Deep brain stimulation for Parkinson’s disease dissociates mood and motor circuits: a functional MRI case study
Open accessAbstract
Behavioral disturbances have been reported with subthalamic (STN) deep brain stimulation (DBS) treatment in Parkinson's disease (PD). We report correlative functional imaging (fMRI) of mood and motor responses induced by successive right and left DBS. A 36‐year‐old woman with medically refractory PD and a history of clinically remitted depression underwent uncomplicated implantation of bilateral STN DBS. High‐frequency stimulation of the left electrode improved motor symptoms. Unexpectedly, right DBS alone elicited several reproducible episodes of acute depressive dysphoria. Structural and functional magnetic resonance imaging (fMRI) imaging was carried out with sequential individual electrode stimulation. The electrode on the left was within the inferior STN, whereas the right electrode was marginally superior and lateral to the intended STN target within the Fields of Forel/zona incerta. fMRI image analysis (Analysis of Functional NeuroImages, AFNI) contrasting OFF versus ON stimulation identified significant lateralized blood oxygen level‐dependent (BOLD) signal changes with DBS (P < 0.001). Left DBS primarily showed changes in motor regions: increases in premotor and motor cortex, ventrolateral thalamus, putamen, and cerebellum as well as decreases in sensorimotor/supplementary motor cortex. Right DBS showed similar but less extensive change in motor regions. More prominent were the unique increases in superior prefrontal cortex, anterior cingulate (Brodmann's area [BA] 24), anterior thalamus, caudate, and brainstem, and marked widespread decreases in medial prefrontal cortex (BA 9/10). The mood disturbance resolved spontaneously in 4 weeks despite identical stimulation parameters. Transient depressive mood induced by subcortical DBS stimulation was correlated with changes in mesolimbic cortical structures. This case provides new evidence supporting cortical segregation of motor and nonmotor cortico‐basal ganglionic systems that may converge in close proximity at the level of the STN and the adjacent white matter tracts (Fields of Forel/zona incerta). © 2003 Movement Disorder Society
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Activation of one DBS electrode in a PD patient with remote depression induced intense dysphoria of rapid onset.
“However, activation of the other electrode had the unexpected effect of inducing an intense dysphoria of rapid onset.”
From Cortico-striatal-thalamic loop circuits of the salience network: A central pathway in psychiatric disease and treatment (2016) · cites this paper as Stefurak et al., 2003
A case study suggests that DBS targeting the SN-CSTC may not necessarily exert desirable effects in MDD.
“One illustrative case study suggests that DBS targeting the SN-CSTC may not necessarily exert desirable effects in MDD (Stefurak et al., 2003).”
From Cortico-striatal-thalamic loop circuits of the salience network: A central pathway in psychiatric disease and treatment (2016) · cites this paper as Stefurak et al., 2003
Stimulation of the other electrode yielded suppression of activity in SN regions including the dACC and caudate nucleus, accompanied by rapid descent into dysphoria.
“Stimulation of the other electrode yielded suppression of activity in the SN regions including the dACC as well as the caudate nucleus, accompanied by rapid descent into dysphoria.”
From Cortico-striatal-thalamic loop circuits of the salience network: A central pathway in psychiatric disease and treatment (2016) · cites this paper as Stefurak et al., 2003
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Cited by
Sorted by citations
Translational principles of deep brain stimulation
Kringelbach, M. L., Jenkinson, N., Owen, S. L. F., & Aziz, T. Z. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2196 · Cited by 853 · see citing works
Peters, S. K., Dunlop, K., & Downar, J. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00104 · Cited by 611 · see citing works
“Importantly, the mesolimbic and nigrostriatal dopaminergic pathway have been implicated in the encoding of ‘‘saliency prediction errors’’, underscoring their broader contributions to the attribution of salience to environmental stimuli (Kapur, 2003; Haber, 2016).”
BackgroundNetwork perspectives on the mechanisms of deep brain stimulation
McIntyre, C. C., & Hahn, P. J. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.09.022 · Cited by 439 · see citing works
Mechanisms of action of deep brain stimulation (DBS)
Montgomery, E. B., & Gale, J. T. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.06.003 · Cited by 344 · see citing works
Deep Brain Stimulation for Neurologic and Neuropsychiatric Disorders
Wichmann, T., & DeLong, M. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.022 · Cited by 331 · see citing works
Bakker, N., Shahab, S., Giacobbe, P., Blumberger, D. M., Daskalakis, Z. J., Kennedy, S. H., & Downar, J. (2015) · Brain Stimulation · doi:10.1016/j.brs.2014.11.002 · Cited by 306 · see citing works
The non-motor syndrome of primary dystonia: clinical and pathophysiological implications
Stamelou, M., Edwards, M. J., Hallett, M., & Bhatia, K. P. (2012) · Brain · doi:10.1093/brain/awr224 · Cited by 299 · see citing works
New targets for rTMS in depression: A review of convergent evidence
Downar, J., & Daskalakis, Z. J. (2013) · Brain Stimulation · doi:10.1016/j.brs.2012.08.006 · Cited by 257 · see citing works
Subsyndromal depression in the elderly: underdiagnosed and undertreated
VanItallie, T. B. (2005) · Metabolism · doi:10.1016/j.metabol.2005.01.012 · Cited by 115 · see citing works
- Authors
- Stefurak, T., Mikulis, D., Mayberg, H., Lang, A. E., Hevenor, S., Pahapill, P., Saint‐Cyr, J., & Lozano, A.
- Affiliations
- University Health Network (CA)
- University of Toronto (CA)
- Corresponding author
- Stefurak, Taresa
- Venue
- Movement Disorders
- Publisher
- Wiley
- Published
- 2003-10-03
- Volume
- 18
- Issue
- 12
- Pages
- 1508-1516
- ISSN
- 0885-3185 (ISSN-L)
- 1531-8257
- OpenAlex
- W2049711835
- Cited by
- 215
- References
- 92
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 17 · 2023: 3 · 2022: 6 · 2021: 7 · 2020: 11 · 2019: 8 · 2018: 4 · 2017: 6 · 2016: 12 · 2015: 11 · 2014: 17 · 2013: 10 · 2012: 15
- FWCI
- 5.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Movement Disorders (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Social Sciences › Psychology › Clinical Psychology › Obsessive-Compulsive Spectrum Disorders
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Keywords
- deep brain stimulation, Parkinson's disease, subthalamic nucleus, mood disturbance, motor circuits, mesolimbic system, anterior cingulate cortex, medial prefrontal cortex, BOLD signal changes
- MeSH terms
- Adult, Cerebellum, Electrodes, Implanted, Electric Stimulation Therapy, Female, Humans, Functional Laterality, Magnetic Resonance Imaging, Motor Cortex, Nerve Net, Parkinson Disease, Putamen, Mood Disorders, Ventral Thalamic Nuclei
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