Lateralized deficits in arousal processing after insula lesions: Behavioral and autonomic evidence

Olga Holtmann; Marcel Franz; Constanze Mönig; Jan-Gerd Tenberge; Insa Schloßmacher; Iskrena Ivanova; Christoph Preul; Wolfram Schwindt; Nico Melzer; Wolfgang H R Miltner; Thomas Straube

doi:10.1016/j.cortex.2021.12.013

Lateralized deficits in arousal processing after insula lesions: Behavioral and autonomic evidence

Cortex. 2022 Mar:148:168-179. doi: 10.1016/j.cortex.2021.12.013. Epub 2022 Jan 31.

Authors

Affiliations

¹ Institute of Medical Psychology and Systems Neuroscience, University of Muenster, Muenster, Germany; Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany. Electronic address: olga.holtmann@uni-muenster.de.
² Department of Clinical Psychology, Friedrich Schiller University Jena, Jena, Germany.
³ Department of Neurology with Institute of Translational Neurology, University Hospital Muenster, Muenster, Germany.
⁴ Institute of Medical Psychology and Systems Neuroscience, University of Muenster, Muenster, Germany; Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.
⁵ Institute of Medical Psychology and Systems Neuroscience, University of Muenster, Muenster, Germany.
⁶ Department of Neurology, University Hospital Jena, Jena, Germany.
⁷ Institute of Clinical Radiology, University Hospital Muenster, Muenster, Germany.
⁸ Department of Neurology with Institute of Translational Neurology, University Hospital Muenster, Muenster, Germany; Department of Neurology, Heinrich-Heine University of Düsseldorf, Düsseldorf, Germany.

PMID: 35180480
DOI: 10.1016/j.cortex.2021.12.013

Abstract

A large body of evidence ascribes a pivotal role in emotion processing to the insular cortex. However, the complex structure and lateralization of emotional deficits following insular damage are not understood. Here, we investigated emotional ratings of valence and arousal and skin conductance responses (SCR) to a graded series of emotionally arousing scenes in patients with left (n = 10) or right (n = 9) insular damage and in healthy controls (n = 18). We found a significant reduction in overall SCRs, arousal ratings and valence extremity scores in right-lesioned patients, as compared to left-lesioned patients and healthy controls. The degree of right insular damage was significantly correlated with the degree of arousal, SCR and extremity attenuation. Additional analyses of correlations between subjective arousal ratings resp. SCR and normative arousal ratings revealed that both lesion groups had evaluative and physiological difficulties to discover changes in stimulus arousal. Although no group differences emerged on overall ratings of valence, analysis of correlations between subjective and normative valence ratings displayed markedly reduced accuracy in right-lesioned patients, as compared to left-lesioned patients and healthy controls. Our findings support the hypothesis that the left and right insulae subserve different functions in emotion processing, potentially due to asymmetrical representations of autonomic information in the left and right human forebrain. The right insula may serve as integral node for sympathetic arousal and cognitive-affective processing.

Keywords: Arousal; Emotion; Hemispheric lateralization; Insular cortex; Lesion analysis.

Publication types

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

MeSH terms

Arousal* / physiology
Autonomic Nervous System
Emotions* / physiology
Humans