Altered reward processing underpins emotional apathy in dementia

Wong, Stephanie; Wei, Grace; Hodges, John R.; Piguet, Olivier; Irish, Muireann; Kumfor, Fiona

doi:10.3758/s13415-022-01048-2

Cited by 12 publications

(10 citation statements)

References 82 publications

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“…Apathy showed the highest reported frequency in FTD including bvFTD in ten studies [ 12 , 21 , 23 , 76 – 82 ], while only two studies addressed PPA [ 76 , 78 ]. In studies comparing FTD with AD, FTD patients had a higher prevalence of apathy [ 12 , 21 ] and higher apathy scores [ 83 , 84 ] than AD patients. Only one study highlighted a higher prevalence of apathy in patients with bvFTD in its early stage [ 82 ].…”

Section: Resultsmentioning

confidence: 99%

“…Eight studies used NPI [ 21 , 76 , 78 , 80 , 82 , 84 – 86 ], and five studies used AES [ 14 , 23 , 78 , 81 ]. One study used LARS [ 12 ], three used CBI-R [ 21 , 76 , 77 ], two used the Motivation and Energy Inventory (MEI) [ 76 , 78 ], three used the Snaith-Hamilton Pleasure Scale (SHAPS) [ 76 , 78 , 79 ], one used DAD [ 21 ], two used the Social and Emotional Assessment (Mini-SEA) [ 82 , 87 ], one used AS [ 87 ], DAS was used in four studies [ 23 , 79 , 83 , 88 ], one used the goal-directed behaviors (GDB) [ 81 ], and one used FBI [ 89 ]. Interestingly, one of the studies investigating bvFTD phenotypes related to WM changes found discordant scores on several apathy administration tests [ 78 ].…”

Section: Resultsmentioning

confidence: 99%

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Prevalence, treatment, and neural correlates of apathy in different forms of dementia: a narrative review

Parrotta,

Cacciatore,

D’Andrea

et al. 2023

Neurol Sci

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Objectives The aim of this review is to provide an overview on prevalence and clinical tools for the diagnosis of apathy, as well as on neurophysiological and neuroimaging findings obtained from studies in patients with apathy in different forms of dementia, including Alzheimer’s disease (AD), vascular (VaD) and mixed dementia, frontotemporal dementia (FTD), and Parkinson’s disease dementia (PDD). Methods Randomized controlled trials, non-randomized controlled trials, controlled before–after studies, and interrupted time series from four databases (WebOfScience, Scopus, Pubmed, and PsycINFO) addressing apathy in adults or older people aged over 65 years of age affected by dementia were included. Results The prevalence of apathy was 26–82% for AD, 28.6–91.7 for VaD, 29–97.5% in PDD, and 54.8–88.0 in FTD. The assessment of apathy was not consistent in the reviewed studies. Methylphenidate was the most successful pharmacological treatment for apathy. Neurobiological studies highlighted the relationship between both structural and functional brain areas and the presence or severity of apathy. Conclusion Apathy is a very common disorder in all types of dementia, although it is often underdiagnosed and undertreated. Further studies are needed to investigate its diagnosis and management. A consensus on the different evaluation scales should be achieved.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Prevalence, treatment, and neural correlates of apathy in different forms of dementia: a narrative review

Parrotta,

Cacciatore,

D’Andrea

et al. 2023

Neurol Sci

View full text Add to dashboard Cite

show abstract

“…This lateralization pattern has previously been reported in HD with the left striatum being predominately affected. 16,44 Further, upon examining signal alterations at an ROI level, we assessed activity disparities among distinct HDGEC subgroups (Controls vs Apathetic vs Nonapathetic). Results revealed that those categorized as apathetic exhibited especially reduced activity levels compared to both the nonapathetic and control groups.…”

Section: Discussionmentioning

confidence: 99%

“…13,14 Apathy may emerge from the impairment of any of these processes or from the inability to integrate these complex functions. [15][16][17] In the context of HD, apathy has conventionally been attributed to executive dysfunction, specifically linked with the well-documented neurodegeneration within the dorsolateral prefrontal cortex (dlPFC)-dorsal striatum loop. 11,18 However, there is a limited understanding of the involvement of limbic regions within the basal ganglia and their impact on reward processing deficits, which ultimately culminate in apathetic behavior.…”

Section: Introductionmentioning

confidence: 99%

Investigating altered limbic reward system in Huntington's Disease: Implications for apathy

Bikou,

de Vicente,

De Paepe

et al. 2024

Preprint

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Huntington's disease (HD) is an inherited neurodegenerative condition characterized by motor, cognitive, and behavioral impairments. Apathy, marked by reduced motivation and goal-directed behavior, is the most prevalent psychiatric symptom in HD, impacting both patients and caregivers. Traditionally linked to executive dysfunction within the dorsolateral prefrontal cortex (dlPFC)-dorsal striatum loop in HD, the role of limbic regions in the basal ganglia and their impact on reward processing deficits remains poorly understood. This study sought to dissociate the functional correlates that are altered in reward valuation and may underlie apathy in HD. We aimed to tease apart whether apathy is associated with insensitivity to processing rewards, hypersensitivity to losses, or both, leading to the observed lack of motivation in apathetic individuals. Thirty-nine HD gene-expansion carriers (HDGEC) and 26 non-apathetic control participants underwent functional magnetic resonance imaging during a gambling task. The goal was to identify disrupted reward-related regions in HDGEC and their association with apathetic symptoms. Whole-brain analysis of gains and losses separately showed a significant reduction in activity, when HD group was compered to controls, within the left ventral striatum (VS), including the nucleus accumbens. The effect observed in the VS remained when clinically apathetic HDGEC were compared with controls. Conversely, non-apathetic HDGEC did not show any significant differences from controls. Interestingly, these group differences appeared exclusively during the processing of the reward. Additionally, higher levels of apathy were associated with especially decreased activity related with the processing of gains in this region. Our findings highlight the vulnerability of the left VS in HD and its association with the altered processing of gains, particularly in apathetic individuals, while preserving the valuation of losses. This suggests that reward insensitivity associated with VS dysfunction may be an important component of apathy in HD. Understanding the underlying mechanisms of reward processing and apathy in HD may help elucidate the implications of limbic regions as opposed to frontal executive dysfunction in apathy.

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“…A study of reward-based decision-making using the Iowa gambling task demonstrated disadvantageous decision-making profiles in those experiencing apathy (that may not be AD specific) [ 142 ]. In a study published in 2023, individuals with dementia experiencing apathy showed impaired learning in social and monetary reward conditions, indicating a relationship between social reward and emotional apathy [ 143 ] and suggesting deficits in reward-based decision-making in apathy syndrome.…”

Section: Neuropsychology Of Apathy In Admentioning

confidence: 99%

An Update on Apathy in Alzheimer’s Disease

et al. 2023

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Apathy is a complex multi-dimensional syndrome that affects up to 70% of individuals with Alzheimer’s disease (AD). Whilst many frameworks to define apathy in AD exist, most include loss of motivation or goal-directed behaviour as the central feature. Apathy is associated with significant impact on persons living with AD and their caregivers and is also associated with accelerated cognitive decline across the AD spectrum. Neuroimaging studies have highlighted a key role of fronto-striatial circuitry including the anterior cingulate cortex (ACC), orbito-frontal cortex (OFC) and associated subcortical structures. Importantly, the presence and severity of apathy strongly correlates with AD stage and neuropathological biomarkers of amyloid and tau pathology. Following from neurochemistry studies demonstrating a central role of biogenic amine neurotransmission in apathy syndrome in AD, recent clinical trial data suggest that apathy symptoms may improve following treatment with agents such as methylphenidate—which may have an important role alongside emerging non-pharmacological treatment strategies. Here, we review the diagnostic criteria, rating scales, prevalence, and risk factors for apathy in AD. The underlying neurobiology, neuropsychology and associated neuroimaging findings are reviewed in detail. Finally, we discuss current treatment approaches and strategies aimed at targeting apathy syndrome in AD, highlighting areas for future research and clinical trials in patient cohorts.

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Altered reward processing underpins emotional apathy in dementia

Cited by 12 publications

References 82 publications

Prevalence, treatment, and neural correlates of apathy in different forms of dementia: a narrative review

Prevalence, treatment, and neural correlates of apathy in different forms of dementia: a narrative review

Investigating altered limbic reward system in Huntington's Disease: Implications for apathy

An Update on Apathy in Alzheimer’s Disease

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