Decoding expectation and surprise in dementia: the paradigm of music

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 characterise. 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, nonfluent-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 MR images. 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, nonfluent-agrammatic primary progressive aphasia was associated with generalised 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.

Implicit auditory memory in older listeners: from encoding to 6-month retention

“…One important open question is why such long-term auditory implicit memory is overall resilient to time decay even later in life. The remarkable examples of preserved auditory memory for music in severe cases of dementia (Baird and Samson, 2009; Benhamou et al, 2021; Jacobsen et al, 2015) suggest that implicit auditory memory has a privileged status in the brain. In young listeners, implicit auditory memory based on repeated exposure has been demonstrated for many sound types, ranging from white noise (Agus et al, 2010; Dauer et al, 2022; Ringer et al, 2022), click trains (Kang et al, 2017), discrete sequences of tones (Bianco et al, 2020a; Bonetti et al, 2022; Herrmann et al, 2021; Leek and Watson, 1988), tone clouds (Agus and Pressnitzer, 2021), and naturalistic textures (Ringer et al, 2022; Woods and Mcdermott, 2018).…”

“…One important open question is why such long-term auditory implicit memory is overall resilient to time decay even later in life? The remarkable examples of preserved auditory memory for music severe cases of dementia [101][102][103] suggest that implicit auditory memory has a privileged status in the brain. In young listeners, implicit auditory memory based on repeated exposure has been demonstrated for many sound types, ranging from white noise [104][105][106] , click trains 107 , discrete sequences of tones 61,84,108,109 , tone clouds 110 , and naturalistic textures 106,111 .…”

Does Amount of Information Support Aesthetic Values?

“…Interestingly, some neurodegenerative disorders impair the ability of the brain to process musical surprise. A recent study explored Alzheimer’s disease and some forms of dementia in regard to this impairment ( Benhamou et al, 2021 ). Alzheimer’s disease associated with normal deviant detection accuracy.…”

More Than Meets the Eye: Art Engages the Social Brain

“…This profile of network disruption causes people to struggle with recalling the details of autobiographical experiences, as well as with perceptual decoding of complex visual scenes and assuming others' viewpoints, whereas emotional awareness and prosocial concepts and impulses often remain relatively intact well into the disease process (Bosch-Domènech et al, 2010;Dodich et al, 2016). Moreover, people with Alzheimer's disease (in contrast to frontotemporal dementia) have retained capacity to process and react appropriately to novel or incongruous features in complex stimuli such as music (Benhamou et al, 2021); this cognitive operation is also likely to be highly relevant to engaging with artworks. In the context of the artistic brain connectome, this dementia profile could be characterized by difficulty with decoding perceptual relationships and/or symbolic meanings from art and/or in finding the right words to describe one's thoughts and perceptions, despite retained appreciation of the emotional resonance of artworks.…”