Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI

Hiroyuki Oya; Matthew A Howard; Vincent A Magnotta; Anton Kruger; Timothy D Griffiths; Louis Lemieux; David W Carmichael; Christopher I Petkov; Hiroto Kawasaki; Christopher K Kovach; Matthew J Sutterer; Ralph Adolphs

doi:10.1016/j.jneumeth.2016.12.014

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Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI

Journal article

Peer reviewed

Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI

Hiroyuki Oya, Matthew A Howard, Vincent A Magnotta, Anton Kruger, Timothy D Griffiths, Louis Lemieux, David W Carmichael, Christopher I Petkov, Hiroto Kawasaki, Christopher K Kovach, …

Journal of neuroscience methods, Vol.277, pp.101-112

02/01/2017

DOI: 10.1016/j.jneumeth.2016.12.014

PMCID: PMC5534177

PMID: 28012852

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https://www.ncbi.nlm.nih.gov/pmc/articles/5534177View

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Abstract

Understanding brain function requires knowledge of how one brain region causally influences another. This information is difficult to obtain directly in the human brain, and is instead typically inferred from resting-state fMRI. Here, we demonstrate the safety and scientific promise of a novel and complementary approach: concurrent electrical stimulation and fMRI (es-fMRI) at 3T in awake neurosurgical patients with implanted depth electrodes. We document the results of safety testing, actual experimental setup, and stimulation parameters, that safely and reliably evoke activation in distal structures through stimulation of amygdala, cingulate, or prefrontal cortex. We compare connectivity inferred from the evoked patterns of activation with that estimated from standard resting-state fMRI in the same patients: while connectivity patterns obtained with each approach are correlated, each method produces unique results. Response patterns were stable over the course of 11min of es-fMRI runs. COMPARISON WITH EXISTING METHOD: es-fMRI in awake humans yields unique information about effective connectivity, complementing resting-state fMRI. Although our stimulations were below the level of inducing any apparent behavioral or perceptual effects, a next step would be to use es-fMRI to modulate task performances. This would reveal the acute network-level changes induced by the stimulation that mediate the behavioral and cognitive effects seen with brain stimulation. es-fMRI provides a novel and safe approach for mapping effective connectivity in the human brain in a clinical setting, and will inform treatments for psychiatric and neurodegenerative disorders that use deep brain stimulation.

Brain - diagnostic imaging

Electric Stimulation

Humans

Middle Aged

Male

Biophysics

Brain - physiology

Neural Pathways - physiology

Oxygen - blood

Young Adult

Brain - blood supply

Magnetic Resonance Imaging

Image Processing, Computer-Assisted

Neural Pathways - diagnostic imaging

Brain Mapping

Adult

Female

Details

Title: Subtitle: Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI
Creators: Hiroyuki Oya - Department of Neurosurgery, Human Brain Research Laboratory, University of Iowa, Iowa City, IA 52241, USA. Electronic address: hiroyuki-oya@uiowa.edu
Matthew A Howard - Department of Neurosurgery, Human Brain Research Laboratory, University of Iowa, Iowa City, IA 52241, USA
Vincent A Magnotta - Department of Radiology, University of Iowa College of Medicine, Iowa City, IA 52241, USA
Anton Kruger - Department of Electrical and Computer Engineering, University of Iowa College of Engineering, USA
Timothy D Griffiths - Institute of Neuroscience, Newcastle University, Newcastle, UK
Louis Lemieux - UCL Institute of Neurology, University College London, London, UK
David W Carmichael - UCL Institute of Child Health, University College London, London, UK
Christopher I Petkov - Institute of Neuroscience, Newcastle University, Newcastle, UK
Hiroto Kawasaki - Department of Neurosurgery, Human Brain Research Laboratory, University of Iowa, Iowa City, IA 52241, USA
Christopher K Kovach - Department of Neurosurgery, Human Brain Research Laboratory, University of Iowa, Iowa City, IA 52241, USA
Matthew J Sutterer - Department of Neurosurgery, Human Brain Research Laboratory, University of Iowa, Iowa City, IA 52241, USA
Ralph Adolphs - Division of Biology and Biological Engineering, California Institute of Technology, USA
Resource Type: Journal article
Publication Details: Journal of neuroscience methods, Vol.277, pp.101-112
DOI: 10.1016/j.jneumeth.2016.12.014
PMID: 28012852
PMCID: PMC5534177
NLM abbreviation: J Neurosci Methods
ISSN: 0165-0270
eISSN: 1872-678X
Publisher: Netherlands
Grant note: R01 DC004290 / NIDCD NIH HHS UL1 RR024979 / NCRR NIH HHS R01 MH067681 / NIMH NIH HHS P50 MH094258 / NIMH NIH HHS
Language: English
Date published: 02/01/2017
Academic Unit: Roy J. Carver Department of Biomedical Engineering; Neurology; Radiology; Electrical and Computer Engineering; Psychiatry; Civil and Environmental Engineering; Psychological and Brain Sciences; Iowa Neuroscience Institute; Neurosurgery; Otolaryngology
Record Identifier: 9984014018902771

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