworkin "The extent and drivers of gender imbalance in neuroscience reference lists" Nat Neurosci (2020) 10.1038/s41593-020-0658-y

[42]

Chatterjee "Gender disparity in citations in high-impact journal articles" JAMA Netw Open (2021) 10.1001/jamanetworkopen.2021.14509

[43]

Fulvio "Gender (im)balance in citation practices in cognitive neuroscience" J Cogn Neurosci (2021) 10.1162/jocn_a_01643

[44]

Bertolero "Racial and ethnic imbalance in neuroscience reference lists and intersections with gender" 10.1101/2020.10.12.336230

[45]

Chintalapati "Predicting race and ethnicity from the sequence of characters in a name" arXiv 10.48550/arxiv.1805.02109

[46]

Ambekar "Name-ethnicity classification from open sources" 10.1145/1557019.1557032

[47]

Conti "Band-specific altered cortical connectivity in early Parkinson’s disease and its clinical correlates" Mov Disord (2023) 10.1002/mds.29615

[48]

van der Velden "Frequency of mood and anxiety fluctuations in Parkinson’s disease patients with motor fluctuations: A systematic review" Mov Disord (2018) 10.1002/mds.27465

[49]

Fumagalli "Conflict-dependent dynamic of subthalamic nucleus oscillations during moral decisions" Soc Neurosci (2011) 10.1080/17470919.2010.515148

[50]

Rosa "Pathological gambling in Parkinson’s disease: Subthalamic oscillations during economics decisions" Mov Disord (2013) 10.1002/mds.25427

Showing 50 of 73 references

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Details

Published: Oct 21, 2024
Vol/Issue: 148(4)
Pages: 1228-1241
License: View

Authors

B

Bart E K S Swinnen

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,; Department of Neurology, Amsterdam University Medical Centers, Amsterdam Neuroscience, University of Amsterdam , Amsterdam 1105 AZ ,

C

Colin W Hoy

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

E

Elena Pegolo

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,; Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,; Department of Information Engineering, University of Padova , Padova 35131 ,

B

Bryony Ishihara

Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

E

Elena Ubeda Matzilevich

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

J

Julia Sun

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

F

Francesca Morgante

Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

E

Erlick Pereira

Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

F

Fahd Baig

Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

M

Michael Hart

Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

H

Huiling Tan

Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford , Oxford OX1 3TH ,

Z

Zimi Sawacha

Department of Information Engineering, University of Padova , Padova 35131 ,

M

Martijn Beudel

Department of Neurology, Amsterdam University Medical Centers, Amsterdam Neuroscience, University of Amsterdam , Amsterdam 1105 AZ ,

S

Sarah Wang

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

P

Philip Starr

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

S

Simon Little

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,

L

Lucia Ricciardi

Department of Neurology, University of California San Francisco , San Francisco, CA 94158 ,; Neurosciences and Cell Biology Institute, Neuromodulation and Motor Control Section, St George’s University of London , London SW17 0RE ,

Funding

National Institutes of Health Award: K23NS120037

National Institute of Mental Health

National Institute of Neurological Disorders and Stroke

CARP MRC/NIHR Award: MR/T023864/1

Wellcome Discovery Award Award: 226645/Z/22/Z

Cite This Article

Bart E K S Swinnen, Colin W Hoy, Elena Pegolo, et al. (2024). Basal ganglia theta power indexes trait anxiety in people with Parkinson's disease. Brain, 148(4), 1228-1241. https://doi.org/10.1093/brain/awae313

Basal ganglia theta power indexes trait anxiety in people with Parkinson's disease

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