Investigating the interaction between white matter and brain state on tDCS-induced changes in brain network activity

TY - JOUR

T1 - Investigating the interaction between white matter and brain state on tDCS-induced changes in brain network activity

AU - Kurtin, Danielle L.

AU - Violante, Ines R.

AU - Zimmerman, Karl

AU - Leech, Robert

AU - Hampshire, Adam

AU - Patel, Maneesh C.

AU - Carmichael, David W.

AU - Sharp, David J.

AU - Li, Lucia M.

N1 - Funding Information: We would like to thank all participants. We would like to thank Dr Jonathan Howard for tireless and insightful technical and methodological assistance, and Dr Alexander Optiz for doing the modelling for peak electric field. This study was conducted at the Imperial College Clinical Imaging Facility. The study was supported by the NIHR Imperial College London Biomedical Research Centre . Funding Information: This work had the following funding: LML was funded by Wellcome Trust Clinical Research Training Fellowship ( 103429/Z/13/Z ) and the NIHR Academic Clinical Lectureship program . I.R.V. was funded by the Wellcome Trust (Ref: 103045/Z/13/Z ) and the BBSRC (Ref: BB/S008314/1 ), DJS is funded by a National Institute for Health Research ( NIHR ) Professorship. Funding Information: This work had the following funding: LML was funded by Wellcome Trust Clinical Research Training Fellowship (103429/Z/13/Z) and the NIHR Academic Clinical Lectureship program. I.R.V. was funded by the Wellcome Trust (Ref: 103045/Z/13/Z) and the BBSRC (Ref: BB/S008314/1), DJS is funded by a National Institute for Health Research (NIHR) Professorship.We would like to thank all participants. We would like to thank Dr Jonathan Howard for tireless and insightful technical and methodological assistance, and Dr Alexander Optiz for doing the modelling for peak electric field. This study was conducted at the Imperial College Clinical Imaging Facility. The study was supported by the NIHR Imperial College London Biomedical Research Centre. Publisher Copyright: © 2021 The Authors Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/9/1

Y1 - 2021/9/1

N2 - BackgroundTranscranial direct current stimulation (tDCS) is a form of noninvasive brain stimulation whose potential as a cognitive therapy is hindered by our limited understanding of how participant and experimental factors influence its effects. Using functional MRI to study brain networks, we have previously shown in healthy controls that the physiological effects of tDCS are strongly influenced by brain state. We have additionally shown, in both healthy and traumatic brain injury (TBI) populations, that the behavioral effects of tDCS are positively correlated with white matter (WM) structure.ObjectivesIn this study we investigate how these two factors, WM structure and brain state, interact to shape the effect of tDCS on brain network activity.MethodsWe applied anodal, cathodal and sham tDCS to the right inferior frontal gyrus (rIFG) of healthy (n = 22) and TBI participants (n = 34). We used the Choice Reaction Task (CRT) performance to manipulate brain state during tDCS. We acquired simultaneous fMRI to assess activity of cognitive brain networks and used Fractional Anisotropy (FA) as a measure of WM structure.ResultsWe find that the effects of tDCS on brain network activity in TBI participants are highly dependent on brain state, replicating findings from our previous healthy control study in a separate, patient cohort. We then show that WM structure further modulates the brain-state dependent effects of tDCS on brain network activity. These effects are not unidirectional - in the absence of task with anodal and cathodal tDCS, FA is positively correlated with brain activity in several regions of the default mode network. Conversely, with cathodal tDCS during CRT performance, FA is negatively correlated with brain activity in a salience network region.ConclusionsOur results show that experimental and participant factors interact to have unexpected effects on brain network activity, and that these effects are not fully predictable by studying the factors in isolation.

AB - BackgroundTranscranial direct current stimulation (tDCS) is a form of noninvasive brain stimulation whose potential as a cognitive therapy is hindered by our limited understanding of how participant and experimental factors influence its effects. Using functional MRI to study brain networks, we have previously shown in healthy controls that the physiological effects of tDCS are strongly influenced by brain state. We have additionally shown, in both healthy and traumatic brain injury (TBI) populations, that the behavioral effects of tDCS are positively correlated with white matter (WM) structure.ObjectivesIn this study we investigate how these two factors, WM structure and brain state, interact to shape the effect of tDCS on brain network activity.MethodsWe applied anodal, cathodal and sham tDCS to the right inferior frontal gyrus (rIFG) of healthy (n = 22) and TBI participants (n = 34). We used the Choice Reaction Task (CRT) performance to manipulate brain state during tDCS. We acquired simultaneous fMRI to assess activity of cognitive brain networks and used Fractional Anisotropy (FA) as a measure of WM structure.ResultsWe find that the effects of tDCS on brain network activity in TBI participants are highly dependent on brain state, replicating findings from our previous healthy control study in a separate, patient cohort. We then show that WM structure further modulates the brain-state dependent effects of tDCS on brain network activity. These effects are not unidirectional - in the absence of task with anodal and cathodal tDCS, FA is positively correlated with brain activity in several regions of the default mode network. Conversely, with cathodal tDCS during CRT performance, FA is negatively correlated with brain activity in a salience network region.ConclusionsOur results show that experimental and participant factors interact to have unexpected effects on brain network activity, and that these effects are not fully predictable by studying the factors in isolation.

KW - Default mode network

KW - Magnetic resonance imaging

KW - Salience network

KW - Stimulation

KW - Traumatic brain injury

KW - White matter structure

UR - http://www.scopus.com/inward/record.url?scp=85113524558&partnerID=8YFLogxK

U2 - 10.1016/j.brs.2021.08.004

DO - 10.1016/j.brs.2021.08.004

M3 - Article

AN - SCOPUS:85113524558

SN - 1935-861X

VL - 14

SP - 1261

EP - 1270

JO - Brain Stimulation

JF - Brain Stimulation

IS - 5

ER -