Neural architectures of music – Insights from acquired amusia Sihvonen, Aleksi J.; Särkämö, Teppo; Rodríguez-Fornells, Antoni ...
Neuroscience & biobehavioral reviews/Neuroscience and biobehavioral reviews,
December 2019, 2019-12-00, 20191201, Letnik:
107
Journal Article
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•Acquired amusia is common after a stroke to the middle cerebral artery region.•Right frontotemporal and insular lesions give rise to acquired amusia.•Less severe and recoverable amusia is associated ...with lesions in the left hemisphere.•Right dual-stream system, especially the ventral stream, are affected in amusia.•Vocal music processing in amusia seems to be spared.
The ability to perceive and produce music is a quintessential element of human life, present in all known cultures. Modern functional neuroimaging has revealed that music listening activates a large-scale bilateral network of cortical and subcortical regions in the healthy brain. Even the most accurate structural studies do not reveal which brain areas are critical and causally linked to music processing. Such questions may be answered by analysing the effects of focal brain lesions in patients´ ability to perceive music. In this sense, acquired amusia after stroke provides a unique opportunity to investigate the neural architectures crucial for normal music processing. Based on the first large-scale longitudinal studies on stroke-induced amusia using modern multi-modal magnetic resonance imaging (MRI) techniques, such as advanced lesion-symptom mapping, grey and white matter morphometry, tractography and functional connectivity, we discuss neural structures critical for music processing, consider music processing in light of the dual-stream model in the right hemisphere, and propose a neural model for acquired amusia.
We report a patient with vocal amusia who was not a musician. The patient was an 81-year-old right-handed woman whose singing ability decreased after infarctions in the right hemisphere. This change ...was not accompanied by dysarthria or dysprosody. On head MRI, cerebral infarctions were detected mainly in the cortex and subcortical region of the right precentral gyrus, and extended to the central region of the insula, cortex of the posterior end of the middle frontal gyrus, and a part of the medial cortex of the superior temporal gyrus. To define the characteristics of the disorder in this case and investigate the association with the developmental mechanism and lesions, receptiveness and expressiveness of music were compared between the patient and 8 control subjects. Music receptiveness had not declined in the patient, but abnormal pitch expression in music expressiveness and flattening to a lower pitch than the target sound were noted, in contrast to the control group. These changes suggest that disorder of pitch expression during singing was not caused by motor or music-receptive disorder, and that the main lesions in the motor-related area of the right frontal lobe and central area of the right insula were involved in pitch phonation control.
Anti-N-methyl-d-aspartate receptor (NMDAR) encephalitis has a high relapse rate at approximately 10–20%. Most relapses occur within 2 years from onset, and 5 years after onset is rare. We report a ...case of anti-NMDAR encephalitis relapse with amusia 10 years after the initial encephalitis and discuss the usefulness of 123I-iomazenil single-photon emission computerized tomography (IMZ-SPECT) for its diagnosis.
A 13-year-old left-handed girl presented with a depressed level of consciousness and focal to bilateral tonic-clonic seizures. Cerebrospinal fluid (CSF) analysis showed a mildly increased white blood cell count, elevated neopterin levels, and positive oligoclonal bands. Brain MRI was normal. IMZ-SPECT revealed reduced uptake in the right frontoparietal region. She received intravenous pulse methylprednisolone (IVMP) and high-dose intravenous immunoglobulin for autoimmune encephalitis; her symptoms resolved without neurological deficits. At 23 years old, she had mild right-sided numbness, dysarthria, amusia, and tonic-clonic seizures. Although the CSF analysis and brain MRI were normal, IMZ-SPECT revealed reduced uptake, indicating a relapse of encephalitis. IVMP administration resolved the symptoms. After discharge, the initial and relapse CSF analysis revealed anti-NMDAR antibodies.
An anti-NMDAR encephalitis relapse 10 years after onset has never been reported. IMZ-SPECT may help in the diagnosis of anti-NMDAR encephalitis.
The past decade of research has provided compelling evidence that musical engagement is a fundamental human trait, and its biological basis is increasingly scrutinized. In this endeavor, the detailed ...study of individuals who have musical deficiencies is instructive because of likely neurogenetic underpinnings. Such individuals have ‘congenital amusia’, an umbrella term for lifelong musical disabilities that cannot be attributed to intellectual disability, lack of exposure, or brain damage after birth. Key points are reviewed here that have emerged during recent years regarding the neurobiology of the disorder, focusing on the importance of recurrent processing between the right inferior frontal cortex and the auditory cortex for conscious monitoring of musical pitch, and how this relates to developmental cognitive disorders in general.
Music is a universal human attribute. The study of amusia, a neurologic music processing deficit, has increasingly elaborated our view on the neural organization of the musical brain. However, ...lesions causing amusia occur in multiple brain locations and often also cause aphasia, leaving the distinct neural networks for amusia unclear. Here, we utilized lesion network mapping to identify these networks. A systematic literature search was carried out to identify all published case reports of lesion-induced amusia. The reproducibility and specificity of the identified amusia network were then tested in an independent prospective cohort of 97 stroke patients (46 female and 51 male) with repeated structural brain imaging, specifically assessed for both music perception and language abilities. Lesion locations in the case reports were heterogeneous but connected to common brain regions, including bilateral temporoparietal and insular cortices, precentral gyrus, and cingulum. In the prospective cohort, lesions causing amusia mapped to a common brain network, centering on the right superior temporal cortex and clearly distinct from the network causally associated with aphasia. Lesion-induced longitudinal structural effects in the amusia circuit were confirmed as reduction of both gray and white matter volume, which correlated with the severity of amusia. We demonstrate that despite the heterogeneity of lesion locations disrupting music processing, there is a common brain network that is distinct from the language network. These results provide evidence for the distinct neural substrate of music processing, differentiating music-related functions from language, providing a testable target for noninvasive brain stimulation to treat amusia.
•We studied whether perceptual adaptation is affected by perceptual acuity, i.e., amusia.•Amusics showed reduced categorical perception of lexical tones.•Amusics failed to recalibrate their tonal ...categories based on different contexts.•Perceptual adaptation is a higher-order cognitive process that depends on perceptual acuity.
Perceptual adaptation is an active cognitive process where listeners re-analyse speech categories based on new contexts/situations/talkers. It involves top-down influences from higher cortical levels on lower-level auditory processes. Individuals with congenital amusia have impaired pitch processing with reduced connectivity between frontal and temporal regions. This study examined whether deficits in amusia would lead to impaired perceptual adaptation in lexical tone perception. Thirteen Mandarin-speaking amusics and 13 controls identified the category of target tones on an 8-step continuum ranging from rising to high-level, either in isolation or in a high-/low-pitched context. For tones with no context, amusics exhibited reduced categorical perception than controls. While controls’ lexical tone categorization demonstrated a significant context effect due to perceptual adaptation, amusics showed similar categorization patterns across both contexts. These findings suggest that congenital amusia impacts the extraction of context-dependent tonal categories in speech perception, indicating that perceptual adaptation may depend on listeners’ perceptual acuity.
This study investigated whether there is a co-occurrence between developmental dyslexia and congenital amusia in adults. First, a database of online musical tests on 18,000 participants was analysed. ...Self-reported dyslexic participants performed significantly lower on melodic skills than matched controls, suggesting a possible link between reading and musical disorders. In order to test this relationship more directly, we evaluated 20 participants diagnosed with dyslexia, 16 participants diagnosed with amusia, and their matched controls, with a whole battery of literacy (reading, fluency, spelling), phonological (verbal working memory, phonological awareness) and musical tests (melody, rhythm and metre perception, incidental memory). Amusia was diagnosed in six (30%) dyslexic participants and reading difficulties were found in four (25%) amusic participants. Thus, the results point to a moderate comorbidity between amusia and dyslexia. Further research will be needed to determine what factors at the neural and/or cognitive levels are responsible for this co-occurrence.
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.
Previous studies have shown that for congenital amusics, long-term tone language experience cannot compensate for lexical tone processing difficulties. However, it is still unknown whether such ...difficulties are merely caused by domain-transferred insensitivity in lower-level acoustic processing and/or by higher-level phonological processing of linguistic pitch as well. The current P300 study links and extends previous studies by uncovering the neurophysiological mechanisms underpinning lexical tone perception difficulties in Mandarin-speaking amusics. Both the behavioral index (
) and P300 amplitude showed reduced within-category as well as between-category sensitivity among the Mandarin-speaking amusics regardless of the linguistic status of the signal. The results suggest that acoustic pitch processing difficulties in amusics are manifested profoundly and further persist into the higher-level phonological processing that involves the neural processing of different lexical tone categories. Our findings indicate that long-term tone language experience may not compensate for the reduced acoustic pitch processing in tone language speakers with amusia but rather may extend to the neural processing of the phonological information of lexical tones during the attentive stage. However, from both the behavioral and neural evidence, the peakedness scores of the
and P300 amplitude were comparable between amusics and controls. It seems that the basic categorical perception (CP) pattern of native lexical tones is preserved in Mandarin-speaking amusics, indicating that they may have normal or near normal long-term categorical memory.
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