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Altered reward processing underpins emotional apathy in dementia

INTRODUCTION: While apathy is broadly defined as a loss of motivation, it is increasingly recognised as a multidimensional syndrome spanning executive, emotional, and initiation domains. Emotional apathy is purportedly driven by deficits in using socioemotional rewards to guide behaviour, yet the li...

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Autores principales: Wong, Stephanie, Wei, Grace, Husain, Masud, Hodges, John R., Piguet, Olivier, Irish, Muireann, Kumfor, Fiona
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10049956/
https://www.ncbi.nlm.nih.gov/pubmed/36417157
http://dx.doi.org/10.3758/s13415-022-01048-2
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author Wong, Stephanie
Wei, Grace
Husain, Masud
Hodges, John R.
Piguet, Olivier
Irish, Muireann
Kumfor, Fiona
author_facet Wong, Stephanie
Wei, Grace
Husain, Masud
Hodges, John R.
Piguet, Olivier
Irish, Muireann
Kumfor, Fiona
author_sort Wong, Stephanie
collection PubMed
description INTRODUCTION: While apathy is broadly defined as a loss of motivation, it is increasingly recognised as a multidimensional syndrome spanning executive, emotional, and initiation domains. Emotional apathy is purportedly driven by deficits in using socioemotional rewards to guide behaviour, yet the link between these symptoms and reward processing, and their common neural correlates, has not been directly examined. METHODS: Sixty-four patients (33 behavioural-variant frontotemporal dementia, 14 Alzheimer’s disease, 8 semantic dementia, 6 progressive nonfluent aphasia, 3 logopenic progressive aphasia) were classified into high (HEA; n = 36) and low (LEA; n = 28) emotional apathy groups based on emotional apathy subscale scores on the Dimensional Apathy Scale. Patients and age-matched healthy controls (n = 27) performed an instrumental reward learning task where they learned to associate cues with either social or monetary outcomes. RESULTS: HEA patients showed impaired learning on both the social and monetary reward conditions, relative to LEA patients (p = 0.016) and controls (p = 0.005). Conversely, the LEA group did not differ from controls (p = 0.925). Importantly, multiple regression analyses indicated that social reward learning significantly predicted emotional apathy. Voxel-based morphometry analyses revealed that emotional apathy and social reward learning were both associated with orbitofrontal cortex, ventral striatum, and insula atrophy. DISCUSSION: Our results demonstrate a unique link between impaired social reward learning and emotional apathy in dementia and reveal a shared neurobiological basis. Greater understanding of these neurocognitive mechanisms of reward processing will help improve the identification of emotional apathy in dementia and inform the development of novel interventions to address these symptoms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-022-01048-2.
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spelling pubmed-100499562023-03-30 Altered reward processing underpins emotional apathy in dementia Wong, Stephanie Wei, Grace Husain, Masud Hodges, John R. Piguet, Olivier Irish, Muireann Kumfor, Fiona Cogn Affect Behav Neurosci Research Article INTRODUCTION: While apathy is broadly defined as a loss of motivation, it is increasingly recognised as a multidimensional syndrome spanning executive, emotional, and initiation domains. Emotional apathy is purportedly driven by deficits in using socioemotional rewards to guide behaviour, yet the link between these symptoms and reward processing, and their common neural correlates, has not been directly examined. METHODS: Sixty-four patients (33 behavioural-variant frontotemporal dementia, 14 Alzheimer’s disease, 8 semantic dementia, 6 progressive nonfluent aphasia, 3 logopenic progressive aphasia) were classified into high (HEA; n = 36) and low (LEA; n = 28) emotional apathy groups based on emotional apathy subscale scores on the Dimensional Apathy Scale. Patients and age-matched healthy controls (n = 27) performed an instrumental reward learning task where they learned to associate cues with either social or monetary outcomes. RESULTS: HEA patients showed impaired learning on both the social and monetary reward conditions, relative to LEA patients (p = 0.016) and controls (p = 0.005). Conversely, the LEA group did not differ from controls (p = 0.925). Importantly, multiple regression analyses indicated that social reward learning significantly predicted emotional apathy. Voxel-based morphometry analyses revealed that emotional apathy and social reward learning were both associated with orbitofrontal cortex, ventral striatum, and insula atrophy. DISCUSSION: Our results demonstrate a unique link between impaired social reward learning and emotional apathy in dementia and reveal a shared neurobiological basis. Greater understanding of these neurocognitive mechanisms of reward processing will help improve the identification of emotional apathy in dementia and inform the development of novel interventions to address these symptoms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-022-01048-2. Springer US 2022-11-23 2023 /pmc/articles/PMC10049956/ /pubmed/36417157 http://dx.doi.org/10.3758/s13415-022-01048-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wong, Stephanie
Wei, Grace
Husain, Masud
Hodges, John R.
Piguet, Olivier
Irish, Muireann
Kumfor, Fiona
Altered reward processing underpins emotional apathy in dementia
title Altered reward processing underpins emotional apathy in dementia
title_full Altered reward processing underpins emotional apathy in dementia
title_fullStr Altered reward processing underpins emotional apathy in dementia
title_full_unstemmed Altered reward processing underpins emotional apathy in dementia
title_short Altered reward processing underpins emotional apathy in dementia
title_sort altered reward processing underpins emotional apathy in dementia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10049956/
https://www.ncbi.nlm.nih.gov/pubmed/36417157
http://dx.doi.org/10.3758/s13415-022-01048-2
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