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Human Auditory-Motor Networks Show Frequency-Specific Phase-Based Coupling in Resting-State MEG

Authors: Bedford ONoly-Gandon AAra AWiesman AIAlbouy PBaillet SPenhune VZatorre RJ


Affiliations

1 Montreal Neurological Institute, McGill University, Montréal, Quebec, Canada.
2 International Laboratory for Brain, Music and Sound Research (BRAMS), Montréal, Quebec, Canada.
3 Centre for Research on Brain, Language and Music (CRBLM), McGill University, Montréal, Quebec, Canada.
4 CERVO Brain Research Centre, School of Psychology, Université Laval, Québec City, Quebec, Canada.
5 Department of Psychology, Concordia University, Montréal, Quebec, Canada.

Description

Perception and production of music and speech rely on auditory-motor coupling, a mechanism which has been linked to temporally precise oscillatory coupling between auditory and motor regions of the human brain, particularly in the beta frequency band. Recently, brain imaging studies using magnetoencephalography (MEG) have also shown that accurate auditory temporal predictions specifically depend on phase coherence between auditory and motor cortical regions. However, it is not yet clear whether this tight oscillatory phase coupling is an intrinsic feature of the auditory-motor loop, or whether it is only elicited by task demands. Further, we do not know if phase synchrony is uniquely enhanced in the auditory-motor system compared to other sensorimotor modalities, or to which degree it is amplified by musical training. In order to resolve these questions, we measured the degree of phase locking between motor regions and auditory or visual areas in musicians and non-musicians using resting-state MEG. We derived phase locking values (PLVs) and phase transfer entropy (PTE) values from 90 healthy young participants. We observed significantly higher PLVs across all auditory-motor pairings compared to all visuomotor pairings in all frequency bands. The pairing with the highest degree of phase synchrony was right primary auditory cortex with right ventral premotor cortex, a connection which has been highlighted in previous literature on auditory-motor coupling. Additionally, we observed that auditory-motor and visuomotor PLVs were significantly higher across all structures in the right hemisphere, and we found the highest differences between auditory and visual PLVs in the theta, alpha, and beta frequency bands. Last, we found that the theta and beta bands exhibited a preference for a motor-to-auditory PTE direction and that the alpha and gamma bands exhibited the opposite preference for an auditory-to-motor PTE direction. Taken together, these findings confirm our hypotheses that motor phase synchrony is significantly enhanced in auditory compared to visual cortical regions at rest, that these differences are highest across the theta-beta spectrum of frequencies, and that there exist alternating information flow loops across auditory-motor structures as a function of frequency. In our view, this supports the existence of an intrinsic, time-based coupling for low-latency integration of sounds and movements which involves synchronized phasic activity between primary auditory cortex with motor and premotor cortical areas.


Keywords: auditory-motor functional connectivityauditory-motor integrationintrinsic connectivityphase couplingresting state MEG


Links

PubMed: https://pubmed.ncbi.nlm.nih.gov/39757971/

DOI: 10.1002/hbm.70045