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

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 stim...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: Elsevier 2019-07-01
Series:Brain Stimulation
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1935861X19300865
id doaj-f03be6dcec53403e950077e2c04c55fb
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author 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
spellingShingle 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
Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
Brain Stimulation
Cingulate cortex
Frequency
Current
Local field potential
Neuromodulation
Intracranial
author_facet 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
author_sort Ishita Basu
title Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
title_short Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
title_full Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
title_fullStr Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
title_full_unstemmed Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
title_sort consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodes
publisher Elsevier
series Brain Stimulation
issn 1935-861X
publishDate 2019-07-01
description 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.
topic Cingulate cortex
Frequency
Current
Local field potential
Neuromodulation
Intracranial
url http://www.sciencedirect.com/science/article/pii/S1935861X19300865
work_keys_str_mv AT ishitabasu consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT madelinemrobertson consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT britnicrocker consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT noampeled consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT karafarnes consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT deborahivallejolopez consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT helendeng consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT matthewthombs consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT clarissamartinezrubio consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT jenniferjcheng consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT ericmcdonald consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT darinddougherty consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT emadneskandar consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT alikswidge consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT angeliquecpaulk consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
AT sydneyscash consistentlinearandnonlinearresponsestoinvasiveelectricalbrainstimulationacrossindividualsandprimatespecieswithimplantedelectrodes
_version_ 1724213698142142464
spelling doaj-f03be6dcec53403e950077e2c04c55fb2021-03-19T07:19:40ZengElsevierBrain Stimulation1935-861X2019-07-01124877892Consistent linear and non-linear responses to invasive electrical brain stimulation across individuals and primate species with implanted electrodesIshita Basu0Madeline M. Robertson1Britni Crocker2Noam Peled3Kara Farnes4Deborah I. Vallejo-Lopez5Helen Deng6Matthew Thombs7Clarissa Martinez-Rubio8Jennifer J. Cheng9Eric McDonald10Darin D. Dougherty11Emad N. Eskandar12Alik S. Widge13Angelique C. Paulk14Sydney S. Cash15Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA 02114, USADepartment of Radiology, MGH/HST Martinos Center for Biomedical Imaging, Charlestown, MA, 02129, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USADepartment of Neurology, Massachusetts General Hospital, Boston, MA 02114, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Department of Radiology, MGH/HST Martinos Center for Biomedical Imaging, Charlestown, MA, 02129, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USADepartment of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USADepartment of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, 02129, USA; Picower Institute for Learning &amp; Memory, Massachusetts Institute of Technology, Cambridge, MA 02124, USANayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA; Corresponding author. Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USABackground: 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.http://www.sciencedirect.com/science/article/pii/S1935861X19300865Cingulate cortexFrequencyCurrentLocal field potentialNeuromodulationIntracranial