Selective modulation of interhemispheric connectivity by transcranial alternating current stimulation influences binaural integration
- 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;
- dDepartment of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6229 GT Maastricht, The Netherlands;
- eLyon Neuroscience Research Center, Cognition Computation and Neurophysiology Team, Université Claude Bernard Lyon 1, 69500 Bron, France;
- fNeuroscience Center Zurich, University of Zurich and Eidgenössische Technische Hochschule Zurich, 8057 Zurich, Switzerland
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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)

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.
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