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

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Creator
  • Alagapan, Sankaraleengam
    • Affiliation: School of Medicine, Department of Psychiatry
  • Schmidt, Stephen L.
    • Affiliation: School of Medicine, Department of Psychiatry
    • Other Affiliation: University of North Carolina at Chapel Hill
  • Lefebvre, Jérémie
    • Other Affiliation: Krembil Research Institute; University Health Network
  • Hadar, Eldad
    • Affiliation: School of Medicine, Department of Neurosurgery
  • Shin, Hae Won
    • Affiliation: School of Medicine, Department of Neurosurgery
    • Other Affiliation: Department of Neurology
  • Frӧhlich, Flavio
    • Affiliation: School of Medicine, Department of Psychiatry
    • Other Affiliation: Neuroscience Curriculum
Abstract
  • Cortical oscillations play a fundamental role in organizing large-scale functional brain networks. Noninvasive brain stimulation with temporally patterned waveforms such as repetitive transcranial magnetic stimulation (rTMS) and transcranial alternating current stimulation (tACS) have been proposed to modulate these oscillations. Thus, these stimulation modalities represent promising new approaches for the treatment of psychiatric illnesses in which these oscillations are impaired. However, the mechanism by which periodic brain stimulation alters endogenous oscillation dynamics is debated and appears to depend on brain state. Here, we demonstrate with a static model and a neural oscillator model that recurrent excitation in the thalamo-cortical circuit, together 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 oscillations to periodic stimulation and support the findings from the computational models. We found that (1) stimulation enhanced the targeted oscillation power, (2) this enhancement outlasted stimulation, and (3) the effect of stimulation depended on behavioral state. Together, our results show successful target engagement of oscillations by periodic brain stimulation and highlight the role of nonlinear interaction between endogenous network oscillations and stimulation. These mechanistic insights will contribute to the design of adaptive, more targeted stimulation paradigms.
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  • Article
Rights statement
  • In Copyright
Journal title
  • PLoS Biology
Journal volume
  • 14
Journal issue
  • 3
Page start
  • e1002424
Language
  • English
ISSN
  • 1545-7885
  • 1544-9173
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