Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden

Chow, Tiffany E.; Veziris, Christina R.; Joie, Renaud La; Lee, Alex J.; Brown, Jesse A.; Yokoyama, Jennifer S.; Rankin, Katherine P.; Kramer, Joel H.; Miller, Bruce L.; Rabinovici, Gil D.; Seeley, William W.; Sturm, Virginia E.

doi:10.1016/j.nicl.2022.103282

Cited by 10 publications

(11 citation statements)

References 134 publications

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“…Often a prominent site of early tau pathology in DAT and MCI [ 3, 22, 23 ], the MTL is also affected in lvPPA and PCA, albeit to a lesser extent [ 10, 105, 106 ]. Taken together with our prior study that found empathic concern gains in cognitively healthy Aβ+ older adults [ 50 ], our research suggests that Aβ and tau may both contribute to emotional empathy increases in people on an AD trajectory. Previous research has suggested that Aβ and tau interact through both local and remote connections and that Aβ deposition facilitates the spread of tau beyond the MTL [ 107 ].…”

Section: Discussionsupporting

confidence: 83%

“…Unlike emotional contagion, which can elicit self-oriented feelings of distress or being overwhelmed during negative emotional situations [ 48 ], empathic concern focuses attention outward onto the needs of others and promotes prosocial actions such as helping and consolation [ 43, 47 ]. In a prior study, we found greater gains in empathic concern over time in Aβ+ than Aβ- cognitively healthy older adults [ 50 ], which suggested there are enhancements in this form of emotional empathy in the preclinical stages of AD. In the present study, we expand on this work by showing that empathic concern is also higher in the clinical phase of AD.…”

Section: Discussionmentioning

confidence: 87%

“…In our prior research, we have found elevations in two forms of emotional empathy—emotional contagion (a self-oriented form of emotional empathy that can be accompanied by feelings of distress) and empathic concern (an other-oriented form of emotional empathy that promotes prosocial actions) [ 47, 48 ]—in people on an AD trajectory. While emotional contagion is higher in MCI and AD than in healthy older adults [ 49 ], empathic concern increases more over time in cognitively healthy older adults with higher cortical Aβ than in those with lower levels [ 50 ].…”

Section: Introductionmentioning

confidence: 99%

“…Unlike cognitive empathy, which does not necessarily elicit changes in subjective experience [ 51 ], emotional empathy evokes shared feeling states between people by activating the MTL (primarily the amygdala) and other structures in the salience network [ 51, 60 ], a system that supports emotion generation and interoception [ 61–64 ]. In early AD, default mode network dysfunction is accompanied by heightened salience network connectivity, a functional gain that relates to neuropsychiatric symptoms in the clinical phase [ 65, 66 ] and increasing empathic concern in the preclinical period [ 50 ]. While there is some evidence that early tau deposition in the MTL relates to heightened stress, anxiety, and depression [ 41, 42 ], whether MTL tau aggregation also relates to higher emotional empathy in AD is unknown.…”

Section: Introductionmentioning

confidence: 99%

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Medial Temporal Lobe Tau Aggregation Relates to Divergent Cognitive and Emotional Empathy Abilities in Alzheimer’s Disease

Chow,

Veziris,

Mundada

et al. 2023

JAD

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Background: In Alzheimer’s disease (AD), the gradual accumulation of amyloid-β (Aβ) and tau proteins may underlie alterations in empathy. Objective: To assess whether tau aggregation in the medial temporal lobes relates to differences in cognitive empathy (the ability to take others’ perspectives) and emotional empathy (the ability to experience others’ feelings) in AD. Methods: Older adults (n = 105) completed molecular Aβ positron emission tomography (PET) scans. Sixty-eight of the participants (35 women) were Aβ positive and symptomatic with diagnoses of mild cognitive impairment, dementia of the Alzheimer’s type, logopenic variant primary progressive aphasia, or posterior cortical atrophy. The remaining 37 (22 women) were asymptomatic Aβ negative healthy older controls. Using the Interpersonal Reactivity Index, we compared current levels of informant-rated cognitive empathy (perspective-taking subscale) and emotional empathy (empathic concern subscale) in the Aβ positive and negative participants. The Aβ positive participants also underwent molecular tau-PET scans, which were used to investigate whether regional tau burden in the bilateral medial temporal lobes related to empathy. Results: Aβ positive participants had lower perspective-taking and higher empathic concern than Aβ negative healthy controls. Medial temporal tau aggregation in the Aβ positive participants had divergent associations with cognitive and emotional empathy. Whereas greater tau burden in the amygdala predicted lower perspective-taking, greater tau burden in the entorhinal cortex predicted greater empathic concern. Tau burden in the parahippocampal cortex did not predict either form of empathy. Conclusions: Across AD clinical syndromes, medial temporal lobe tau aggregation is associated with lower perspective-taking yet higher empathic concern.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Medial Temporal Lobe Tau Aggregation Relates to Divergent Cognitive and Emotional Empathy Abilities in Alzheimer’s Disease

Chow,

Veziris,

Mundada

et al. 2023

JAD

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“…In neurodegenerative diseases, atrophy in 1 brain region predicts atrophy in other functionally connected brain regions 2,5,18 . Prior studies have shown functional enhancement of the ACC and other salience network nodes that are anticorrelated to locations of atrophy in AD, with increased connectivity in the salience node correlating with neuropsychiatric symptoms 29–35 . To our knowledge, prior studies have not investigated whether there is a similar reciprocal relationship between networks showing brain atrophy and increased cortical thickness in AD.…”

mentioning

confidence: 99%

Increased Cortical Thickness in Alzheimer's Disease

Phan,

Baratono,

Drew

et al. 2024

Annals of Neurology

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ObjectivePatients with Alzheimer's disease (AD) have diffuse brain atrophy, but some regions, such as the anterior cingulate cortex (ACC), are spared and may even show increase in size compared to controls. The extent, clinical significance, and mechanisms associated with increased cortical thickness in AD remain unknown. Recent work suggested neural facilitation of regions anticorrelated to atrophied regions in frontotemporal dementia. Here, we aim to determine whether increased thickness occurs in sporadic AD, whether it relates to clinical symptoms, and whether it occur in brain regions functionally connected to—but anticorrelated with—locations of atrophy.MethodsCross‐sectional clinical, neuropsychological, and neuroimaging data from the Alzheimer's Disease Neuroimaging Initiative were analyzed to investigate cortical thickness in AD subjects versus controls. Atrophy network mapping was used to identify brain regions functionally connected to locations of increased thickness and atrophy.ResultsAD patients showed increased thickness in the ACC in a region‐of‐interest analysis and the visual cortex in an exploratory analysis. Increased thickness in the left ACC was associated with preserved cognitive function, while increased thickness in the left visual cortex was associated with hallucinations. Finally, we found that locations of increased thickness were functionally connected to, but anticorrelated with, locations of brain atrophy (r = −0.81, p < 0.05).InterpretationOur results suggest that increased cortical thickness in Alzheimer's disease is relevant to AD symptoms and preferentially occur in brain regions functionally connected to, but anticorrelated with, areas of brain atrophy. Implications for models of compensatory neuroplasticity in response to neurodegeneration are discussed. ANN NEUROL 2024

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Social cognition and behavioral changes in patients with posterior cortical atrophy

St-Georges,

Wang,

Chapleau

et al. 2023

J Neurol

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Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden

Cited by 10 publications

References 134 publications

Medial Temporal Lobe Tau Aggregation Relates to Divergent Cognitive and Emotional Empathy Abilities in Alzheimer’s Disease

Medial Temporal Lobe Tau Aggregation Relates to Divergent Cognitive and Emotional Empathy Abilities in Alzheimer’s Disease

Increased Cortical Thickness in Alzheimer's Disease

Social cognition and behavioral changes in patients with posterior cortical atrophy

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