Neuroimaging Meta-Analyses Reveal Convergence of Interoception, Emotion, and Social Cognition Across Neurodegenerative Diseases.

BACKGROUND

Simultaneous interoceptive, emotional, and social cognition deficits are observed across neurodegenerative diseases. Indirect evidence suggests shared neurobiological bases underlying these impairments, termed the allostatic-interoceptive network (AIN). However, no study has yet explored the convergence of these deficits in neurodegenerative diseases or examined how structural and functional changes contribute to cross-domain impairments.

METHODS

A Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) activated likelihood estimate meta-analysis encompassed studies that met the following inclusion criteria: interoception, emotion, or social cognition tasks; neurodegenerative diseases (behavioral variant frontotemporal dementia, primary progressive aphasias, Alzheimer's disease, Parkinson's disease, multiple sclerosis); and neuroimaging (structural: magnetic resonance imaging voxel-based morphometry; functional: magnetic resonance imaging and fluorodeoxyglucose-positron emission tomography).

RESULTS

Of 20,593 studies, 170 met inclusion criteria (58 interoception, 65 emotion, and 47 social cognition) involving 7032 participants (4963 patients and 2069 healthy control participants). In all participants combined, conjunction analyses revealed AIN involvement of the insula, amygdala, orbitofrontal cortex, anterior cingulate, striatum, thalamus, and hippocampus across domains. In behavioral variant frontotemporal dementia, this conjunction was replicated across domains, with further involvement of the temporal pole, temporal fusiform cortex, and angular gyrus. A convergence of interoception and emotion in the striatum, thalamus, and hippocampus in Parkinson's disease and the posterior insula in primary progressive aphasias was also observed. In Alzheimer's disease and multiple sclerosis, disruptions in the AIN were observed during interoception, but no convergence with emotion was identified.

CONCLUSIONS

Neurodegeneration induces dysfunctional AIN across atrophy, connectivity, and metabolism, more accentuated in behavioral variant frontotemporal dementia. Findings bolster the predictive coding theories of large-scale AIN, calling for more synergistic approaches to understanding interoception, emotion, and social cognition impairments in neurodegeneration.