Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes

Ishita Basu, Madeline M. Robertson, Britni Crocker, Noam Peled, Kara Farnes, Deborah I. Vallejo-Lopez, Helen Deng, Matthew Thombs, Clarissa Martinez-Rubio, Jennifer J. Cheng, Eric McDonald, Darin D. Dougherty, Emad N. Eskandar, Alik S. Widge, Angelique C. Paulk, Sydney S. Cash

Research output: Contribution to journalArticle

Abstract

Background: Electrical neuromodulation via implanted electrodes is used in treating numerous neurological disorders, yet our knowledge of how different brain regions respond to varying stimulation parameters is sparse. Objective/Hypothesis: We hypothesized that the neural response to electrical stimulation is both region-specific and non-linearly related to amplitude and frequency. Methods: We examined evoked neural responses following 400 ms trains of 10–400 Hz electrical stimulation ranging from 0.1 to 10 mA. We stimulated electrodes implanted in cingulate cortex (dorsal anterior cingulate and rostral anterior cingulate) and subcortical regions (nucleus accumbens, amygdala) of non-human primates (NHP, N = 4) and patients with intractable epilepsy (N = 15) being monitored via intracranial electrodes. Recordings were performed in prefrontal, subcortical, and temporal lobe locations. Results: In subcortical regions as well as dorsal and rostral anterior cingulate cortex, response waveforms depended non-linearly on frequency (Pearson's linear correlation r < 0.39), but linearly on current (r > 0.58). These relationships between location, and input-output characteristics were similar in homologous brain regions with average Pearson's linear correlation values r > 0.75 between species and linear correlation values between participants r > 0.75 across frequency and current values per brain region. Evoked waveforms could be described by three main principal components (PCs) which allowed us to successfully predict response waveforms across individuals and across frequencies using PC strengths as functions of current and frequency using brain region specific regression models. Conclusions: These results provide a framework for creation of an atlas of input-output relationships which could be used in the principled selection of stimulation parameters per brain region.

Original languageEnglish (US)
JournalBrain Stimulation
DOIs
StatePublished - Jan 1 2019
Externally publishedYes

Fingerprint

Implanted Electrodes
Deep Brain Stimulation
Gyrus Cinguli
Primates
Brain
Electric Stimulation
Atlases
Nucleus Accumbens
Temporal Lobe
Amygdala
Nervous System Diseases
Electrodes

Keywords

  • Cingulate cortex
  • Current
  • Frequency
  • Intracranial
  • Local field potential
  • Neuromodulation

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biophysics
  • Clinical Neurology

Cite this

Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes. / Basu, Ishita; Robertson, Madeline M.; Crocker, Britni; Peled, Noam; Farnes, Kara; Vallejo-Lopez, Deborah I.; Deng, Helen; Thombs, Matthew; Martinez-Rubio, Clarissa; Cheng, Jennifer J.; McDonald, Eric; Dougherty, Darin D.; Eskandar, Emad N.; Widge, Alik S.; Paulk, Angelique C.; Cash, Sydney S.

In: Brain Stimulation, 01.01.2019.

Research output: Contribution to journalArticle

Basu, I, Robertson, MM, Crocker, B, Peled, N, Farnes, K, Vallejo-Lopez, DI, Deng, H, Thombs, M, Martinez-Rubio, C, Cheng, JJ, McDonald, E, Dougherty, DD, Eskandar, EN, Widge, AS, Paulk, AC & Cash, SS 2019, 'Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes', Brain Stimulation. https://doi.org/10.1016/j.brs.2019.03.007
Basu, Ishita ; Robertson, Madeline M. ; Crocker, Britni ; Peled, Noam ; Farnes, Kara ; Vallejo-Lopez, Deborah I. ; Deng, Helen ; Thombs, Matthew ; Martinez-Rubio, Clarissa ; Cheng, Jennifer J. ; McDonald, Eric ; Dougherty, Darin D. ; Eskandar, Emad N. ; Widge, Alik S. ; Paulk, Angelique C. ; Cash, Sydney S. / Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes. In: Brain Stimulation. 2019.
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AU - Robertson, Madeline M.

AU - Crocker, Britni

AU - Peled, Noam

AU - Farnes, Kara

AU - Vallejo-Lopez, Deborah I.

AU - Deng, Helen

AU - Thombs, Matthew

AU - Martinez-Rubio, Clarissa

AU - Cheng, Jennifer J.

AU - McDonald, Eric

AU - Dougherty, Darin D.

AU - Eskandar, Emad N.

AU - Widge, Alik S.

AU - Paulk, Angelique C.

AU - Cash, Sydney S.

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N2 - Background: Electrical neuromodulation via implanted electrodes is used in treating numerous neurological disorders, yet our knowledge of how different brain regions respond to varying stimulation parameters is sparse. Objective/Hypothesis: We hypothesized that the neural response to electrical stimulation is both region-specific and non-linearly related to amplitude and frequency. Methods: We examined evoked neural responses following 400 ms trains of 10–400 Hz electrical stimulation ranging from 0.1 to 10 mA. We stimulated electrodes implanted in cingulate cortex (dorsal anterior cingulate and rostral anterior cingulate) and subcortical regions (nucleus accumbens, amygdala) of non-human primates (NHP, N = 4) and patients with intractable epilepsy (N = 15) being monitored via intracranial electrodes. Recordings were performed in prefrontal, subcortical, and temporal lobe locations. Results: In subcortical regions as well as dorsal and rostral anterior cingulate cortex, response waveforms depended non-linearly on frequency (Pearson's linear correlation r < 0.39), but linearly on current (r > 0.58). These relationships between location, and input-output characteristics were similar in homologous brain regions with average Pearson's linear correlation values r > 0.75 between species and linear correlation values between participants r > 0.75 across frequency and current values per brain region. Evoked waveforms could be described by three main principal components (PCs) which allowed us to successfully predict response waveforms across individuals and across frequencies using PC strengths as functions of current and frequency using brain region specific regression models. Conclusions: These results provide a framework for creation of an atlas of input-output relationships which could be used in the principled selection of stimulation parameters per brain region.

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