Abstract
Frontotemporal dementia is an important neurodegenerative disorder of younger life led by profound emotional and social dysfunction. Here we used fMRI to assess brain mechanisms of music emotion processing in a cohort of patients with frontotemporal dementia (n = 15) in relation to healthy age-matched individuals (n = 11). In a passive-listening paradigm, we manipulated levels of emotion processing in simple arpeggio chords (mode versus dissonance) and emotion modality (music versus human emotional vocalizations). A complex profile of disease-associated functional alterations was identified with separable signatures of musical mode, emotion level, and emotion modality within a common, distributed brain network, including posterior and anterior superior temporal and inferior frontal cortices and dorsal brainstem effector nuclei. Separable functional signatures were identified post-hoc in patients with and without abnormal craving for music (musicophilia): a model for specific abnormal emotional behaviors in frontotemporal dementia. Our findings indicate the potential of music to delineate neural mechanisms of altered emotion processing in dementias, with implications for future disease tracking and therapeutic strategies.
Highlights
Music is an exceptionally emotionally rich and engaging sensory stimulus
Musical mode variation produced greater activation in dorsal brainstem in the healthy control group than in the bvFTD group ((MCM > MFC) ×, P < 0.05 family-wise error (FWE) whole brain)); post-hoc analysis of  parameter estimates showed that this interaction was driven by a crossover interaction, whereby changing mode enhanced activity in controls (t10 = −3.31, P = 0.008) and reduced activity in patients (t10 = 6.68, P < 0.001) compared to fixed mode
There was a significant effect of music emotion level in the left planum temporale and right inferior frontal gyrus in the bvFTD group compared to the healthy control group ((MCD > MCM) ×, P < 0.05 FWE small volume)); post-hoc analysis of  parameter estimates revealed that this interaction was driven by patient group effects of greater responses to musical mode than dissonance variation in left planum temporale (t14 = −2.22, P = 0.04) with no effect in controls, and the reverse pattern in right inferior frontal gyrus (t14 = 4.24, P < 0.001) with the opposite effect in controls (t10 = −2.34, P = 0.035)
Summary
Music is an exceptionally emotionally rich and engaging sensory stimulus. Cognitive neuropsychology and functional neuroimaging studies in the healthy brain have shown that the neural mechanisms involved in analyzing music are intimately linked to the machinery of pleasure and reward.[1,2] Emotion in music is processed by a complex distributed brain network architecture, including salience and evaluation systems in the insula, amygdala, and orbitofrontal cortex projecting to mesolimbic and subcortical dopaminergic pathways.[1,2,3,4,5,6] More elemental affective attributes of dissonance and pleasantness, cognitive labeling of musical emotions, attribution of mental states to music, and appreciation of musical structure are likely to represent at least partially separable dimensions of music emotion coding.[2,3,4,5,7,8] Taken together, this evidence suggests that the essentially abstract phenomenon of music may have had a neurobiological role during human evolution, perhaps by engaging a neural puzzle-solving algorithm that facilitates decoding of emotional mental states.[9]. This formulation underlines the social function of music, a key theme in contemporary neuroscience accounts.[2,9]
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