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

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, intraparietal 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.

Dual-stream cortical feedbacks mediate sensory prediction

“…Significant activity was observed in the left PMC in the motor-based prediction task of IS and its representational specificity was supported by MVPA (Figure 1,2). These results are consistent with previous studies that stress PMC’s role in speech planning (Castellucci et al, 2022) as well as studies on speech imagery (Li et al .,2020; Proix et al, 2022; Tian et al ., 2016). In terms of lateralization, left PMC was more engaged in speech prediction.…”

“…Common activation in both motor-based and memory-based imagery in the auditory cortex agrees with previous work on musical imagery (Halpern and Zatorre, 1999; Li et al ., 2020), speech imagery (Proix et al ., 2022; Tian et al ., 2016), and imagery of complex sounds (Bunzeck et al ., 2005). Imagery induced similar activations in the auditory cortices as hearing controls, supporting the nature of sensory-like representation as the ending result of prediction.…”

“…Moreover, our novel dual-imagery paradigm maximized the differences between motor-based and memory-based prediction as participants were asked to imagining speech or natural sounds that human articulators cannot produce (Figure 1b). The DSPM model and preliminary empirical findings (Li et al, 2020; Ma and Tian, 2019; Tian and Poeppel, 2010; Tian et al ., 2016) derive three major experimental predictions. First, both motor-based and memory-based predictions in different types of imagery would reactivate the auditory cortex without external acoustic stimulation.…”

Imagined speech can be decoded from low- and cross-frequency features in perceptual space

“…This finding aligns well with the notion that the beta band plays an important role in endogenous processes, notably in relation with top-down control, in particular in the context of language (Arnal and Giraud, 2012;Bowers et al, 2019;Fontolan et al, 2014;Pefkou et al, 2017). Although repeating a heard or written word engages automatic, almost reflex, neural routines, imagined speech is a more voluntary action requiring enhanced endogenous control from action planning frontal regions (Buschman et al, 2012;Li et al, 2020;Morillon et al, 2019). These results must however be taken with caution as spurious CFC can result from non-linearity, non-stationarity, and power changes across conditions in the signal (Aru et al, 2015;Hyafil, 2015).…”

Imagined speech can be decoded from low- and cross-frequency intracranial EEG features

“…This finding aligns well with the notion that the beta band plays an important role in endogenous processes, notably in relation with top-down control in the language domain 16,17,40,43,48,49 . Although repeating a heard or written word engages automatic, almost reflex, neural routines, imagined speech is a more voluntary action requiring enhanced endogenous control from action planning frontal regions [50][51][52] . Since spurious CFC can sometimes result from non-linearity, nonstationarity, and power changes across conditions in the signal 53,54 , we carefully selected spectral peaks for the modulating signal to ensure a well-defined phase and specific bandwidths for the modulated signal.…”