Highlights
- •Endogenous oscillations constrain neuromodulation by weak electric fields.
- •Weak electric fields enhance neocortical oscillations by resonance.
- •Frequency-matched tACS is likely most effective for enhancement of cortical rhythms.
Abstract
Background
Transcranial alternating current stimulation (tACS) is a non-invasive brain stimulation
modality that may modulate cognition by enhancing endogenous neocortical oscillations
by application of sine-wave electric fields. Yet, the role of endogenous network activity
in enabling and shaping the effects of tACS has remained unclear.
Objective
We combined optogenetic stimulation and multichannel slice electrophysiology to elucidate
how the effect of a weak sine-wave electric field depends on the ongoing cortical
oscillatory activity. We hypothesized that endogenous cortical oscillations constrain
neuromodulation by tACS.
Methods
We studied the effect of weak sine-wave electric fields on oscillatory activity in
mouse neocortical slices. Optogenetic control of the network activity enabled the
generation of in vivo-like cortical oscillations for studying the temporal relationship between network
activity and sine-wave electric field stimulation.
Results
Weak electric fields enhanced endogenous oscillations but failed to induce a frequency
shift of the ongoing oscillation for stimulation frequencies that were not matched
to the endogenous oscillation. This constraint on the effect of electric field stimulation
imposed by endogenous network dynamics was limited to the case of weak electric fields
targeting in vivo-like network dynamics. Together, these results suggest that the key mechanism of
tACS may be enhancing, but not overriding, intrinsic network dynamics.
Conclusion
Our results contribute to understanding the inconsistent tACS results from human studies
and propose that stimulation precisely adjusted in frequency to the endogenous oscillations
is key to rational design of non-invasive brain stimulation paradigms.
Keywords
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Article info
Publication history
Published online: July 18, 2014
Accepted:
July 13,
2014
Received in revised form:
June 18,
2014
Received:
March 11,
2014
Footnotes
Authorship statement: SS and FF designed the experiments; SS, AI, and AF performed the experiments; SS analyzed the data; MB validated the analysis code, and SS and FF wrote the paper.
The authors declare no competing financial interests.
A small subset of the data included in this manuscript was previously presented in abstract form (6th IEEE Neuroengineering Meeting 2013 and SfN 2013, both San Diego).
Research reported in this publication was supported in part by the National Institute of Mental Health of the National Institutes of Health under Award Number R01MH101547. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. AAF was funded by the Summer Undergraduate Research Fellowship from the Office of Undergraduate Research at University of North Carolina at Chapel Hill.
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© 2014 Elsevier Inc. Published by Elsevier Inc. All rights reserved.
