eprintid: 10135841
rev_number: 12
eprint_status: archive
userid: 608
dir: disk0/10/13/58/41
datestamp: 2021-10-07 11:05:43
lastmod: 2021-10-07 11:05:43
status_changed: 2021-10-07 11:05:43
type: article
metadata_visibility: show
creators_name: Benhamou, E
creators_name: Zhao, S
creators_name: Sivasathiaseelan, H
creators_name: Johnson, JCS
creators_name: Requena-Komuro, M-C
creators_name: Bond, RL
creators_name: van Leeuwen, JEP
creators_name: Russell, LL
creators_name: Greaves, CV
creators_name: Nelson, A
creators_name: Nicholas, JM
creators_name: Hardy, CJD
creators_name: Rohrer, JD
creators_name: Warren, JD
title: Decoding expectation and surprise in dementia: the paradigm of music
ispublished: pub
divisions: UCL
divisions: B02
divisions: C07
divisions: D07
divisions: F86
keywords: frontotemporal dementia, music, pupillometry, surprise, voxel-based morphometry
note: © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
abstract: Making predictions about the world and responding appropriately to unexpected events are essential functions of the healthy brain. In neurodegenerative disorders, such as frontotemporal dementia and Alzheimer's disease, impaired processing of 'surprise' may underpin a diverse array of symptoms, particularly abnormalities of social and emotional behaviour, but is challenging to characterize. Here, we addressed this issue using a novel paradigm: music. We studied 62 patients (24 female; aged 53-88) representing major syndromes of frontotemporal dementia (behavioural variant, semantic variant primary progressive aphasia, non-fluent-agrammatic variant primary progressive aphasia) and typical amnestic Alzheimer's disease, in relation to 33 healthy controls (18 female; aged 54-78). Participants heard famous melodies containing no deviants or one of three types of deviant note-acoustic (white-noise burst), syntactic (key-violating pitch change) or semantic (key-preserving pitch change). Using a regression model that took elementary perceptual, executive and musical competence into account, we assessed accuracy detecting melodic deviants and simultaneously recorded pupillary responses and related these to deviant surprise value (information-content) and carrier melody predictability (entropy), calculated using an unsupervised machine learning model of music. Neuroanatomical associations of deviant detection accuracy and coupling of detection to deviant surprise value were assessed using voxel-based morphometry of patients' brain MRI. Whereas Alzheimer's disease was associated with normal deviant detection accuracy, behavioural and semantic variant frontotemporal dementia syndromes were associated with strikingly similar profiles of impaired syntactic and semantic deviant detection accuracy and impaired behavioural and autonomic sensitivity to deviant information-content (all P < 0.05). On the other hand, non-fluent-agrammatic primary progressive aphasia was associated with generalized impairment of deviant discriminability (P < 0.05) due to excessive false-alarms, despite retained behavioural and autonomic sensitivity to deviant information-content and melody predictability. Across the patient cohort, grey matter correlates of acoustic deviant detection accuracy were identified in precuneus, mid and mesial temporal regions; correlates of syntactic deviant detection accuracy and information-content processing, in inferior frontal and anterior temporal cortices, putamen and nucleus accumbens; and a common correlate of musical salience coding in supplementary motor area (all P < 0.05, corrected for multiple comparisons in pre-specified regions of interest). Our findings suggest that major dementias have distinct profiles of sensory 'surprise' processing, as instantiated in music. Music may be a useful and informative paradigm for probing the predictive decoding of complex sensory environments in neurodegenerative proteinopathies, with implications for understanding and measuring the core pathophysiology of these diseases.
date: 2021-08-10
date_type: published
official_url: https://doi.org/10.1093/braincomms/fcab173
oa_status: green
full_text_type: pub
pmcid: PMC8376684
language: eng
primo: open
primo_central: open_green
verified: verified_manual
elements_id: 1884006
doi: 10.1093/braincomms/fcab173
pii: fcab173
lyricists_name: Johnson, Jeremy
lyricists_name: Rohrer, Jonathan
lyricists_name: Warren, Jason
lyricists_id: JCSJO54
lyricists_id: JDROH34
lyricists_id: JDWAR75
actors_name: Kalinowski, Damian
actors_id: DKALI47
actors_role: owner
full_text_status: public
publication: Brain Communications
volume: 3
number: 3
article_number: fcab173
event_location: England
citation:        Benhamou, E;    Zhao, S;    Sivasathiaseelan, H;    Johnson, JCS;    Requena-Komuro, M-C;    Bond, RL;    van Leeuwen, JEP;                             ... Warren, JD; + view all <#>        Benhamou, E;  Zhao, S;  Sivasathiaseelan, H;  Johnson, JCS;  Requena-Komuro, M-C;  Bond, RL;  van Leeuwen, JEP;  Russell, LL;  Greaves, CV;  Nelson, A;  Nicholas, JM;  Hardy, CJD;  Rohrer, JD;  Warren, JD;   - view fewer <#>    (2021)    Decoding expectation and surprise in dementia: the paradigm of music.                   Brain Communications , 3  (3)    , Article fcab173.  10.1093/braincomms/fcab173 <https://doi.org/10.1093/braincomms%2Ffcab173>.       Green open access   
 
document_url: https://discovery.ucl.ac.uk/id/eprint/10135841/1/Johnson_Decoding%20expectation%20and%20surprise%20in%20dementia-%20the%20paradigm%20of%20music_AOP.pdf