Abstract

Neural entrainment is the synchronization of neural activity to the frequency of repetitive external stimuli, which can be observed as an increase in the electroencephalogram (EEG) power spectrum at the driving frequency, -also known as the steady-state response. Although it has been systematically reported that the entrained EEG oscillation persists for approximately three cycles after stimulus offset, the neural mechanisms underpinning it remain unknown. Focusing on alpha oscillations, we adopt the dynamical excitation/inhibition framework, which suggests that phases of entrained EEG signals correspond to alternating excitatory/inhibitory states of the neural circuitry. We hypothesize that the duration of the persistence of entrainment is determined by the specific functional state of the entrained neural network at the time the stimulus ends. Steady-state visually evoked potentials (SSVEP) were elicited in 19 healthy volunteers at the participants’ individual alpha peaks. Visual stimulation consisted of a sinusoidally-varying light terminating at one of four phases: 0, π/2, π, and 3π/2. The persistence duration of the oscillatory activity was analyzed as a function of the terminating phase of the stimulus. Phases of the SSVEP at the stimulus termination were distributed within a constant range of values relative to the phase of the stimulus. Longer persistence durations were obtained when visual stimulation terminated towards the troughs of the alpha oscillations, while shorter persistence durations occurred when stimuli terminated near the peaks. Source localization analysis suggests that the persistence of entrainment reflects the functioning of fronto-occipital neuronal circuits, which might prime the sensory representation of incoming visual stimuli based on predictions about stimulus rhythmicity. Consequently, different states of the network at the end of the stimulation, corresponding to different states of intrinsic neuronal coupling, may determine the time windows over which coding of incoming sensory stimulation is modulated by the preceding oscillatory activity.

Highlights

  • Neural entrainment refers to the synchronization of neural activity with the periodic properties of external stimuli

  • The analysis of the topographic distribution of the state visually evoked potentials (SSVEP) revealed that the increase in the power of alpha oscillations resulting from the visual stimulation was located in occipital scalp locations (Figure 3B)

  • When visual stimulation ended at rising phases of the sinusoidal wave

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Summary

Introduction

Neural entrainment refers to the synchronization of neural activity with the periodic properties of external stimuli. Entrainment can occur without power enhancement, if only the phase of the intrinsic oscillations is aligned to the external force. Multiple oscillators are recorded in the electroencephalogram (EEG), their aligned phases add up and appear like an enhanced amplitude (Notbohm et al, 2016). When periodic visual stimulation is presented, entrainment can lead to the generation of steady-state visually evoked potentials (SSVEP), i.e., scalp-recorded brain oscillations locked to the periodicity of the visual stimuli, which have relatively constant amplitude and phase over the stimulation interval. Evidence suggests that at least part of the SSVEP driven by visual stimulation in the alpha band of the EEG (8–14 Hz) can be attributed to the entrainment of alpha neural generators (Mathewson et al, 2012; Zauner et al, 2012; Spaak et al, 2014; Notbohm et al, 2016; Gulbinaite et al, 2017)

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