Abstract
Recent applications of simultaneous scalp electroencephalography (EEG) and transcranial magnetic stimulation (TMS) suggest that adapting stimulation to underlying brain states may enhance neuroplastic effects of TMS. It is often assumed that longer-lasting effects of TMS on brain function may be mediated by phasic interactions between TMS pulses and endogenous cortical oscillatory dynamics. The mechanisms by which TMS exerts its neuromodulatory effects, however, remain unknown. Here, we discuss evidence concerning the functional effects on synaptic plasticity of oscillatory cross-frequency coupling in cortical networks as a potential framework for understanding the neuromodulatory effects of TMS. We first discuss evidence for interactions between endogenous oscillatory brain dynamics and externally induced electromagnetic field activity. Alpha band (8–12 Hz) activities are of special interest here because of the wide application and therapeutic effectiveness of rhythmic TMS (rTMS) using a stimulus repetition frequency at or near 10 Hz. We discuss the large body of literature on alpha oscillations suggesting that alpha oscillatory cycles produce periodic inhibition or excitation of neuronal processing through phase-amplitude coupling (PAC) of low-frequency oscillations with high-frequency broadband (or gamma) bursting. Such alpha-gamma coupling may reflect excitability of neuronal ensembles underlying neuroplasticity effects of TMS. We propose that TMS delivery with simultaneous EEG recording and near real-time estimation of source-resolved alpha-gamma PAC might be used to select the precise timing of TMS pulse deliveries so as to enhance the neuroplastic effects of TMS therapies.
Highlights
Non-invasive transcranial magnetic stimulation (TMS) of the human brain has gained increasing popularity over the last decades and today is being widely used in both research and clinical applications
Timing TMS pulse presentations to specific phases of ongoing oscillatory activity has been demonstrated to increase subsequent corticospinal excitability—a measure of cortical plasticity (Bergmann et al, 2012; Zrenner et al, 2018). This suggests that electric field activity in the brain produced by TMS pulses may enhance underlying cortical excitability which is modulated by oscillatory field activity occurring within distributed brain networks, thereby affecting basic synaptic mechanisms producing long-term potentiation (LTP) and/or depression (LTD) within those networks (Ridding and Rothwell, 2007)
We discuss how high and low excitability states relate to the phase of oscillatory field potentials, and how phase controls excitability states through cross-frequency coupling. Based on this body of research we argue that brain stimulation timed to particular phases of spontaneous low-frequency oscillations may enhance neural excitability, by increasing occurrence of appropriately timed high-frequency gamma oscillations through the mechanism of cross-frequency phase-amplitude coupling (PAC)
Summary
Non-invasive transcranial magnetic stimulation (TMS) of the human brain has gained increasing popularity over the last decades and today is being widely used in both research and clinical applications. Timing TMS pulse presentations to specific phases of ongoing oscillatory activity has been demonstrated to increase subsequent corticospinal excitability—a measure of cortical plasticity (Bergmann et al, 2012; Zrenner et al, 2018). This suggests that electric field activity in the brain produced by TMS pulses may enhance underlying cortical excitability which is modulated by oscillatory field activity occurring within distributed brain networks, thereby affecting basic synaptic mechanisms producing long-term potentiation (LTP) and/or depression (LTD) within those networks (Ridding and Rothwell, 2007).
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