Auditory hedonic phenotypes in dementia: A behavioural and neuroanatomical analysis.
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.
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Phillip D
PD
Fletcher
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Laura E
LE
Downey
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Hannah L
HL
Golden
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Camilla N
CN
Clark
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Catherine F
CF
Slattery
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Ross W
RW
Paterson
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Jonathan M
JM
Schott
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Jonathan D
JD
Rohrer
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom.
Martin N
MN
Rossor
Dementia Research Centre, UCL Institute of Neurology, University College London, United Kingdom. Electronic address: jason.warren@ucl.ac.uk.
Jason D
JD
Warren
D000339:Affect; D000368:Aged; D000369:Aged, 80 and over; D000544:Alzheimer Disease / Q000473:pathology / Q000503:physiopathology* / Q000523:psychology; D001307:Auditory Perception; D001921:Brain / Q000473:pathology*; D004644:Emotions; D005260:Female; D057180:Frontotemporal Dementia / Q000473:pathology / Q000503:physiopathology* / Q000523:psychology; D006179:Gyrus Cinguli / Q000473:pathology; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009146:Music / Q000523:psychology*; D009714:Nucleus Accumbens / Q000473:pathology; D010641:Phenotype; D057178:Primary Progressive Nonfluent Aphasia / Q000473:pathology / Q000503:physiopathology* / Q000523:psychology; D013702:Temporal Lobe / Q000473:pathology
Affect; Alzheimer's disease; Environmental sounds; Frontotemporal dementia; Music; Musicophilia; Progressive aphasia; Reward; Semantic dementia; VBM