Effects of absolute pitch on brain activation and functional connectivity during hearing-in-noise perception

Speech comprehension in noisy environments relies on hearing-in-noise (HIN) ability. For the elderly and hearing-impaired, HIN perception is notably challenging and may lead to emotional stress (Henry & Heinz, 2012; Zendel & Alain, 2012). Studies show that both bottom-up stimulus attributes and top-down cognitive factors affect HIN performance (Coffey et al., 2017; Hennessy et al., 2022). In particular, one form of human experience—musicianship—has been associated with HIN benefits though some controversies remain. The notion that sensory and/or cognitive processing fine-tuned by music training may transfer to enhance processing in non-musical domains (e.g., language) is important in terms of both establishing grounds of applying music training to mitigate HIN declines and providing insights into neural plasticity (Coffey et al., 2017; Parbery-Clark et al., 2009).

The putative musician HIN advantage is hypothesized on the grounds that processing music and language draws on shared neural resources. Specifically, the OPERA hypothesis proposes that the higher engagement on five aspects (overlap, precision, emotion, repetition, attention) of music training can enhance neural functioning in speech processing (Patel, 2011, 2014). Functional magnetic resonance imaging (fMRI) studies have reported greater recruitment of the bilateral auditory cortices, right superior temporal gyrus (STG), and left inferior frontal gyrus (IFG) in musicians than in non-musicians for identifying syllables in noise (Du & Zatorre, 2017). Additionally, relative to non-musicians, musicians showed enhanced interhemispheric functional connectivity between auditory regions (e.g., STG, planum temporale [PT]) and speech motor regions (e.g., ventromedial premotor cortex [vPMC]), which paralleled higher accuracy of phoneme identification in noise (Bidelman et al., 2014; Du et al., 2014; Du & Zatorre, 2017). Moreover, musical expertise mitigates age-related HIN declines by increasing neural alignment with younger brains in bilateral sensorimotor regions (Zhang et al., 2022) and enhancing cortical responses to speech in the middle frontal and supramarginal gyri (Fleming et al., 2019). Collectively, these findings suggest that musical experience is associated with greater activation of, and enhanced functional connectivity between auditory and speech-motor regions.

Although accumulating evidence suggests a putative musician HIN advantage, discrepant findings remain, possibly due to the heterogeneity (in auditory/perceptual abilities) of musicians. Importantly, recent studies indicate that absolute pitch (AP) proficiency may be one critical factor that modulates musician HIN advantage. AP, the relatively rare ability to identify isolated musical notes (Deutsch, 2013), is one of the most fascinating abilities related to musicianship requiring both a genetic origin and a critical period for development (Athos et al., 2007; Baharloo et al., 1998; Gregersen et al., 2001). Behaviorally, two recent studies reported that AP musicians outperformed non-AP musicians at identifying melodic targets against a background of interleaved melodies (Wenhart, Hwang, et al., 2019) or multi-music noise (Hsieh et al., 2022). At the cortical level, limited evidence exists on the relationship between AP ability and HIN perception. Previous studies on AP ability and brain networks have primarily focused on activation or functional connectivity during perception in silence. AP-dependent activation has been largely reported in auditory regions (e.g., Leipold et al., 2019; Schulze et al., 2009; Wengenroth et al., 2014) during passive listening to tones, with most recent findings, using combined fMRI and magnetoencephalography (MEG) methods, revealing distinct temporal hierarchical patterns of auditory responses in AP possessors (Benner et al., 2023). Additionally, AP ability is associated with activations in speech relevant regions, including Broca's motor speech area, planum temporale, and temporo-parietal junction (TPJ) during tone perception in silence (Wengenroth et al., 2014). Apart from neural activation, results from studies examining AP-specific effects on neural connectivity have been relatively inconsistent. While some have reported increased functional connectivity during music listening in silence (Jäncke et al., 2012; Loui et al., 2012; Kim & Knösche, 2017), others have found diminished whole brain network connectivity during naturalistic listening to audiobooks and music (Brauchli et al., 2020) and resting-state electroencephalography (EEG) (Wenhart, Bethlehem, et al., 2019). Specifically, Wenhart et al. reported that AP musicians exhibited neural network indices indicating reduced functional integration and enhanced segregation during resting state. While these findings indicate a potential role of AP ability in segregation, they are based on AP perception in the absence of background noise. As such, the underlying neural mechanism that supports AP's benefits for perception, particularly in noisy environments, i.e., HIN perception, remains unclear.

This study aims to investigate AP effects on neural activation and functional connectivity underlying HIN perception across both linguistic and musical domains. To our knowledge, no study thus far has examined how AP ability affects perception in the presence of background noise. Moreover, given the hypothesized neural overlap between speech and music, a comparison between HIN perception for speech and music streams, and its modulation by AP ability, can provide further insights into the musician HIN advantage. Functional MRI is used here to contrast activation differences among AP musicians, non-AP musicians, and non-musicians during the Mandarin Speech-in-Noise Task (Wong et al., 2008) and Music-in-Noise Task (Coffey et al., 2019) at various signal-to-noise ratios (SNRs). We include the non-musician group without music training to assess musician effects under comparable AP ability. Given the potential link of AP with HIN, we hypothesize that AP musicians would show greater activation and functional connectivity in auditory and speech-motor regions compared to non-AP musicians during HIN tasks, with functional connectivity potentially mediated by the HIN domain (music vs speech).

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