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Research Article

Selective modulation of interhemispheric connectivity by transcranial alternating current stimulation influences binaural integration

View ORCID ProfileBasil C. Preisig, View ORCID ProfileLars Riecke, View ORCID ProfileMatthias J. Sjerps, View ORCID ProfileAnne Kösem, View ORCID ProfileBenjamin R. Kop, View ORCID ProfileBob Bramson, View ORCID ProfilePeter Hagoort, and View ORCID ProfileAlexis Hervais-Adelman
  1. aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
  2. bMax Planck Institute for Psycholinguistics, 6525 XD Nijmegen, The Netherlands;
  3. cDepartment of Psychology, Neurolinguistics, University of Zurich, 8050 Zurich, Switzerland;
  4. dDepartment of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6229 GT Maastricht, The Netherlands;
  5. eLyon Neuroscience Research Center, Cognition Computation and Neurophysiology Team, Université Claude Bernard Lyon 1, 69500 Bron, France;
  6. fNeuroscience Center Zurich, University of Zurich and Eidgenössische Technische Hochschule Zurich, 8057 Zurich, Switzerland

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PNAS February 16, 2021 118 (7) e2015488118; https://doi.org/10.1073/pnas.2015488118
Basil C. Preisig
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
bMax Planck Institute for Psycholinguistics, 6525 XD Nijmegen, The Netherlands;
cDepartment of Psychology, Neurolinguistics, University of Zurich, 8050 Zurich, Switzerland;
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  • ORCID record for Basil C. Preisig
  • For correspondence: basilpreisig@gmx.ch
Lars Riecke
dDepartment of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6229 GT Maastricht, The Netherlands;
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  • ORCID record for Lars Riecke
Matthias J. Sjerps
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
bMax Planck Institute for Psycholinguistics, 6525 XD Nijmegen, The Netherlands;
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  • ORCID record for Matthias J. Sjerps
Anne Kösem
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
bMax Planck Institute for Psycholinguistics, 6525 XD Nijmegen, The Netherlands;
eLyon Neuroscience Research Center, Cognition Computation and Neurophysiology Team, Université Claude Bernard Lyon 1, 69500 Bron, France;
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  • ORCID record for Anne Kösem
Benjamin R. Kop
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
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Bob Bramson
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
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Peter Hagoort
aDonders Institute for Brain, Cognition, and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
bMax Planck Institute for Psycholinguistics, 6525 XD Nijmegen, The Netherlands;
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Alexis Hervais-Adelman
cDepartment of Psychology, Neurolinguistics, University of Zurich, 8050 Zurich, Switzerland;
fNeuroscience Center Zurich, University of Zurich and Eidgenössische Technische Hochschule Zurich, 8057 Zurich, Switzerland
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  1. Edited by Barry Giesbrecht, University of California, Santa Barbara, CA, and accepted by Editorial Board Member Michael S. Gazzaniga January 6, 2021 (received for review July 30, 2020)

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Significance

Sensory processing depends upon the integration of widely distributed neural assemblies. During every day listening, our ears receive different information (due to interaural time and amplitude differences) and it is known that both hemispheres extract different acoustic features. Nonetheless, acoustic features belonging to the same source become integrated. It has been suggested that the brain overcomes this “binding problem” by synchronization of oscillatory activity across the relevant regions. Here we probe interhemispheric oscillatory synchronization as a mechanism for acoustic feature binding using bihemispheric transcranial alternating current stimulation. Concurrent functional MRI reveals that antiphase stimulation of auditory areas changes effective connectivity between these areas, and that this change in connectivity predicts perceptual integration of dichotic stimuli.

Abstract

Brain connectivity plays a major role in the encoding, transfer, and integration of sensory information. Interregional synchronization of neural oscillations in the γ-frequency band has been suggested as a key mechanism underlying perceptual integration. In a recent study, we found evidence for this hypothesis showing that the modulation of interhemispheric oscillatory synchrony by means of bihemispheric high-density transcranial alternating current stimulation (HD-TACS) affects binaural integration of dichotic acoustic features. Here, we aimed to establish a direct link between oscillatory synchrony, effective brain connectivity, and binaural integration. We experimentally manipulated oscillatory synchrony (using bihemispheric γ-TACS with different interhemispheric phase lags) and assessed the effect on effective brain connectivity and binaural integration (as measured with functional MRI and a dichotic listening task, respectively). We found that TACS reduced intrahemispheric connectivity within the auditory cortices and antiphase (interhemispheric phase lag 180°) TACS modulated connectivity between the two auditory cortices. Importantly, the changes in intra- and interhemispheric connectivity induced by TACS were correlated with changes in perceptual integration. Our results indicate that γ-band synchronization between the two auditory cortices plays a functional role in binaural integration, supporting the proposed role of interregional oscillatory synchrony in perceptual integration.

  • speech perception
  • transcranial alternating current stimulation
  • fMRI
  • dynamic causal modeling
  • dichotic listening

Footnotes

  • ↵1To whom correspondence may be addressed. Email: basilpreisig{at}gmx.ch.
  • Author contributions: B.C.P., L.R., M.J.S., and A.H.-A. designed research; B.R.K. and B.B. performed research; B.C.P. analyzed data; and B.C.P., L.R., M.J.S., A.K., B.B., P.H., and A.H.-A. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission. B.G. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2015488118/-/DCSupplemental.

Data Availability.

Data have been deposited in di.dccn.DSC_3011204.02_657 (https://doi.org/10.34973/dt33-sj34).

Change History

February 11, 2021: The author line has been updated.

Published under the PNAS license.

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Selective modulation of interhemispheric connectivity by transcranial alternating current stimulation influences binaural integration
Basil C. Preisig, Lars Riecke, Matthias J. Sjerps, Anne Kösem, Benjamin R. Kop, Bob Bramson, Peter Hagoort, Alexis Hervais-Adelman
Proceedings of the National Academy of Sciences Feb 2021, 118 (7) e2015488118; DOI: 10.1073/pnas.2015488118

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Selective modulation of interhemispheric connectivity by transcranial alternating current stimulation influences binaural integration
Basil C. Preisig, Lars Riecke, Matthias J. Sjerps, Anne Kösem, Benjamin R. Kop, Bob Bramson, Peter Hagoort, Alexis Hervais-Adelman
Proceedings of the National Academy of Sciences Feb 2021, 118 (7) e2015488118; DOI: 10.1073/pnas.2015488118
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Proceedings of the National Academy of Sciences: 118 (7)
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