Auditory hedonic phenotypes in dementia: A behavioural and neuroanatomical analysis

Abstract

Patients with dementia may exhibit abnormally altered liking for environmental sounds and music but such altered auditory hedonic responses have not been studied systematically. Here we addressed this issue in a cohort of 73 patients representing major canonical dementia syndromes (behavioural variant frontotemporal dementia (bvFTD), semantic dementia (SD), progressive nonfluent aphasia (PNFA) amnestic Alzheimer's disease (AD)) using a semi-structured caregiver behavioural questionnaire and voxel-based morphometry (VBM) of patients' brain MR images. Behavioural responses signalling abnormal aversion to environmental sounds, aversion to music or heightened pleasure in music (‘musicophilia’) occurred in around half of the cohort but showed clear syndromic and genetic segregation, occurring in most patients with bvFTD but infrequently in PNFA and more commonly in association with MAPT than C9orf72 mutations. Aversion to sounds was the exclusive auditory phenotype in AD whereas more complex phenotypes including musicophilia were common in bvFTD and SD. Auditory hedonic alterations correlated with grey matter loss in a common, distributed, right-lateralised network including antero-mesial temporal lobe, insula, anterior cingulate and nucleus accumbens. Our findings suggest that abnormalities of auditory hedonic processing are a significant issue in common dementias. Sounds may constitute a novel probe of brain mechanisms for emotional salience coding that are targeted by neurodegenerative disease.

Musical anhedonia and rewards of music listening: current advances and a proposed model

“…The authors suggest that, in this group of patients, musicophilia reflects a shift toward enjoyment of abstract activities due to impairments in social behaviors . A more recent study in patients with dementia indicated that musicophilia was associated with gray matter decreases in a network including both the striatum and AC . This seems consistent with the idea that changes in musical reward are associated with changes in the connectivity of the auditory and reward systems.…”

“…It is worth briefly noting here that individuals with brain damage can also exhibit extremely high hedonic responses to music, or an “abnormal craving for music,” which has been termed “musicophilia.” As with musical anhedonia, musicophilia has not been widely studied. However, prior work indicates that musicophilia is a somewhat common symptom of certain neurological disorders, which has shed light onto the neural substrates of this abnormal hedonic response to music . Individuals with frontotemporal dementia who experience musicophilia have increased gray matter volume in the left hemisphere hippocampus and decreased gray matter volume in the posterior parietal cortex, medial OFC, and frontal pole.…”

Strategic value‐directed learning and memory in Alzheimer's disease and behavioural‐variant frontotemporal dementia

“…While our correlational analyses indicated that reduced encoding selectivity was related to inhibitory dysfunction, an additional explanation may be that bvFTD patients were not sensitive to the motivational aspect of the reward values during the learning task. Indeed, reduced motivation is a diagnostic symptom of bvFTD (Rascovsky et al ., ), and evidence indicates that these patients show altered sensitivity to primary and secondary rewards (Fletcher et al ., ; Perry & Kramer, ; Perry, Sturm, Wood, Miller, & Kramer, ) and poor performance on value‐based decision‐making tasks (Kloeters et al ., ; Strenziok et al ., ). Conversely, symptoms of apathy are relatively less prevalent in AD compared with bvFTD (Chow et al ., ), and these patient groups show divergent profiles of reward sensitivity (Perry et al ., ).…”

Characterisation of “Positive” Behaviours in Primary Progressive Aphasias

“…Conversely, the emergence of visually based activities (puzzle, drawing, and photography) was seen in the nfvPPA group, but not in the lvPPA group. Changes in the degree of appreciation of environmental sounds or music have previously been compared among patients with different subtypes of frontotemporal dementia and Alzheimer disease [35], but not in lvPPA patients. The present findings provide additional support for an increase in music-related activities in a subset of svPPA patients, but also showed that this increase occurred in some lvPPA patients.…”