Cognitive enhancement with Salience Network electrical stimulation is influenced by network structural connectivity

Lucia M. Li; Ines R. Violante; Rob Leech; Adam Hampshire; Alexander Opitz; David McArthur; David W. Carmichael; David J. Sharp

doi:10.1016/j.neuroimage.2018.10.069

Cognitive enhancement with Salience Network electrical stimulation is influenced by network structural connectivity

Lucia M. Li, Ines R. Violante, Rob Leech, Adam Hampshire, Alexander Opitz, David McArthur, David W. Carmichael, David J. Sharp

Biomedical Engineering

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29 Scopus citations

Abstract

The Salience Network (SN) and its interactions are important for cognitive control. We have previously shown that structural damage to the SN is associated with abnormal functional connectivity between the SN and Default Mode Network (DMN), abnormal DMN deactivation, and impaired response inhibition, which is an important aspect of cognitive control. This suggests that stimulating the SN might enhance cognitive control. Here, we tested whether non-invasive transcranial direct current stimulation (TDCS) could be used to modulate activity within the SN and enhance cognitive control. TDCS was applied to the right inferior frontal gyrus/anterior insula cortex during performance of the Stop Signal Task (SST) and concurrent functional (f)MRI. Anodal TDCS improved response inhibition. Furthermore, stratification of participants based on SN structural connectivity showed that it was an important influence on both behavioural and physiological responses to anodal TDCS. Participants with high fractional anisotropy within the SN showed improved SST performance and increased activation of the SN with anodal TDCS, whilst those with low fractional anisotropy within the SN did not. Cathodal stimulation of the SN produced activation of the right caudate, an effect which was not modulated by SN structural connectivity. Our results show that stimulation targeted to the SN can improve response inhibition, supporting the causal influence of this network on cognitive control and confirming it as a target to produce cognitive enhancement. Our results also highlight the importance of structural connectivity as a modulator of network to TDCS, which should guide the design and interpretation of future stimulation studies.

Original language	English (US)
Pages (from-to)	425-433
Number of pages	9
Journal	NeuroImage
Volume	185
DOIs	https://doi.org/10.1016/j.neuroimage.2018.10.069
State	Published - Jan 15 2019

Bibliographical note

Funding Information:
LML is supported by a Wellcome Trust Clinical Research Training Fellowship (103429/Z/13/Z). IV is supported by a Sir Henry Wellcome Trust Fellowship (103045/Z/13/Z) and receives funding from the NIHR Imperial BRC. AO is supported in parts by NIH grants MH110217 and MH111439. DJS is supported by a National Institute for Health Research (NIHR) Professorship (NIHR-RP-011-048). We would like to thank Dr Jonathan Howard for tireless and insightful technical and methodological assistance. The study was supported by the NIHR Imperial College London Biomedical Research Centre, and the Imperial College Clinical Imaging Facility.

Publisher Copyright:
© 2018 The Authors

Keywords

Cognitive control
Fractional anisotropy
Functional MRI
Response inhibition
Salience Network
Stop Signal Task
TDCS
Transcranial direct current stimulation
White matter tract

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title = "Cognitive enhancement with Salience Network electrical stimulation is influenced by network structural connectivity",

abstract = "The Salience Network (SN) and its interactions are important for cognitive control. We have previously shown that structural damage to the SN is associated with abnormal functional connectivity between the SN and Default Mode Network (DMN), abnormal DMN deactivation, and impaired response inhibition, which is an important aspect of cognitive control. This suggests that stimulating the SN might enhance cognitive control. Here, we tested whether non-invasive transcranial direct current stimulation (TDCS) could be used to modulate activity within the SN and enhance cognitive control. TDCS was applied to the right inferior frontal gyrus/anterior insula cortex during performance of the Stop Signal Task (SST) and concurrent functional (f)MRI. Anodal TDCS improved response inhibition. Furthermore, stratification of participants based on SN structural connectivity showed that it was an important influence on both behavioural and physiological responses to anodal TDCS. Participants with high fractional anisotropy within the SN showed improved SST performance and increased activation of the SN with anodal TDCS, whilst those with low fractional anisotropy within the SN did not. Cathodal stimulation of the SN produced activation of the right caudate, an effect which was not modulated by SN structural connectivity. Our results show that stimulation targeted to the SN can improve response inhibition, supporting the causal influence of this network on cognitive control and confirming it as a target to produce cognitive enhancement. Our results also highlight the importance of structural connectivity as a modulator of network to TDCS, which should guide the design and interpretation of future stimulation studies.",

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note = "Funding Information: LML is supported by a Wellcome Trust Clinical Research Training Fellowship (103429/Z/13/Z). IV is supported by a Sir Henry Wellcome Trust Fellowship (103045/Z/13/Z) and receives funding from the NIHR Imperial BRC. AO is supported in parts by NIH grants MH110217 and MH111439. DJS is supported by a National Institute for Health Research (NIHR) Professorship (NIHR-RP-011-048). We would like to thank Dr Jonathan Howard for tireless and insightful technical and methodological assistance. The study was supported by the NIHR Imperial College London Biomedical Research Centre, and the Imperial College Clinical Imaging Facility. Publisher Copyright: {\textcopyright} 2018 The Authors",

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AU - Hampshire, Adam

AU - Opitz, Alexander

AU - McArthur, David

AU - Carmichael, David W.

AU - Sharp, David J.

N1 - Funding Information: LML is supported by a Wellcome Trust Clinical Research Training Fellowship (103429/Z/13/Z). IV is supported by a Sir Henry Wellcome Trust Fellowship (103045/Z/13/Z) and receives funding from the NIHR Imperial BRC. AO is supported in parts by NIH grants MH110217 and MH111439. DJS is supported by a National Institute for Health Research (NIHR) Professorship (NIHR-RP-011-048). We would like to thank Dr Jonathan Howard for tireless and insightful technical and methodological assistance. The study was supported by the NIHR Imperial College London Biomedical Research Centre, and the Imperial College Clinical Imaging Facility. Publisher Copyright: © 2018 The Authors

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N2 - The Salience Network (SN) and its interactions are important for cognitive control. We have previously shown that structural damage to the SN is associated with abnormal functional connectivity between the SN and Default Mode Network (DMN), abnormal DMN deactivation, and impaired response inhibition, which is an important aspect of cognitive control. This suggests that stimulating the SN might enhance cognitive control. Here, we tested whether non-invasive transcranial direct current stimulation (TDCS) could be used to modulate activity within the SN and enhance cognitive control. TDCS was applied to the right inferior frontal gyrus/anterior insula cortex during performance of the Stop Signal Task (SST) and concurrent functional (f)MRI. Anodal TDCS improved response inhibition. Furthermore, stratification of participants based on SN structural connectivity showed that it was an important influence on both behavioural and physiological responses to anodal TDCS. Participants with high fractional anisotropy within the SN showed improved SST performance and increased activation of the SN with anodal TDCS, whilst those with low fractional anisotropy within the SN did not. Cathodal stimulation of the SN produced activation of the right caudate, an effect which was not modulated by SN structural connectivity. Our results show that stimulation targeted to the SN can improve response inhibition, supporting the causal influence of this network on cognitive control and confirming it as a target to produce cognitive enhancement. Our results also highlight the importance of structural connectivity as a modulator of network to TDCS, which should guide the design and interpretation of future stimulation studies.

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Cognitive enhancement with Salience Network electrical stimulation is influenced by network structural connectivity

Abstract

Bibliographical note

Keywords

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