Cited by 89Neurological disorders and treatmentsTranscranial Magnetic Stimulation StudiesVagus Nerve Stimulation Research

Field potential 1/f activity in the subcallosal cingulate region as a candidate signal for monitoring deep brain stimulation for treatment-resistant depression

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Veerakumar, Ashan, Tiruvadi, Vineet, Howell, Bryan, Waters, Allison C., Crowell, Andrea L., Voytek, Bradley, Riva-Posse, Patricio, Denison, Lydia +5 more·2019·Journal of Neurophysiology

Abstract

Subcallosal cingulate cortex deep brain stimulation (SCC-DBS) is an experimental therapy for treatment-resistant depression (TRD). Refinement and optimization of SCC-DBS will benefit from increased study of SCC electrophysiology in context of ongoing high-frequency SCC-DBS therapy. The study objective was a 7-mo observation of frequency-domain 1/ f slope in off-stimulation local field potentials (SCC-LFPs) alongside standardized measurements of depression severity in 4 patients undergoing SCC-DBS. SCC was implanted bilaterally with a combined neurostimulation-LFP recording system. Following a 1-mo off-stimulation postoperative phase with multiple daily recordings, patients received bilateral SCC-DBS therapy (130 Hz, 90 μs) and weekly resting-state SCC-LFP recordings over a 6-mo treatment phase. 1/ f slopes for each time point were estimated via linear regression of log-transformed Welch periodograms. General linear mixed-effects models were constructed to estimate pretreatment sources of 1/ f slope variance, and 95% bootstrap confidence intervals were constructed to estimate treatment phase 1/ f slope association with treatment response (50% decrease in preimplantation symptom severity). Results show the time of recording was a prominent source of pretreatment 1/ f slope variance bilaterally, with increased 1/ f slope magnitude observed during night hours (2300–0659). Increase in right 1/ f slope was observed in the setting of treatment response, with bootstrap analysis supporting this observation in 3 of 4 subjects. We conclude that 1/ f slope can be measured longitudinally in a combined SCC-DBS/LFP recording system and likely conforms to known 1/ f circadian variability. The preliminary evidence of 1/ f slope increase during treatment response suggests a potential utility as a candidate biomarker for ongoing development of adaptive TRD-neuromodulation strategies. NEW & NOTEWORTHY In four patients with treatment-resistant depression undergoing therapeutic deep brain stimulation (DBS), we present the first longitudinal observations of local field potentials (LFP) from the subcallosal cingulate region outside the postoperative period. Specifically, our results demonstrate that frequency-domain 1/ f activity is measurable in a combined DBS-LFP recording system and that right hemisphere recordings appear sensitive to mood state, thus suggesting a potential readout suitable for consideration in ongoing efforts to develop adaptive DBS delivery systems.

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  • Investigators showed local field potential (LFP) spectral changes over time during SCC DBS for MDD, although it was difficult to demonstrate a clear and consistent correlation between any individual LFP feature and clinical outcome.

    “In a recent psychiatric example, investigators showed local field potential (LFP) spectral changes over time during SCC DBS for MDD (Veerakumar et al. 2019), although it was difficult to demonstrate a clear and consistent correlation between any individual LFP feature and the clinical outcome.”
  • Recent psychiatric studies have shown network-level oscillatory changes from DBS at psychiatric targets.

    “This has long been recognized in movement disorders (Little & Brown, 2012), but recent psychiatric studies have also shown network-level oscillatory changes from DBS at psychiatric targets (Veerakumar et al. 2019).”
  • Effective DBS modulates oscillations and their synchrony.

    “Moreover, effective DBS modulates oscillations and their synchrony.”
  • In chronic SCC-DBS, local field potential 1/f slope changes recorded weekly at the right SCC lead during the first 6 months discriminated depressed from non-depressed states in three of four patients.

    “local field potential changes in 1/f slope, a putative correlate of neuronal excitability, recorded weekly at the right SCC-lead during the first 6 months of SCC-DBS discriminated depressed from non-depressed states in three out of the four patients [85].”

    From Deep brain stimulation for depression. (2022) · cites this paper as [85]

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Research works printed but not linked: 2

  1. Haller M, Donoghue D, Peterson E, Varma P, Sebastian P, Gao R, Noto T, Knight RT, Shestyuk A, Voytek B. Parameterizing neural power spectra (Preprint). bioRxiv 299859, 2018. doi:10.1101/299859. · DOI
  2. Hamilton M. Assessment of Depression. Berlin: Springer, 1986, p. 143-152.

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Authors
Veerakumar, A., Tiruvadi, V., Howell, B., Waters, A. C., Crowell, A. L., Voytek, B., Riva-Posse, P., Denison, L., Rajendra, J. K., Edwards, J. A., Bijanki, K. R., Choi, K. S., & Mayberg, H. S.
Affiliations
  • Emory University (US)
  • Georgia Institute of Technology (US)
  • University of California San Diego (US)
  • Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, Georgia
  • National Institutes of Health (US)
Corresponding author
Mayberg, Helen S.
Venue
Journal of Neurophysiology
Published
2019-09-01
Volume
122
Issue
3
Pages
1023-1035
ISSN
  • 0022-3077 (ISSN-L)
  • 1522-1598
OpenAlex
W2958634274
Cited by
89
References
68
Citations by year
2026: 9 · 2025: 16 · 2024: 12 · 2023: 21 · 2022: 10 · 2021: 9 · 2020: 9 · 2019: 2 · 2018: 1
FWCI
5.07
Type
journal article
Language
en
Open access
Locations
  • Journal of Neurophysiology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Howard Hughes Medical Institute (HHMI)
  • HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) (UH3NS103550)
  • HHS | NIH | National Institute of Mental Health (NIMH) (R01 MH102238, R01 MH106173)
  • NIH (F32 NS096839)
  • Hope for Depression Research Foundation (Depression Research Foundation)
Topics
  • Health Sciences › Medicine › Neurology › Neurological disorders and treatments
  • Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
  • Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
Keywords
treatment-resistant depression, deep brain stimulation, local field potentials, circadian variation, biomarkers, adaptive neuromodulation, right hemisphere, treatment response
MeSH terms
Aged, Female, Gyrus Cinguli, Humans, Longitudinal Studies, Male, Middle Aged, Process Assessment, Health Care, Deep Brain Stimulation, Electrophysiological Phenomena, Depressive Disorder, Treatment-Resistant

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