Neural Basis of Acquired Amusia and Its Recovery after Stroke

Although acquired amusia is a relatively common disorder after stroke, its precise neuroanatomical basis is still unknown. To evaluate which brain regions form the neural substrate for acquired amusia and its recovery, we performed a voxel-based lesion-symptom mapping (VLSM) and morphometry (VBM) st...

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Published in:The Journal of neuroscience 2016-08, Vol.36 (34), p.8872-8881
Main Authors: Sihvonen, Aleksi J, Ripollés, Pablo, Leo, Vera, Rodríguez-Fornells, Antoni, Soinila, Seppo, Särkämö, Teppo
Format: Article
Language:English
Subjects:
Afàsia
Aged
Aphasia
Auditory Perceptual Disorders - diagnostic imaging
Auditory Perceptual Disorders - etiology
Auditory Perceptual Disorders - rehabilitation
Brain damage
Brain Mapping
Female
Functional Laterality
Humans
Image Processing, Computer-Assisted
Language Disorders - diagnostic imaging
Language Disorders - etiology
Lesions cerebrals
Magnetic Resonance Imaging
Male
Mapatge del cervell
Middle Aged
Middle Cerebral Artery - diagnostic imaging
Recovery of Function - physiology
Retrospective Studies
Stroke - complications
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Summary:Although acquired amusia is a relatively common disorder after stroke, its precise neuroanatomical basis is still unknown. To evaluate which brain regions form the neural substrate for acquired amusia and its recovery, we performed a voxel-based lesion-symptom mapping (VLSM) and morphometry (VBM) study with 77 human stroke subjects. Structural MRIs were acquired at acute and 6 month poststroke stages. Amusia and aphasia were behaviorally assessed at acute and 3 month poststroke stages using the Scale and Rhythm subtests of the Montreal Battery of Evaluation of Amusia (MBEA) and language tests. VLSM analyses indicated that amusia was associated with a lesion area comprising the superior temporal gyrus, Heschl's gyrus, insula, and striatum in the right hemisphere, clearly different from the lesion pattern associated with aphasia. Parametric analyses of MBEA Pitch and Rhythm scores showed extensive lesion overlap in the right striatum, as well as in the right Heschl's gyrus and superior temporal gyrus. Lesions associated with Rhythm scores extended more superiorly and posterolaterally. VBM analysis of volume changes from the acute to the 6 month stage showed a clear decrease in gray matter volume in the right superior and middle temporal gyri in nonrecovered amusic patients compared with nonamusic patients. This increased atrophy was more evident in anterior temporal areas in rhythm amusia and in posterior temporal and temporoparietal areas in pitch amusia. Overall, the results implicate right temporal and subcortical regions as the crucial neural substrate for acquired amusia and highlight the importance of different temporal lobe regions for the recovery of amusia after stroke. Lesion studies are essential in uncovering the brain regions causally linked to a given behavior or skill. For music perception ability, previous lesion studies of amusia have been methodologically limited in both spatial accuracy and time domain as well as by small sample sizes, providing coarse and equivocal information about which brain areas underlie amusia. By using longitudinal MRI and behavioral data from a large sample of stroke patients coupled with modern voxel-based analyses methods, we were able provide the first systematic evidence for the causal role of right temporal and striatal areas in music perception. Clinically, these results have important implications for the diagnosis and prognosis of amusia after stroke and for rehabilitation planning.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.0709-16.2016