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...
Main Authors: | , , , , , , , , , , , , , , , |
---|---|
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 & 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 |