Neuroimaging meta-analyses reveal convergence of interoception, emotion, and social cognition across neurodegenerative diseases

Jessica L Hazelton; Fábio Carneiro; Marcelo Maito; Fabian Richter; Agustina Legaz; Florencia Altschuler; Leidy Cubillos-Pinilla; Yu Chen; Colin P Doherty; Sandra Baez; Agustín Ibáñez

doi:10.1016/j.biopsych.2024.10.013

Neuroimaging meta-analyses reveal convergence of interoception, emotion, and social cognition across neurodegenerative diseases

Biol Psychiatry. 2024 Oct 21:S0006-3223(24)01697-4. doi: 10.1016/j.biopsych.2024.10.013. Online ahead of print.

Authors

Affiliations

¹ Latin American Brain Health Institute (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile; Cognitive Neuroscience Center (CNC), Universidad de San Andres, Buenos Aires, Argentina; The University of Sydney, Brain and Mind Centre, School of Psychology, Sydney, Australia.
² Laboratory of Neuropsychophysiology, Faculty of Psychology and Education Sciences, University of Porto, Portugal; Faculty of Medicine, University of Porto, Portugal; Department of Neurology, ULS do Alto Ave, Guimarães, Portugal.
³ Latin American Brain Health Institute (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile; Cognitive Neuroscience Center (CNC), Universidad de San Andres, Buenos Aires, Argentina.
⁴ Deutsches Herzzentrum der Charité, Department of Cardiothoracic and Vascular Surgery, Berlin, Germany; Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
⁵ Cognitive Neuroscience Center (CNC), Universidad de San Andres, Buenos Aires, Argentina.
⁶ Neurophysiological Leadership Lab, Technical University of Munich, Munich, Germany.
⁷ Department of Neurology, Memory and Aging Center, Weill Institute for Neurosciences, University of California San Francisco, San Francisco, California, USA.
⁸ Trinity College Dublin, Dublin, Ireland; Global Brain Health Institute (GBHI), University of California San Francisco (UCSF), CA, USA, Trinity College Dublin, Dublin, Ireland.
⁹ Global Brain Health Institute (GBHI), University of California San Francisco (UCSF), CA, USA, Trinity College Dublin, Dublin, Ireland; Universidad de los Andes, Bogota, Colombia.
¹⁰ Latin American Brain Health Institute (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile; Cognitive Neuroscience Center (CNC), Universidad de San Andres, Buenos Aires, Argentina; Global Brain Health Institute (GBHI), University of California San Francisco (UCSF), CA, USA, Trinity College Dublin, Dublin, Ireland. Electronic address: agustin.ibanez@gbhi.org.

PMID: 39442786
DOI: 10.1016/j.biopsych.2024.10.013

Abstract

Introduction: 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 PRISMA Activated Likelihood Estimate (ALE) metanalyses encompassed studies meeting inclusion criteria: interoception, emotion, or social cognition tasks; neurodegenerative diseases (behavioral variant frontotemporal dementia (bvFTD), primary progressive aphasias (PPAs) Alzheimer's disease (AD), Parkinson's Disease (PD), multiple sclerosis (MS)); and neuroimaging (structural: MRI voxel-based morphometry; functional: fMRI and FDG-PET).

Results: From 20,593 studies, 170 met inclusion criteria (58 interoception, 65 emotion, and 47 social cognition) involving 7032 participants (4963 patients and 2069 healthy controls). In all participants combined, conjunction analyses revealed AIN involvement of the insula, amygdala, orbitofrontal cortex, anterior cingulate, striatum, thalamus, and hippocampus across domains. In bvFTD 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 PD and the posterior insula in PPAs was also observed. In AD and MS, disruptions in the AIN were observed during interoception, but no convergence with emotion was identified.

Interpretation: Neurodegeneration induces dysfunctional AIN across atrophy, connectivity, and metabolism, more accentuated in bvFTD. 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.

Keywords: Interoception; allostasis; emotion; metanalysis; neuroimaging; social cognition.