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: 10.23). 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.

  • [Show abstract] [Hide abstract]
    ABSTRACT: The combination of information across senses can enhance perception, as revealed for example by decreased reaction times or improved stimulus detection. Interestingly, these facilitatory effects have been shown to be maximal when responses to unisensory modalities are weak. The present study investigated whether audiovisual facilitation can be observed in congenital amusia, a music-specific disorder primarily ascribed to impairments of pitch processing. Amusic individuals and their matched controls performed two tasks. In Task 1, they were required to detect auditory, visual, or audiovisual stimuli as rapidly as possible. In Task 2, they were required to detect as accurately and as rapidly as possible a pitch change within an otherwise monotonic 5-tone sequence that was presented either only auditorily (A condition), or simultaneously with a temporally congruent, but otherwise uninformative visual stimulus (AV condition). Results of Task 1 showed that amusics exhibit typical auditory and visual detection, and typical audiovisual integration capacities: both amusics and controls exhibited shorter response times for audiovisual stimuli than for either auditory stimuli or visual stimuli. Results of Task 2 revealed that both groups benefited from simultaneous uninformative visual stimuli to detect pitch changes: accuracy was higher and response times shorter in the AV condition than in the A condition. The audiovisual improvements of response times were observed for different pitch interval sizes depending on the group. These results suggest that both typical listeners and amusic individuals can benefit from multisensory integration to improve their pitch processing abilities and that this benefit varies as a function of task difficulty. These findings constitute the first step towards the perspective to exploit multisensory paradigms to reduce pitch-related deficits in congenital amusia, notably by suggesting that audiovisual paradigms are effective in an appropriate range of unimodal performance. Copyright © 2014. Published by Elsevier Ltd.
    Neuropsychologia 12/2014; 67. · 3.45 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Congenital amusia is defined by marked deficits in pitch perception and production. Though historically examined only in otherwise typically developing (TD) populations, amusia has recently been documented in Williams syndrome (WS), a genetic, neurodevelopmental disorder with a unique auditory phenotype including auditory sensitivities and increased emotional responsiveness to music but variable musical skill. The current study used structural T1-weighted magnetic resonance imaging and diffusion tensor imaging to examine neural correlates of amusia in 17 individuals with WS (4 of whom met criteria for amusia). Consistent with findings from TD amusics, amusia in WS was associated with decreased fractional anisotropy (FA) in the right superior longitudinal fasciculus (SLF). The relationship between amusia and FA in the inferior component of the SLF was particularly robust, withstanding corrections for cognitive functioning, auditory sensitivities, or musical training. Though the number of individuals with amusia in the study is small, results add to evidence for the role of fronto-temporal disconnectivity in congenital amusia and suggest that novel populations with developmental differences can provide a window into understanding gene-brain-behavior relationships that underlie musical behaviors.
    Brain sciences. 12/2014; 4(4):594-612.
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The issue of whether human perception of speech and song recruit integrated or dissociated neural systems is contentious. This issue is difficult to address directly since these stimulus classes differ in their physical attributes. We therefore used a compelling illusion (Deutsch et al. 2011) in which acoustically identical auditory stimuli are perceived as either speech or song. Deutsch's illusion was used in a functional MRI experiment to provide a direct, within-subject investigation of the brain regions involved in the perceptual transformation from speech into song, independent of the physical characteristics of the presented stimuli. An overall differential effect resulting from the perception of song compared with that of speech was revealed in right midposterior superior temporal sulcus / right middle temporal gyrus. A left frontotemporal network, previously implicated in higher-level cognitive analyses of music and speech, was found to co-vary with a behavioural measure of the subjective vividness of the illusion, and this effect was driven by the illusory transformation. These findings provide evidence that illusory song perception is instantiated by a network of brain regions that are predominantly shared with the speech perception network. Copyright © 2014. Published by Elsevier Inc.
    NeuroImage 12/2014; 108. · 6.13 Impact Factor