Bihemispheric sensorimotor oscillatory network states determine cortical responses to transcranial magnetic stimulation

BACKGROUND: Brain responses to external stimuli vary with fluctuating states of neuronal activity. Previous work has demonstrated effects of phase and power of the ongoing local sensorimotor μ-alpha-oscillation on responses to transcranial magnetic stimulation (TMS) of motor cortex (M1). However, M1 is part of a distributed network, and the effects of oscillatory activity in this network on TMS-evoked EEG responses (TEPs) have not been explored. OBJECTIVES: To determine the effects of oscillatory activity in the bihemispheric sensorimotor network on TEPs. METHODS: 31 healthy subjects received single-pulse TMS of the left M1 hand area during EEG recording. Ongoing bihemispheric sensorimotor cortex oscillatory states were reconstructed from the EEG directly preceding TMS, and inferred by a data-driven method combining a multivariate autoregressive model and a Hidden Markov model. TEP amplitudes (P25, N45, P70, N100 and P180) were then compared between different bihemispheric sensorimotor cortex oscillatory states. RESULTS: Four bihemispheric sensorimotor cortex oscillatory states were identified, with different interhemispheric expressions of theta and alpha oscillations. High alpha-power states in the stimulated sensorimotor cortex increased P25 amplitude. Alpha power in the alpha-alpha state (stimulated - non-stimulated hemisphere) correlated in both hemispheres with N45 amplitude. Theta power in the alpha-theta state correlated in the non-stimulated hemisphere with P70 amplitude. CONCLUSIONS: Bihemispheric sensorimotor cortex oscillatory states contribute to TEPs, with a relevance shift from stimulated to non-stimulated M1 from P25 over N45 to P70. This significantly extends previous findings: not only ongoing local oscillations but distributed network oscillatory states determine cortical responsiveness to external stimuli.