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

Fang Liu,Akshay R Maggu,Patrick C M Wong,Joseph C Y Lau

doi:10.3389/fnhum.2014.01029

Fang Liu, Akshay R Maggu + Show 2 more

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https://doi.org/10.3389/fnhum.2014.01029

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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.

Highlights

Congenital amusia is a neuro-genetic disorder of musical processing (Drayna et al, 2001; Peretz et al, 2007), affecting around 4% of the general population for both tone and non-tonal language speakers (Kalmus and Fry, 1980; Nan et al, 2010; Wong et al, 2012; see Henry and McAuley, 2010, 2013, for criticisms)
BRAINSTEM ENCODING OF SPEECH (IN QUIET AND NOISE) AND MUSICAL STIMULI (IN QUIET) Figure 2 shows the waveforms of the six Cantonese lexical tones, and grand average waveforms of the frequency-following responses (FFRs) to the six tones of the amusic and control groups
Linear mixed-effects models were first fit on all FFR measures for each experimental condition, with group, tone (Tones 1–6 in the speech-in-quiet condition, Tone 1 versus Tone 6 in the speech-in-noise condition, and high versus low cello tone in the music condition), and noise (SNR = 0 and 20 dB in the speech-in-noise condition) as fixed effects, education as a covariate, and participants as random effects

Summary

Introduction

Congenital amusia is a neuro-genetic disorder of musical processing (Drayna et al, 2001; Peretz et al, 2007), affecting around 4% of the general population for both tone and non-tonal language speakers (Kalmus and Fry, 1980; Nan et al, 2010; Wong et al, 2012; see Henry and McAuley, 2010, 2013, for criticisms). Some early studies reported ceiling performance of amusics on speech intonation processing, presumably due to the coarse intonational contrasts used (Ayotte et al, 2002; Peretz et al, 2002; Patel et al, 2005), more recent research has suggested that amusia is a domain-general pitch processing deficit that compromises subtle aspects of pitch processing in speech, including lexical tone perception, linguistic and emotional prosody processing, and speech intonation imitation (Patel et al, 2008; Hutchins et al, 2010; Jiang et al, 2010, 2012a,b; Liu et al, 2010, 2012a, 2013; Nan et al, 2010; Tillmann et al, 2011a,b; Thompson et al, 2012). The amusic brain has reduced white matter and increased gray matter in the right inferior frontal gyrus (Hyde et al, 2006; Albouy et al, 2013a), reduced gray matter in the right superior temporal gyrus (Albouy et al, 2013a), and thicker cortex in the right

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