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

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

doi:10.1101/2021.03.24.436828

Cited by 4 publications

(4 citation statements)

References 72 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The activation dominance of the right anterior insula may be explained by the functional roles of cardiac interoceptive awareness: people can notice increased arousal with heartbeat perception (Paulus et al, 2019). The right insula appears essential to perceive arousal as resection of the region causally diminishes physiological and emotional arousal (Terasawa et al, 2021;Holtmann et al, 2022). Moreover, presenting accelerated cardiac feedback increases perceived physiological arousal (Story and Craske, 2008) and, more importantly, activates the right anterior insula (Gray et al, 2007;Kleint et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Cardiac and Gastric Interoceptive Awareness Have Distinct Neural Substrates

Haruki

Ogawa²

2023

eNeuro

View full text Add to dashboard Cite

Interoceptive awareness, an awareness of the internal body state, guides adaptive behavior by providing ongoing information on body signals, such as heart rate and energy status. However, it is still unclear how interoceptive awareness of different body organs are represented in the human brain. Hence, we directly compared the neural activations accompanying attention to cardiac (related to heartbeat) and gastric (related to stomach) sensations, which generate cardiac and gastric interoceptive awareness, in the same population (healthy humans, N = 31). Participants were asked to direct their attention towards heart and stomach sensations and become aware of them in a magnetic resonance imaging scanner. The results indicated that the neural activations underlying gastric attention encompassed larger brain regions, including the occipitotemporal visual cortices, bilateral primary motor cortices, primary somatosensory cortex, left orbitofrontal cortex, and hippocampal regions. Cardiac attention, however, selectively activated the right anterior insula extending to the frontal operculum compared to gastric attention. Moreover, our detailed analyses focusing on the insula, the most relevant region for interoceptive awareness, revealed that the left dorsal middle insula encoded cardiac and gastric attention via different activation patterns, but the posterior insula did not. Our results demonstrate that cardiac and gastric attention evoke different brain activation patterns; in particular, the selective activation may reflect differences in the functional roles of cardiac and gastric interoceptive awareness.Significance statementInteroceptive awareness, senses that arise from within the body, play a critical role in adaptive behavior by providing ongoing information on bodily states, such as the heart rate and energy status. Although interoceptive awareness has various functions depending on its source, previous neuroimaging studies have extensively used cardiac awareness (related to the heartbeat). The present study showed that attention to cardiac and gastric (related to the stomach) sensations evoked distinct neural activation patterns by combining mass-univariate analysis with multivoxel pattern analysis using fMRI, indicating that the brain encodes attention to and thus awareness of different bodily organs in different manner. Moreover, the selective brain activation may reflect differences in the functional roles of cardiac and gastric awareness.

show abstract

Section: Discussionmentioning

confidence: 99%

Cardiac and Gastric Interoceptive Awareness Have Distinct Neural Substrates

Haruki

Ogawa²

2023

eNeuro

View full text Add to dashboard Cite

show abstract

“…Contrary to our expectations, patients with insula lesions showed SCRs comparable with those of HCs. In contrast, in a number of different emotion-processing tasks, patients with insula lesions showed reduced SCR towards pictures of emotional scenes [ 28 ] and auditory stimuli [ 27 ]. An explanation might be that facial expressions induce lower subjective arousal [ 54 ] and smaller SCRs [ 55 ] compared to pictures of emotional scenes for example, and, hence, result in less variability in the data.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, SCR was found to differentiate between facial expressions [ 24 , 26 ]. In contrast, in patients with insular lesions after stroke reduced arousal have been shown during emotionally evocative stimuli [ 27 , 28 ], though responses towards facial expressions have been rarely examined in stroke cohorts [ 29 ]. However, since insular cortex thickness was found to be positively associated with SCR during facial expressions of emotions in healthy participants [ 30 ], we expect to find lowered SCR during face processing in our insula stroke cohort.…”

Section: Introductionmentioning

confidence: 99%

Down-modulation of functional ventral striatum activation for emotional face stimuli in patients with insula damage

K.,

M.,

et al. 2024

PLoS ONE

View full text Add to dashboard Cite

Insula damage results in substantial impairments in facial emotion recognition. In particular, left hemispheric damage appears to be associated with poorer recognition of aversively rated facial expressions. Functional imaging can provide information on differences in the processing of these stimuli in patients with insula lesions when compared to healthy matched controls (HCs). We therefore investigated 17 patients with insula lesions in the chronic stage following stroke and 13 HCs using a passive-viewing task with pictures of facial expressions testing the blood oxygenation dependent (BOLD) effect in predefined regions of interest (ROIs). We expected a decrease in functional activation in an area modulating emotional response (left ventral striatum) but not in the facial recognition areas in the left inferior fusiform gyrus. Quantification of BOLD-response in ROIs but also voxel-based statistics confirmed this hypothesis. The voxel-based analysis demonstrated that the decrease in BOLD in the left ventral striatum was driven by left hemispheric damaged patients (n = 10). In our patient group, insula activation was strongly associated with the intensity rating of facial expressions. In conclusion, the combination of performance testing and functional imaging in patients following circumscribed brain damage is a challenging method for understanding emotion processing in the human brain.

show abstract

“…The activation dominance in the right anterior insula may be explained by its functional roles: people can notice increased arousal with cardiac interoception (Paulus et al, 2019). The right insula appears essential to perceive arousal as the resection of the region causally diminishes physiological and emotional arousal (Holtmann et al, 2022; Terasawa et al, 2021). Moreover, presenting accelerated cardiac feedback increases perceived physiological arousal (Story and Craske, 2008) and, more importantly, activates the right anterior insula (Gray et al, 2007; Kleint et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Cardiac and gastric interoception have distinct neural substrates

Haruki

Ogawa

2022

Preprint

View full text Add to dashboard Cite

The functional roles of interoception or senses that arise from within the body have been thought to guide the agents in adaptive behavior by informing of various bodily states such as a heart rate or energy status. However, direct evidence that the different types of interoception are processed or represented differently in the human brain is still lacking. Here, we directly compared the neural activation for cardiac (awareness related to heartbeats) and gastric (awareness related to stomach) interoception in the same population (N = 31) where the participants were asked to focus on sensations of their heart and stomach in the magnetic resonance imaging scanner. The result showed that neural activation underlying gastric interoception encompassed the sensorimotor and reward-related regions when compared to cardiac interoception, including the occipitotemporal visual cortices, bilateral primary motor cortex, primary somatosensory cortex, left orbitofrontal cortex, and bilateral hippocampal regions. Conversely, cardiac interoception selectively activated the right frontal operculum/insula in contrast to gastric interoception. Moreover, we found that the left dorsal middle insula encoded cardiac and gastric interoception differently but the posterior insula was not by performing multivoxel pattern analysis. Our results demonstrated that cardiac and gastric interoception, different types of bodily awareness, have distinct neural substrates particularly relevant to the functions for each interoception for the first time.

show abstract

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

Cited by 4 publications

References 72 publications

Cardiac and Gastric Interoceptive Awareness Have Distinct Neural Substrates

Cardiac and Gastric Interoceptive Awareness Have Distinct Neural Substrates

Down-modulation of functional ventral striatum activation for emotional face stimuli in patients with insula damage

Cardiac and gastric interoception have distinct neural substrates

Contact Info

Product

Resources

About