Modulation of Cortical Oscillations by Low-Frequency Direct Cortical Stimulation Is State-Dependent

Authors:

Alagapan S; Schmidt SL; Lefebvre J; Hadar E; Shin HW; Frohlic h F. Institution Alagapan,Sankaraleengam. Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America. Schmidt,Stephen L. Department of Psychiatry, University of North C arolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ame rica. Schmidt,Stephen L. UNC/NCSU Joint Department of Biomedical Engineering , University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America. Lefebvre,Jeremie. Krembil Research Institute, University Health Netwo rk, Toronto, Ontario, Canada. Lefebvre,Jeremie. Department of Mathematics, University of Toronto, Toronto, Ontario, Canada. Hadar,Eldad. Department of Neurosurgery, University of North Car olina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Shin,Hae Won. Department of Neurosurgery, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Shin,Hae Won. Department of Neurology, University of North C arolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Frohlich,Flavio. Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Frohlich,Flavio. UNC/NCSU Joint Department of Biomedical Engineeri ng, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America. Frohlich,Flavio. Department of Neurology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Frohlich,Flavio. Neurobiology Curriculum, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca. Frohlich,Flavio. Department of Cell Biology and Physiology, Un iversity of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America. Frohlich,Flavio. Neuroscience Center, University of North C arolina at Chapel Hill, Chapel Hill, North Carolina, United States of Ameri ca.

Title:

Modulation of Cortical Oscillations by Low-Frequency Direct Cortical Stimulation Is State-Dependent.

Source:

Plos Biology. 14(3):e1002424, 2016 Mar.

Abstract:

Cortical oscillations play a fundamental role in organizing large-scale functional brain networks. Noninvasive brain stimulation w ith temporally patterned waveforms such as repetitive transcranial magnetic stimul ation (rTMS) and transcranial alternating current stimulation (tACS) h ave been proposed to modulate these oscillations. Thus, these stimulati on modalities represent promising new approaches for the treatment o f psychiatric illnesses in which these oscillations are impair ed. However, the mechanism by which periodic brain stimulation alters endogen ous oscillation dynamics is debated and appears to depend on bra in state. Here, we demonstrate with a static model and a neural oscillator model that recurrent excitation in the thalamo-cortical circuit, to gether with recruitment of cortico-cortical connections, can explain the enhancement of oscillations by brain stimulation as a function of brain state. We then performed concurrent invasive recording and stimulation of the human cortical surface to elucidate the response of cortical oscillat ions to periodic stimulation and support the findings from the comp utational models. We found that (1) stimulation enhanced the targeted osc illation power, (2) this enhancement outlasted stimulation, and (3) t he effect of stimulation depended on behavioral state. Together, our results show successful target engagement of oscillations by periodic brai n stimulation and highlight the role of nonlinear interaction between endo genous network oscillations and stimulation. These mechanistic insights will contribute to the design of adaptive, more targeted stimulation paradigms .

Publication Type:

Journal Article. Research Support, N.I.H., Extramural. Research Support, Non-U.S. Gov’t.