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A physiological signature of sound meaning in dementia.

Fletcher, PD; Nicholas, JM; Downey, LE; Golden, HL; Clark, CN; Pires, C; Agustus, JL; Mummery, CJ; Schott, JM; Rohrer, JD; et al. Fletcher, PD; Nicholas, JM; Downey, LE; Golden, HL; Clark, CN; Pires, C; Agustus, JL; Mummery, CJ; Schott, JM; Rohrer, JD; Crutch, SJ; Warren, JD (2016) A physiological signature of sound meaning in dementia. Cortex, 77. pp. 13-23. ISSN 1973-8102 https://doi.org/10.1016/j.cortex.2016.01.007
SGUL Authors: Clark, Camilla Neegaard

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Abstract

The meaning of sensory objects is often behaviourally and biologically salient and decoding of semantic salience is potentially vulnerable in dementia. However, it remains unclear how sensory semantic processing is linked to physiological mechanisms for coding object salience and how that linkage is affected by neurodegenerative diseases. Here we addressed this issue using the paradigm of complex sounds. We used pupillometry to compare physiological responses to real versus synthetic nonverbal sounds in patients with canonical dementia syndromes (behavioural variant frontotemporal dementia - bvFTD, semantic dementia - SD; progressive nonfluent aphasia - PNFA; typical Alzheimer's disease - AD) relative to healthy older individuals. Nonverbal auditory semantic competence was assessed using a novel within-modality sound classification task and neuroanatomical associations of pupillary responses were assessed using voxel-based morphometry (VBM) of patients' brain MR images. After taking affective stimulus factors into account, patients with SD and AD showed significantly increased pupil responses to real versus synthetic sounds relative to healthy controls. The bvFTD, SD and AD groups had a nonverbal auditory semantic deficit relative to healthy controls and nonverbal auditory semantic performance was inversely correlated with the magnitude of the enhanced pupil response to real versus synthetic sounds across the patient cohort. A region of interest analysis demonstrated neuroanatomical associations of overall pupil reactivity and differential pupil reactivity to sound semantic content in superior colliculus and left anterior temporal cortex respectively. Our findings suggest that autonomic coding of auditory semantic ambiguity in the setting of a damaged semantic system may constitute a novel physiological signature of neurodegenerative diseases.

Item Type: Article
Additional Information: ©2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Alzheimer's disease, Dementia, Frontotemporal, Nonverbal sound, Physiology, Progressive aphasia, Pupillometry, Semantic, Adult, Cognition, Female, Frontotemporal Dementia, Frontotemporal Lobar Degeneration, Humans, Male, Neuropsychological Tests, Primary Progressive Nonfluent Aphasia, Recognition (Psychology), Temporal Lobe, Young Adult, Temporal Lobe, Humans, Cognition, Recognition (Psychology), Neuropsychological Tests, Adult, Female, Male, Young Adult, Frontotemporal Lobar Degeneration, Primary Progressive Nonfluent Aphasia, Frontotemporal Dementia, Experimental Psychology, 1109 Neurosciences, 1702 Cognitive Sciences
SGUL Research Institute / Research Centre: Academic Structure > Molecular and Clinical Sciences Research Institute (MCS)
Journal or Publication Title: Cortex
ISSN: 1973-8102
Language: eng
Dates:
DateEvent
April 2016Published
23 January 2016Published Online
9 January 2016Accepted
Publisher License: Creative Commons: Attribution 4.0
Projects:
Project IDFunderFunder ID
MR/M008525/1Medical Research Councilhttp://dx.doi.org/10.13039/501100000265
091673/Z/10/ZWellcome Trusthttp://dx.doi.org/10.13039/100004440
MR/J011274/1Medical Research Councilhttp://dx.doi.org/10.13039/501100000265
ART-PhD2011-10Alzheimer's Research UKUNSPECIFIED
CBRC 161National Institute for Health Researchhttp://dx.doi.org/10.13039/501100000272
PubMed ID: 26889604
Go to PubMed abstract
URI: https://openaccess.sgul.ac.uk/id/eprint/111499
Publisher's version: https://doi.org/10.1016/j.cortex.2016.01.007

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