Hemispheric contributions toward interoception and emotion recognition in left-vs right-semantic dementia

Jessica L Hazelton; Emma Devenney; Rebekah Ahmed; James Burrell; Yun Hwang; Olivier Piguet; Fiona Kumfor

doi:10.1016/j.neuropsychologia.2023.108628

Hemispheric contributions toward interoception and emotion recognition in left-vs right-semantic dementia

Neuropsychologia. 2023 Sep 9:188:108628. doi: 10.1016/j.neuropsychologia.2023.108628. Epub 2023 Jun 20.

Authors

Jessica L Hazelton¹, Emma Devenney², Rebekah Ahmed³, James Burrell⁴, Yun Hwang⁵, Olivier Piguet¹, Fiona Kumfor⁶

Affiliations

¹ The University of Sydney, School of Psychology, Sydney, NSW, Australia; The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia.
² The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia; The University of Sydney, Faculty of Medicine and Health Translational Research Collective, Sydney, NSW, Australia.
³ The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia; Memory and Cognition Clinic, Department of Clinical Neurosciences, Royal Prince Alfred Hospital, Sydney, NSW, Australia.
⁴ The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia; The University of Sydney, Concord Clinical School, Sydney, NSW, Australia.
⁵ The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia; Gosford General Hospital, Gosford, NSW, Australia.
⁶ The University of Sydney, School of Psychology, Sydney, NSW, Australia; The University of Sydney, Brain and Mind Centre, Sydney, NSW, Australia. Electronic address: [email protected].

PMID: 37348648
DOI: 10.1016/j.neuropsychologia.2023.108628

Abstract

Background: The hemispheric contributions toward interoception, the perception of internal bodily cues, and emotion recognition remains unclear. Semantic dementia cases with either left-dominant (i.e., left-SD) or right-dominant (i.e., right-SD) anterior temporal lobe atrophy experience emotion recognition difficulties, however, little is known about interoception in these syndromes. Here, we hypothesised that right-SD would show worse interoception and emotion recognition due to right-dominant atrophy.

Methods: Thirty-five participants (8 left-SD; 6 right-SD; 21 controls) completed a monitoring task. Participants pressed a button when they: (1) felt their heartbeat, without pulse measurement (Interoception); or (2) heard a recorded heartbeat (Exteroception-control). Simultaneous ECG was recorded. Accuracy was calculated by comparing the event frequency (i.e., heartbeat or sound) to response frequency. Emotion recognition was assessed via the Facial Affect Selection Task. Voxel-based morphometry analyses identified neural correlates of interoception and emotion recognition.

Results: Right-SD showed worse interoception than controls and left-SD (both p's < 0.001). Both patient groups showed worse emotion recognition than controls (right-SD: p < .001; left-SD: p = .018), and right-SD showed worse emotion recognition than left-SD (p = .003). Regression analyses revealed that worse emotion recognition was predicted by right-SD (p = .002), left-SD (p = .005), and impaired interoception (p = .004). Interoception and emotion were associated with the integrity of right-lateralised structures including the insula, temporal pole, thalamus, superior temporal gyrus, and hippocampus.

Conclusion: Our study provides the first evidence for impaired interoception in right-SD, suggesting that impaired emotion recognition in this syndrome is driven by inaccurate internal monitoring. Further we identified a common neurobiological basis for interoception and emotion in the right hemisphere.

Keywords: Emotion; Insula; Interoception; Lateralisation; Semantic dementia.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Atrophy
Emotions / physiology
Frontotemporal Dementia* / diagnostic imaging
Frontotemporal Dementia* / psychology
Humans
Interoception*
Magnetic Resonance Imaging
Recognition, Psychology / physiology