Jessica L. Hazelton , Emma Devenney , Rebekah Ahmed , James Burrell , Yun Hwang , Olivier Piguet , Fiona Kumfor
{"title":"Hemispheric contributions toward interoception and emotion recognition in left-vs right-semantic dementia","authors":"Jessica L. Hazelton , Emma Devenney , Rebekah Ahmed , James Burrell , Yun Hwang , Olivier Piguet , Fiona Kumfor","doi":"10.1016/j.neuropsychologia.2023.108628","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><p>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.</p></div><div><h3>Methods</h3><p>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.</p></div><div><h3>Results</h3><p>Right-SD showed worse interoception than controls and left-SD (both <em>p's</em> < 0.001). Both patient groups showed worse emotion recognition than controls (right-SD: <em>p</em> < .001; left-SD: <em>p</em> = .018), and right-SD showed worse emotion recognition than left-SD (<em>p</em> = .003). Regression analyses revealed that worse emotion recognition was predicted by right-SD (<em>p</em> = .002), left-SD (<em>p</em> = .005), and impaired interoception (<em>p</em> = .004). Interoception and emotion were associated with the integrity of right-lateralised structures including the insula, temporal pole, thalamus, superior temporal gyrus, and hippocampus.</p></div><div><h3>Conclusion</h3><p>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.</p></div>","PeriodicalId":19279,"journal":{"name":"Neuropsychologia","volume":"188 ","pages":"Article 108628"},"PeriodicalIF":2.0000,"publicationDate":"2023-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"1","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuropsychologia","FirstCategoryId":"102","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0028393223001628","RegionNum":3,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BEHAVIORAL SCIENCES","Score":null,"Total":0}
引用次数: 1
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.
期刊介绍:
Neuropsychologia is an international interdisciplinary journal devoted to experimental and theoretical contributions that advance understanding of human cognition and behavior from a neuroscience perspective. The journal will consider for publication studies that link brain function with cognitive processes, including attention and awareness, action and motor control, executive functions and cognitive control, memory, language, and emotion and social cognition.