Impaired pitch perception and memory in congenital amusia: The deficit starts in the auditory cortex

INSERM U1028 - CNRS UMR5292, Centre de Recherche en Neurosciences de Lyon, Equipe Dynamique Cérébrale et Cognition, Centre Hospitalier le Vinatier, Batiment 452, 95 Bd Pinel, Bron, F-69500, France. .
Brain (Impact Factor: 9.2). 05/2013; 136(Pt 5):1639-61. DOI: 10.1093/brain/awt082
Source: PubMed


Congenital amusia is a lifelong disorder of music perception and production. The present study investigated the cerebral bases of impaired pitch perception and memory in congenital amusia using behavioural measures, magnetoencephalography and voxel-based morphometry. Congenital amusics and matched control subjects performed two melodic tasks (a melodic contour task and an easier transposition task); they had to indicate whether sequences of six tones (presented in pairs) were the same or different. Behavioural data indicated that in comparison with control participants, amusics' short-term memory was impaired for the melodic contour task, but not for the transposition task. The major finding was that pitch processing and short-term memory deficits can be traced down to amusics' early brain responses during encoding of the melodic information. Temporal and frontal generators of the N100m evoked by each note of the melody were abnormally recruited in the amusic brain. Dynamic causal modelling of the N100m further revealed decreased intrinsic connectivity in both auditory cortices, increased lateral connectivity between auditory cortices as well as a decreased right fronto-temporal backward connectivity in amusics relative to control subjects. Abnormal functioning of this fronto-temporal network was also shown during the retention interval and the retrieval of melodic information. In particular, induced gamma oscillations in right frontal areas were decreased in amusics during the retention interval. Using voxel-based morphometry, we confirmed morphological brain anomalies in terms of white and grey matter concentration in the right inferior frontal gyrus and the right superior temporal gyrus in the amusic brain. The convergence between functional and structural brain differences strengthens the hypothesis of abnormalities in the fronto-temporal pathway of the amusic brain. Our data provide first evidence of altered functioning of the auditory cortices during pitch perception and memory in congenital amusia. They further support the hypothesis that in neurodevelopmental disorders impacting high-level functions (here musical abilities), abnormalities in cerebral processing can be observed in early brain responses.

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    • "Another, not mutually exclusive explanation is that our findings are the result of impaired top-down attentional monitoring (originating from the attentional hubs located in the frontal lobes). There is substantial evidence that backward propagation from the inferior frontal gyrus to the auditory cortex is dysfunctional in amusics (Hyde et al., 2011; Albouy et al., 2013). This poor frontotemporal connectivity may compromise normal shaping of auditory responses in both the auditory cortex and the brainstem. "
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    ABSTRACT: Congenital amusia is a neurogenetic condition, characterized by a deficit in music perception and production, not explained by hearing loss, brain damage or lack of exposure to music. Despite inferior musical performance, amusics exhibit normal auditory cortical responses, with abnormal neural correlates suggested to lie beyond auditory cortices. Here we show, using auditory brainstem responses to complex sounds in humans, that fine-grained automatic processing of sounds is impoverished in amusia. Compared to matched non-musician controls, spectral amplitude was decreased in amusics for higher harmonic components of the auditory brainstem response. We also found a delayed response to the early transient aspects of the auditory stimulus in amusics. Neural measures of spectral amplitude and response timing correlated with participants' behavioral assessments of music processing. We demonstrate, for the first time, that amusia affects how complex acoustic signals are processed in the auditory brainstem. This neural signature of amusia mirrors what is observed in musicians, such that the aspects of the auditory brainstem responses that are enhanced in musicians are degraded in amusics. By showing that gradients of music abilities are reflected in the auditory brainstem, our findings have implications not only for current models of amusia but also for auditory functioning in general. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    European Journal of Neuroscience 04/2015; 42(1). DOI:10.1111/ejn.12931 · 3.18 Impact Factor
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    • "To investigate whether the GMV of the amygdala is associated with music processing, we measured participants' ability to extract pitch interval size (i.e., interval perception), a core ability of music processing [18], [42]. After validating that interval perception was correlated with daily emotional experiences, we examined correlations between participants' amygdala GMV and interval perception. "
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    ABSTRACT: Music is not simply a series of organized pitches, rhythms, and timbres, it is capable of evoking emotions. In the present study, voxel-based morphometry (VBM) was employed to explore the neural basis that may link music to emotion. To do this, we identified the neuroanatomical correlates of the ability to extract pitch interval size in a music segment (i.e., interval perception) in a large population of healthy young adults (N = 264). Behaviorally, we found that interval perception was correlated with daily emotional experiences, indicating the intrinsic link between music and emotion. Neurally, and as expected, we found that interval perception was positively correlated with the gray matter volume (GMV) of the bilateral temporal cortex. More important, a larger GMV of the bilateral amygdala was associated with better interval perception, suggesting that the amygdala, which is the neural substrate of emotional processing, is also involved in music processing. In sum, our study provides one of first neuroanatomical evidence on the association between the amygdala and music, which contributes to our understanding of exactly how music evokes emotional responses.
    PLoS ONE 06/2014; 9(6):e99889. DOI:10.1371/journal.pone.0099889 · 3.23 Impact Factor
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    • "The present study did not only consider performance accuracy, but also reaction times since amusics have been shown to react more slowly than controls [8] [21] [22]. "
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    ABSTRACT: Congenital Amusia is a developmental disorder that has a negative influence on pitch perception. While it used to be described as a disorder of musical pitch perception, recent studies indicate that congenital amusics also show deficits in linguistic pitch perception. This study investigates the perception of linguistic and non-linguistic pitch by ten German amusics and their matched controls. To test the influence of amusia on linguistic pitch perception, the present study parametrically varied pitch differences in steps of one semitone in resynthesized statement-question pairs. In addition, we looked at the influence of stimulus duration, continuity of pitch and direction of pitch change (statement or question). Performance accuracy and reaction times were recorded. Behavioral results show that amusics performed worse than controls over all conditions. The reaction time analysis supports these findings, as amusics were significantly slower across all conditions. Both groups were faster in discriminating statements than questions. Performance accuracy supports these findings, as questions were also harder to discriminate. The present results warrant further investigation of the linguistic factors influencing amusics' perception of intonation.
    Social and Linguistic Speech Prosody: Speech Prosody 7; 05/2014
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