Article

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

ABSTRACT

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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Available from: Philippe Albouy, Jan 06, 2016
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    • "It indexes not only the behavioural discrimination accuracy but also the sensory memory traces of the preceding stimulation, forming the bases for change detection (Näätänen et al., 2007). More importantly, the MMN is localized in bilateral auditory and right frontal regions in the brain (Alain, Woods, & Knight, 1998), which converges with the affected auditory-fronal cortical network of pitch processing in amusics (Albouy et al., 2013; Hyde et al., 2011; Loui et al., 2009). Hence, the MMN seems well suited to examine the neurophysiological basis underlying amusics' lexical tone deficits. "
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    ABSTRACT: The association/dissociation of pitch processing between music and language is a long lasting debate. We examined this music-language relationship by investigating to what extent pitch deficits in these two domains were dissociable. We focused on a special neurodevelopmental pitch disorder-congenital amusia, which primarily affects musical pitch processing. Recent research has also revealed lexical tone deficits in speech among amusics. Approximately one-third of Mandarin amusics exhibits behavioural difficulties in lexical tone perception, which is known as tone agnosia. Using mismatch negativities (MMNs), our current work probed lexical tone encoding at the pre-attentive level among the Mandarin amusics with (tone agnosics) and without (pure amusics) behavioural lexical tone deficits compared with age- and IQ-matched controls. Relative to the controls and the pure amusics, the tone agnosics exhibited reduced MMNs specifically in response to lexical tone changes. Their tone-consonant MMNs were intact and similar to those of the other two groups. Moreover, the tone MMN reduction over the left hemisphere was tightly linked to behavioural insensitivity to lexical tone changes. The current study thus provides the first psychophysiological evidence of subgroup differences in lexical tone processing among Mandarin amusics and links amusics' behavioural tone deficits to impaired pre-attentive tone processing. Despite the overall music pitch deficits, the subgroup differences in lexical tone processing in Mandarin-speaking amusics suggest dissociation of pitch deficits between music and speech.
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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.
    Full-text · Article · Apr 2015 · European Journal of Neuroscience
    • "Individuals with amusia (amusics hereafter) have difficulty detecting out-of-tune notes in melodies and cannot sing in tune despite having normal hearing, intelligence, and regular exposure to music (Ayotte et al., 2002). Apart from musical problems, amusics also demonstrate elevated thresholds for pitch change detection and pitch direction discrimination (Foxton et al., 2004;Hyde and Peretz, 2004;Jiang et al., 2013;Liu et al., 2012b) and impaired memory for pitch (Albouy et al., 2013;Tillmann et al., 2009;Williamson and Stewart, 2010). Recent research suggests that amusia is not a music-specific disorder, as amusics exhibit impaired performance on lexical tone perception, linguistic and emotional prosody processing, phonological processing, and speech imitation in laboratory conditions (Jiang et al., 2012b;Jones et al., 2009a;Liu et al., 2013Liu et al., , 2010Liu and Jiang et al., 2012;Nan et al., 2010;Patel et al., 2008;Thompson et al., 2012). "
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    No preview · Article · Nov 2014 · Neuropsychologia
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