Thinking versus feeling: How interoception and cognition influence emotion recognition in behavioural-variant frontotemporal dementia, Alzheimer's disease, and Parkinson's disease

Author: Jessica L Hazelton1, Sol Fittipaldi2, Matias Fraile-Vazquez3, Marion Sourty4, Agustina Legaz5, Anna L Hudson6, Indira Garcia Cordero7, Paula C Salamone8, Adrian Yoris9, Agustín Ibañez10, Olivier Piguet1, Fiona Kumfor11
Affiliation:
1 The University of Sydney, School of Psychology, Sydney, Australia; The University of Sydney, Brain & Mind Centre, Sydney, Australia.
2 Cognitive Neuroscience Center (CNC) Universidad de San Andres, Buenos Aires, Argentina; National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Facultad de Psicología, Universidad Nacional de Córdoba, Argentina; Latin American Brain Health Institute (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile.
3 Cognitive Neuroscience Center (CNC) Universidad de San Andres, Buenos Aires, Argentina.
4 The University of Sydney, Brain & Mind Centre, Sydney, Australia; The University of Sydney, School of Engineering, Sydney, Australia.
5 Cognitive Neuroscience Center (CNC) Universidad de San Andres, Buenos Aires, Argentina; National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Facultad de Psicología, Universidad Nacional de Córdoba, Argentina.
6 Flinders University, College of Medicine and Public Health, Adelaide, Australia; Neuroscience Research Australia (NeuRA), Sydney, Australia; The University of New South Wales, School of Medical Sciences, Sydney, Australia.
7 Cognitive Neuroscience Center (CNC) Universidad de San Andres, Buenos Aires, Argentina; National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, Canada.
8 National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Department of Biomedical and Clinical Sciences, Center for Social and Affective Neuroscience, Linköping University, Linköping, Sweden.
9 National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Institute of Cognitive and Translational Neuroscience (INCYT), Buenos Aires, Argentina.
10 Cognitive Neuroscience Center (CNC) Universidad de San Andres, Buenos Aires, Argentina; National Scientific and Technical Research Council (CONICET), Buenos Aires, Argentina; Latin American Brain Health Institute (BrainLat), Universidad Adolfo Ibáñez, Santiago, Chile; Global Brain Health Institute, University of California, San Francisco, USA; Trinity College Dublin (TCD), Dublin, Ireland.
11 The University of Sydney, School of Psychology, Sydney, Australia; The University of Sydney, Brain & Mind Centre, Sydney, Australia. Electronic address: fiona.kumfor@sydney.edu.au.
Conference/Journal: Cortex
Date published: 2023 Mar 23
Other: Volume ID: 163 , Pages: 66-79 , Special Notes: doi: 10.1016/j.cortex.2023.02.009. , Word Count: 255


Disease-specific mechanisms underlying emotion recognition difficulties in behavioural-variant frontotemporal dementia (bvFTD), Alzheimer's disease (AD), and Parkinson's disease (PD) are unknown. Interoceptive accuracy, accurately detecting internal cues (e.g., one's heart beating), and cognitive abilities are candidate mechanisms underlying emotion recognition. One hundred and sixty-eight participants (52 bvFTD; 41 AD; 24 PD; 51 controls) were recruited. Emotion recognition was measured via the Facial Affect Selection Task or the Mini-Social and Emotional Assessment Emotion Recognition Task. Interoception was assessed with a heartbeat detection task. Participants pressed a button each time they: 1) felt their heartbeat (Interoception); or 2) heard a recorded heartbeat (Exteroception-control). Cognition was measured via the Addenbrooke's Cognitive Examination-III or the Montreal Cognitive Assessment. Voxel-based morphometry analyses identified neural correlates associated with emotion recognition and interoceptive accuracy. All patient groups showed worse emotion recognition and cognition than controls (all P's ≤ .008). Only the bvFTD showed worse interoceptive accuracy than controls (P < .001). Regression analyses revealed that in bvFTD worse interoceptive accuracy predicted worse emotion recognition (P = .008). Whereas worse cognition predicted worse emotion recognition overall (P < .001). Neuroimaging analyses revealed that the insula, orbitofrontal cortex, and amygdala were involved in emotion recognition and interoceptive accuracy in bvFTD. Here, we provide evidence for disease-specific mechanisms for emotion recognition difficulties. In bvFTD, emotion recognition impairment is driven by inaccurate perception of the internal milieu. Whereas, in AD and PD, cognitive impairment likely underlies emotion recognition deficits. The current study furthers our theoretical understanding of emotion and highlights the need for targeted interventions.

Keywords: Behavioural-variant frontotemporal dementia; Emotion; Insula; Interoception; Social cognition.

PMID: 37075507 DOI: 10.1016/j.cortex.2023.02.009

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