Dataset Information

A common gustatory and interoceptive representation in the human mid-insula.

ABSTRACT: The insula serves as the primary gustatory and viscerosensory region in the mammalian cortex. It receives visceral and gustatory afferent projections through dedicated brainstem and thalamic nuclei, which suggests a potential role as a site for homeostatic integration. For example, while human neuroimaging studies of gustation have implicated the dorsal mid-insular cortex as one of the primary gustatory regions in the insula, other recent studies have implicated this same region of the insula in interoception. This apparent convergence of gustatory and interoceptive information could reflect a common neural representation in the insula shared by both interoception and gustation. This idea finds support in translational studies in rodents, and may constitute a medium for integrating homeostatic information with feeding behavior. To assess this possibility, healthy volunteers were asked to undergo fMRI while performing tasks involving interoceptive attention to visceral sensations as well as a gustatory mapping task. Analysis of the unsmoothed, high-resolution fMRI data confirmed shared representations of gustatory and visceral interoception within the dorsal mid-insula. Group conjunction analysis revealed overlapping patterns of activation for both tasks in the dorsal mid-insula, and region-of-interest analyses confirmed that the dorsal mid-insula regions responsive for visceral interoception also exhibit strong responses to tastants.

SUBMITTER: Avery JA

PROVIDER: S-EPMC4795826 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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A common gustatory and interoceptive representation in the human mid-insula.

Avery Jason A JA Kerr Kara L KL Ingeholm John E JE Burrows Kaiping K Bodurka Jerzy J Simmons W Kyle WK

Human brain mapping 20150506 8

The insula serves as the primary gustatory and viscerosensory region in the mammalian cortex. It receives visceral and gustatory afferent projections through dedicated brainstem and thalamic nuclei, which suggests a potential role as a site for homeostatic integration. For example, while human neuroimaging studies of gustation have implicated the dorsal mid-insular cortex as one of the primary gustatory regions in the insula, other recent studies have implicated this same region of the insula in ...[more]

PMID: 25950427

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Project description:Interoceptive awareness (IA), the subjective and conscious perception of visceral and physiological signals from the body, has been associated with functions of cortical and subcortical neural systems involved in emotion control, mood and anxiety disorders. We recently hypothesized that IA and its contributions to mental health are realized by a brain interoception network (BIN) linking brain regions that receive ascending interoceptive information from the brainstem, such as the amygdala, insula and anterior cingulate cortex (ACC). However, little evidence exists to support this hypothesis. In order to test this hypothesis, we used a publicly available dataset that contained both anatomical neuroimaging data and an objective measure of IA assessed with a heartbeat detection task. Whole-brain Voxel-Based Morphometry (VBM) was used to investigate the association of IA with gray matter volume (GMV) and the structural covariance network (SCN) of the amygdala, insula and ACC. The relationship between IA and mental health was investigated with questionnaires that assessed depressive symptoms and anxiety. We found a positive correlation between IA and state anxiety, but not with depressive symptoms. In the VBM analysis, only the GMV of the left anterior insula showed a positive association with IA. A similar association was observed between the parcellated GMV of the left dorsal agranular insula, located in the anterior insula, and IA. The SCN linking the right dorsal agranular insula with the left dorsal agranular insula and left hyper-granular insula were positively correlated with IA. No association between GMV or SCN and depressive symptoms or anxiety were observed. These findings revealed a previously unknown association between IA, insula volume and intra-insula SCNs. These results may support development of non-invasive neuroimaging interventions, e.g., neurofeedback, seeking to improve IA and to prevent development of mental health problems, such anxiety disorders.

Project description:Individuals with anorexia nervosa (AN) typically display anxious traits prior to the onset of food avoidance and weight loss that characterize the disorder. Meal associated anxiety is an especially common clinical feature in these patients, and heightened sensitivity to sympathetically mediated interoceptive sensations has also been observed. However, it remains unclear how heightened interoceptive sensitivity relates to experiences of anxiety before and after meals. To investigate this relationship, we experimentally induced anxiety and panic symptoms with isoproterenol, a peripheral sympathetic agonist similar to adrenaline, across several different conditions: during panic provocation, during anticipation of a 1,000 Calorie meal, and after meal consumption. Fifteen AN and 15 age- and sex-matched healthy comparisons received bolus infusions of isoproterenol and saline in a double-blinded, randomized design. Participants rated anxiety symptoms after each infusion, completed panic rating scales, and traced the location of perceived palpitations on a manikin to index interoceptive "body map" representation. The AN group reported significantly elevated anxiety relative to healthy comparisons during infusions before and after the meal, but surprisingly, not during panic provocation. These symptoms were accompanied by geographical differences in patterns of perceived heartbeat sensations across each condition. In particular, the AN group localized heartbeat sensations disproportionately to the chest during meal related saline infusions, when no cardiorespiratory modulation actually occurred. The AN group also showed a trend toward higher panic attack rates during the meal anticipation period. Correcting for anxiety levels reported during saline infusions abolished group differences in anxiety change across all conditions, suggesting a significant contribution of anxious traits in AN. The observation of meal related "visceral illusions" provides further evidence that AN is associated with abnormal interoceptive representation of the heartbeat and suggests that meal consumption, particularly when anticipated, preferentially alters the processing of interoception related signals in AN.

Dataset Information

A common gustatory and interoceptive representation in the human mid-insula.

Publications

A common gustatory and interoceptive representation in the human mid-insula.

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