Musicality and social cognition in dementia: clinical and anatomical associations.

IF 4.1 Q1 CLINICAL NEUROLOGY Brain communications Pub Date : 2024-12-13 eCollection Date: 2024-01-01 DOI:10.1093/braincomms/fcae429
Jochum J van 't Hooft, Willem L Hartog, Michelle Braun, Dewi Boessen, Jay L P Fieldhouse, Marie-Paule E van Engelen, Ellen H Singleton, Artur C Jaschke, Rebecca S Schaefer, Vikram Venkatraghavan, Frederik Barkhof, Argonde C van Harten, Flora H Duits, Sigfried N T M Schouws, Mardien L Oudega, Jason D Warren, Betty M Tijms, Yolande A L Pijnenburg
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Abstract

Human musicality might have co-evolved with social cognition abilities, but common neuroanatomical substrates remain largely unclear. In behavioural variant frontotemporal dementia, social cognitive abilities are profoundly impaired, whereas these are typically spared in Alzheimer's disease. If musicality indeed shares a neuroanatomical basis with social cognition, it could be hypothesized that clinical and neuroanatomical associations of musicality and social cognition should differ between these causes of dementia. We recruited 73 participants from the Amsterdam Dementia Cohort (n = 30 female; aged 50-78), of whom 23 had behavioural variant frontotemporal dementia, 22 Alzheimer's disease and 28 were healthy controls. Musicality was assessed using a music-emotion recognition test, melody, tempo, accent and tuning subscores, a musicality summed score, the identification of auditory hedonic phenotypes and music emotion induction using skin conductance responses. Social cognition was assessed across multiple levels, including emotion recognition, theory of mind, socio-emotional sensitivity and understanding of social norms. We used ANCOVA to investigate subgroup differences in musicality and social cognition and linear regressions to investigate associations between musicality and social cognition. All analyses were adjusted for age, sex, musical training and mini mental state examination. Finally, we performed voxel-based morphometry analyses on T1-weighted MRI to study whether regions for musicality and social cognition overlapped anatomically. We found that patients with behavioural variant frontotemporal dementia performed worse on music-emotion recognition (all P < 0.001) and tempo recognition (all P < 0.05) compared with Alzheimer's disease and on musicality summed score (all P = 0.02) compared to controls only. Furthermore, patients with behavioural variant frontotemporal dementia had lower mean skin conductance responses during emotion-inducing music, compared to Alzheimer's disease (all P < 0.045). Worse music emotion recognition scores were associated with worse facial emotion recognition (P < 0.0001), worse theory of mind (P = 0.0005) and worse understanding of social norms (P = 0.01). Melody and tempo recognition were associated with facial emotion recognition and theory of mind, and accent recognition was associated with the theory of mind. Music emotion recognition and tempo recognition were also associated with executive functions. Worse music emotion recognition, melody recognition, tempo recognition, facial emotion recognition and theory of mind scores were all related to atrophy in the anterior temporal regions and the fusiform gyri, which play a role in multisensory integration, and worse tempo recognition was associated with atrophy of the anterior cingulate cortex. These results support the idea that musicality and social cognition may share a neurobiological basis, which may be vulnerable in behavioural variant frontotemporal dementia.

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人类的音乐性可能是与社会认知能力共同进化而来的,但其共同的神经解剖基质在很大程度上仍不清楚。行为变异型额颞叶痴呆症患者的社会认知能力严重受损,而阿尔茨海默氏症患者的社会认知能力通常不受影响。如果音乐性确实与社会认知能力有着共同的神经解剖学基础,那么可以假设音乐性和社会认知能力的临床和神经解剖学关联在不同的痴呆症病因中应该有所不同。我们从阿姆斯特丹痴呆症队列中招募了 73 名参与者(女性 30 人;年龄 50-78 岁),其中 23 人患有行为变异性额颞叶痴呆症,22 人患有阿尔茨海默病,28 人为健康对照组。对音乐性的评估包括音乐情感识别测试、旋律、节奏、重音和调谐子分数、音乐性总分、听觉享乐表型的识别以及利用皮肤传导反应进行的音乐情感诱导。对社会认知进行了多层次评估,包括情绪识别、心智理论、社会情感敏感性和对社会规范的理解。我们使用方差分析来研究音乐性和社会认知的亚组差异,并使用线性回归来研究音乐性和社会认知之间的关联。所有分析都对年龄、性别、音乐训练和迷你精神状态检查进行了调整。最后,我们对 T1 加权核磁共振成像进行了体素形态计量分析,以研究音乐性和社会认知区域在解剖学上是否重叠。我们发现,与阿尔茨海默氏症患者相比,行为变异型额颞叶痴呆症患者在音乐情感识别(P均<0.001)和节奏识别(P均<0.05)方面表现较差;与对照组相比,音乐性总分(P均=0.02)方面表现较差。此外,与阿尔茨海默病相比,行为变异性额颞叶痴呆症患者在情绪诱导音乐中的平均皮肤传导反应较低(均为 P < 0.045)。较差的音乐情绪识别得分与较差的面部情绪识别(P < 0.0001)、心智理论(P = 0.0005)和对社会规范的理解(P = 0.01)有关。旋律和节奏识别与面部情绪识别和思维理论相关,而重音识别与思维理论相关。音乐情绪识别和节奏识别也与执行功能有关。较差的音乐情感识别、旋律识别、节奏识别、面部情感识别和心智理论得分都与颞叶前区和纺锤形回的萎缩有关,而颞叶前区和纺锤形回在多感官整合中发挥作用,较差的节奏识别与扣带回前皮层的萎缩有关。这些结果支持这样一种观点,即音乐性和社会认知可能具有共同的神经生物学基础,而这种基础在行为变异性额颞叶痴呆症中可能很脆弱。
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期刊最新文献
Brain age in genetic and idiopathic Parkinson's disease. Deep learning-based patient stratification for prognostic enrichment of clinical dementia trials. Could AI safeguard us from AI? Musicality and social cognition in dementia: clinical and anatomical associations. Correction to: Revisiting anti-Hu paraneoplastic autoimmunity: phenotypic characterization and cancer diagnosis.
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