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

Oya, Hiroyuki and Howard, Matthew A. and Magnotta, Vincent A. and Kruger, Anton and Griffiths, Timothy D. and Lemieux, Louis and Carmichael, David W. and Petkov, Christopher I. and Kawasaki, Hiroto and Kovach, Christopher K. and Sutterer, Matthew J. and Adolphs, Ralph (2017) Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI. Journal of Neuroscience Methods, 277 . pp. 101-112. ISSN 0165-0270. https://resolver.caltech.edu/CaltechAUTHORS:20170104-155858584

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Abstract

Background: 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. New method: Here, we demonstrate the safety and scientific promise of a novel and complementary approach: concurrent electrical stimulation and fMRI (es-fMRI) at 3 T in awake neurosurgical patients with implanted depth electrodes. Results: 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 11 min 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. Conclusions: 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.jneumeth.2016.12.014DOIArticle
http://www.sciencedirect.com/science/article/pii/S0165027016302965PublisherArticle
ORCID:
AuthorORCID
Adolphs, Ralph0000-0002-8053-9692
Additional Information:© 2016 Elsevier B.V. Received 20 September 2016; Received in revised form 22 November 2016; Accepted 20 December 2016; Available online 21 December 2016. Support for this work was provided by the National Institute on Deafness and Other Communication Disorders (R01-DC04290), National Center for Research Resources (UL1RR024979), and an NIMH Conte Center (P50MH094258). We thank Haiming Chen, Phillip Gander, Rick Reale for assistance with conducting the experiments, and Jeremy Greenlee, Goldie Boone, Julien Dubois, Swaloop Guntapalli and Tim Tierney for helpful discussion. We thank our patients for their contribution.
Funders:
Funding AgencyGrant Number
NIHR01-DC04290
NIHUL1RR024979
NIHP50MH094258A
National Institute on Deafness and Other Communication DisordersUNSPECIFIED
National Institute of Mental Health (NIMH)UNSPECIFIED
Subject Keywords:Effective connectivity; Human; Electrical stimulation; Functional MRI; DBS; Amygdala
Record Number:CaltechAUTHORS:20170104-155858584
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170104-155858584
Official Citation: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, Mapping effective connectivity in the human brain with concurrent intracranial electrical stimulation and BOLD-fMRI, Journal of Neuroscience Methods, Volume 277, 1 February 2017, Pages 101-112, ISSN 0165-0270, http://dx.doi.org/10.1016/j.jneumeth.2016.12.014. (http://www.sciencedirect.com/science/article/pii/S0165027016302965)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:73238
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:05 Jan 2017 00:16
Last Modified:03 Oct 2019 16:25

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