Entrainment of somatosensory beta and gamma oscillations accompany improvement in tactile acuity after periodic and aperiodic repetitive sensory stimulation

Abstract

Previous research showed that repetitive sensory stimulation entrains neural oscillations at the stimulation rate, facilitates long-term potentiation like perceptual learning, and improves behavioural performance. For example, short-time repetitive tactile stimulation improved tactile acuity measured with two-point or spatial orientation discrimination tests. The behavioural gain was maximal for a stimulation rate of 20 Hz, the same frequency at which repetitive somatosensory stimulation elicits a steady-state response with maximum amplitude. The current study investigated whether sensory stimulation must be strictly periodic to induce perceptual learning and whether the 20-Hz steady-state response plays a crucial role in the neural mechanisms of perceptual learning. In a crossover-designed experiment, young, healthy adults received sensory stimulation to the fingertip on three subsequent days. The stimulation was either periodic or temporally randomized (aperiodic) with the same number of stimuli. Tactile acuity was assessed with a grating orientation discrimination task, and brain activity was measured with magnetoencephalography (MEG). Stimulus type-by-session interactions were found for behavioural and brain data. Tactile acuity improved more after a session with aperiodic than periodic stimulation. Beta-band 20-Hz steady-state responses were localized in the primary somatosensory cortex contralateral to the stimulated finger and had larger amplitudes after periodic than aperiodic stimulation. Both stimulus types also elicited gamma oscillations, which increased in amplitude more with aperiodic than periodic stimulation. Sensory stimuli caused a phase reset of sensorimotor beta oscillations phase-coupled to alpha oscillations. The system of stimulus-related oscillations was discussed as underlying temporal processing. Learning may result from facilitating the temporal code. More pronounced behavioural gain with aperiodic than periodic stimulation suggests beneficial effects of temporal stimulus variability for perceptual learning.

Keywords: Entrainment; Gamma oscillations; Perceptual learning; Somatosensory cortex; Steady-state responses; Tactile stimulation.