Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations during Perception.

Abstract

Auditory and sensorimotor brain areas interact during the action-perception cycle of sound making. Neurophysiological evidence of a feedforward model of the action and its outcome has been associated with attenuation of the N1 wave of auditory evoked responses elicited by self-generated sounds, such as talking and singing or playing a musical instrument. Moreover, neural oscillations at β-band frequencies have been related to predicting the sound outcome after action initiation. We hypothesized that a newly learned action-perception association would immediately modify interpretation of the sound during subsequent listening. Nineteen healthy young adults (7 female, 12 male) participated in three magnetoencephalographic recordings while first passively listening to recorded sounds of a bell ringing, then actively striking the bell with a mallet, and then again listening to recorded sounds. Auditory cortex activity showed characteristic P1-N1-P2 waves. The N1 was attenuated during sound making, while P2 responses were unchanged. In contrast, P2 became larger when listening after sound making compared with the initial naive listening. The P2 increase occurred immediately, while in previous learning-by-listening studies P2 increases occurred on a later day. Also, reactivity of β-band oscillations, as well as θ coherence between auditory and sensorimotor cortices, was stronger in the second listening block. These changes were significantly larger than those observed in control participants (eight female, five male), who triggered recorded sounds by a key press. We propose that P2 characterizes familiarity with sound objects, whereas β-band oscillation signifies involvement of the action-perception cycle, and both measures objectively indicate functional neuroplasticity in auditory perceptual learning.SIGNIFICANCE STATEMENT While suppression of auditory responses to self-generated sounds is well known, it is not clear whether the learned action-sound association modifies subsequent perception. Our study demonstrated the immediate effects of sound-making experience on perception using magnetoencephalographic recordings, as reflected in the increased auditory evoked P2 wave, increased responsiveness of β oscillations, and enhanced connectivity between auditory and sensorimotor cortices. The importance of motor learning was underscored as the changes were much smaller in a control group using a key press to generate the sounds instead of learning to play the musical instrument. The results support the rapid integration of a feedforward model during perception and provide a neurophysiological basis for the application of music making in motor rehabilitation training.