Brainstem encoding of speech and musical stimuli in congenital amusia: evidence from Cantonese speakers

Abstract

Congenital amusia is a neurodevelopmental disorder of musical processing that also impacts subtle aspects of speech processing. It remains debated at what stage(s) of auditory processing deficits in amusia arise. In this study, we investigated whether amusia originates from impaired subcortical encoding of speech (in quiet and noise) and musical sounds in the brainstem. Fourteen Cantonese-speaking amusics and 14 matched controls passively listened to six Cantonese lexical tones in quiet, two Cantonese tones in noise (signal-to-noise ratios at 0 and 20 dB), and two cello tones in quiet while their frequency-following responses (FFRs) to these tones were recorded. All participants also completed a behavioral lexical tone identification task. The results indicated normal brainstem encoding of pitch in speech (in quiet and noise) and musical stimuli in amusics relative to controls, as measured by FFR pitch strength, pitch error, and stimulus-to-response correlation. There was also no group difference in neural conduction time or FFR amplitudes. Both groups demonstrated better FFRs to speech (in quiet and noise) than to musical stimuli. However, a significant group difference was observed for tone identification, with amusics showing significantly lower accuracy than controls. Analysis of the tone confusion matrices suggested that amusics were more likely than controls to confuse between tones that shared similar acoustic features. Interestingly, this deficit in lexical tone identification was not coupled with brainstem abnormality for either speech or musical stimuli. Together, our results suggest that the amusic brainstem is not functioning abnormally, although higher-order linguistic pitch processing is impaired in amusia. This finding has significant implications for theories of central auditory processing, requiring further investigations into how different stages of auditory processing interact in the human brain.

Hidden Markov modeling of frequency-following responses to Mandarin lexical tones

“…In particular, the decoding of T4 was considerably less accurate than any of the other three tones. This result is in line with previous findings showing a suboptimal subcortical encoding of falling tonal patterns (Krishnan et al, 2010; Krishnan et al, 2009; Krishnan et al, 2004; Liu, Maggu, Lau, & Wong, 2015). For example, Krishnan et al (2010) used normalized autocorrelation to estimate the strength of periodicity in the FFR (peak autocorrelation metric).…”

Congenital amusics use a secondary pitch mechanism to identify lexical tones

“…This is consistent with a pitch mechanism reliant upon TFS remaining the primary mechanism in amusics, and with amusics performing better at pitch discrimination when TFS cues are available than when not, despite performing poorly compared to controls (Cousineau et al, 2015). Consistent with Cousineau et al (2015), and with Liu et al (2014) who found no evidence for the representation of pitch information being degraded at the level of the auditory brainstem in amusics, no evidence was found in the present study for a deficit in the peripheral representation of TFS in amusics (Fig. 2A).…”

“…Any mechanism for pitch-extraction is likely to reside beyond the superior olive, at or after the lateral lemniscus or the inferior colliculus (Gockel et al, 2011), suggesting that any TFS processing deficit associated with impaired pitch perception in amusia must reside at or central of this stage of the auditory brainstem. Consistent with this, a recent study has failed to find evidence of impaired pitch encoding in the rostral auditory brainstem as indicated by the frequency-following response (Liu et al, 2014, although see also Lehmann et al, 2015).…”

Meta-analytic evidence for the non-modularity of pitch processing in congenital amusia

“…Various studies have converged in identifying the right inferior frontal cortex (BA47), right auditory cortex (BA22), and the arcuate fasciculus as potential sources of these abnormal electrical responses (Hyde, Zatorre, Griffiths, Lerch, & Peretz, 2006;Hyde, Zatorre, & Peretz, 2011;Loui, Alsop, & Schlaug, 2009), and recent evidence suggests that BA47 is responsible for amusics' abnormal P300 (Albouy, Schulze, et al, 2013). The centrality of these cortical mechanisms to amusia is supported by recent c o r t e x 6 9 ( 2 0 1 5 ) 1 8 6 e2 0 0 evidence that amusics show intact brainstem encoding of speech and music, as measured by the frequency following response (Liu, Maggu, Lau, & Wong, 2015). Therefore, TMS could be used to mimic amusic brain function in non-amusic participants by creating a transient lesion in BA47.…”