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

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.

Transcranial Alternating Current Stimulation at Beta Frequency: Lack of Immediate Effects on Excitation and Interhemispheric Inhibition of the Human Motor Cortex

“…Since we also applied 20 Hz tACS, but at rest, it is possible that this frequency band is primarily effective when background activity is modulated (by task activation) and not at rest. Indeed, previous study found brainstate dependent effects of tACS (Feurra et al, 2013; Neuling et al, 2013; Alagapan et al, 2016; Ruhnau et al, 2016). Therefore, it might be interesting to alter the task context to see whether effects of tACS are context-dependent and differ from effects of tACS on resting IHI.…”

Feedback-Controlled Transcranial Alternating Current Stimulation Reveals a Functional Role of Sleep Spindles in Motor Memory Consolidation

“…However, they focused on alpha activity during wakefulness and a different mechanism might hold true for sleep. A recent report from our group [53] showed stimulation effects that outlast stimulation depended on the specific state in wakefulness. Moreover, using a computational model, the study suggested that recurrent connections in thalamo-cortical and cortico-cortical loops led to outlasting effects of stimulation.…”

Oscillatory Dynamics of Prefrontal Cognitive Control

“…Novel brain stimulation tools such as rTMS [5], tACS [18] or direct cortical stimulation [125] allow entraining distinct spectral signatures to subsequently study cross-frequency interactions. Using this approach, it has been demonstrated that both alpha and gamma oscillations might drive CFC interactions, which allows for true bidirectional information integration across temporal scales [78].…”