Mental operations in rhythm: Motor-to-sensory transformation mediates imagined singing.

Yanzhu Li,Huan Luo,Xing Tian,Hugo Merchant

doi:10.1371/journal.pbio.3000504

Abstract

What enables the mental activities of thinking verbally or humming in our mind? We hypothesized that the interaction between motor and sensory systems induces speech and melodic mental representations, and this motor-to-sensory transformation forms the neural basis that enables our verbal thinking and covert singing. Analogous with the neural entrainment to auditory stimuli, participants imagined singing lyrics of well-known songs rhythmically while their neural electromagnetic signals were recorded using magnetoencephalography (MEG). We found that when participants imagined singing the same song in similar durations across trials, the delta frequency band (1-3 Hz, similar to the rhythm of the songs) showed more consistent phase coherence across trials. This neural phase tracking of imagined singing was observed in a frontal-parietal-temporal network: the proposed motor-to-sensory transformation pathway, including the inferior frontal gyrus (IFG), insula (INS), premotor area, intra-parietal sulcus (IPS), temporal-parietal junction (TPJ), primary auditory cortex (Heschl's gyrus [HG]), and superior temporal gyrus (STG) and sulcus (STS). These results suggest that neural responses can entrain the rhythm of mental activity. Moreover, the theta-band (4-8 Hz) phase coherence was localized in the auditory cortices. The mu (9-12 Hz) and beta (17-20 Hz) bands were observed in the right-lateralized sensorimotor systems that were consistent with the singing context. The gamma band was broadly manifested in the observed network. The coherent and frequency-specific activations in the motor-to-sensory transformation network mediate the internal construction of perceptual representations and form the foundation of neural computations for mental operations.

Highlights

The phase-coherence analysis revealed that the significant differences (pcorr(FDR) < 0.05) between the inter-trial phase coherence (ITC) of the within-group and between-group were localized mostly in the primary auditory cortex (Heschl’s gyrus [HG]) and its adjacent areas, including the left anterior superior temporal gyrus and sulcus, and bilateral posterior insula (Fig 2C). (See S1 Fig and S1 Table for precise anatomical locations.) These results suggest that auditory systems can reliably follow the rhythm of acoustic signals and demonstrate the validity and accuracy of source localization based on phase coherence
We investigated the function and dynamics of neural networks that mediate the mental operations of inner speech and covert singing
With a rhythmic entrainment imagined singing paradigm, we found that frontal-parietal-temporal regions in the proposed motor-to-sensory network collaboratively synchronize at the rate of mental operations

Summary

Introduction

“What is this paper about?” You are probably asking this question in your mind. We think in a verbal form all the time in our everyday lives. This study aims to use a rhythmic entrainment paradigm to investigate the neural mechanisms that mediate mental operations such as inner speech and covert singing. This “entrainment” is in a broader sense, as suggested by Obleser and Kayser [35]. According to our hypothesis that the motor-to-sensory transformation neural network mediates inner speech and covert singing, we predicted that the different degrees of neural tracking to the rate of mental operations would be observed in specific areas in the frontal, parietal, and temporal regions (Fig 1F), where the core computations for motor simulations and perceptual estimations in motor-to-sensory transformation have been indicated [3, 22, 25]

Results

Discussion

Participants

Procedure