Tags

Type your tag names separated by a space and hit enter

Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations during Perception.
J Neurosci. 2017 06 14; 37(24):5948-5959.JN

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.

Authors+Show Affiliations

Rotman Research Institute, Baycrest Centre, Toronto, Ontario M6A 2E1, Canada, bross@research.baycrest.org. Department of Medical Biophysics, University of Toronto, Toronto, Ontario M5G 2M9, Canada, and.Rotman Research Institute, Baycrest Centre, Toronto, Ontario M6A 2E1, Canada.Center for Computer Research in Music and Acoustics, Department of Music, and. Stanford Neurosciences Institute, Stanford University, Stanford, California 94305.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28539421

Citation

Ross, Bernhard, et al. "Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations During Perception." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 37, no. 24, 2017, pp. 5948-5959.
Ross B, Barat M, Fujioka T. Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations during Perception. J Neurosci. 2017;37(24):5948-5959.
Ross, B., Barat, M., & Fujioka, T. (2017). Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations during Perception. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 37(24), 5948-5959. https://doi.org/10.1523/JNEUROSCI.3613-16.2017
Ross B, Barat M, Fujioka T. Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations During Perception. J Neurosci. 2017 06 14;37(24):5948-5959. PubMed PMID: 28539421.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Sound-Making Actions Lead to Immediate Plastic Changes of Neuromagnetic Evoked Responses and Induced β-Band Oscillations during Perception. AU - Ross,Bernhard, AU - Barat,Masihullah, AU - Fujioka,Takako, Y1 - 2017/05/24/ PY - 2016/11/23/received PY - 2017/04/18/revised PY - 2017/05/13/accepted PY - 2017/5/26/pubmed PY - 2017/8/19/medline PY - 2017/5/26/entrez KW - N1 suppression KW - action–perception association KW - auditory evoked responses KW - learning-induced plasticity KW - magnetoencephalography KW - β oscillation SP - 5948 EP - 5959 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 37 IS - 24 N2 - 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. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/28539421/Sound_Making_Actions_Lead_to_Immediate_Plastic_Changes_of_Neuromagnetic_Evoked_Responses_and_Induced_β_Band_Oscillations_during_Perception_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=28539421 DB - PRIME DP - Unbound Medicine ER -