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.

Keywords: gustation; insula; interoception.

Figure 1

fMRI task design. (A) Gustatory Mapping task. The delivery of a sweet or neutral tastant was preceded by a word cue and followed by a “wash/swallow” period to rinse out and remove the liquid. (B) Interoceptive Attention task. During 10‐second trials, subjects would focus on a part of the body indicated by a cue word, either “HEART”, “STOMACH”, or “BLADDER,” or would count the number of times (between 1 and 7) that the word “TARGET” switched to the lowercase “target.” [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Gustatory–Interoceptive Overlap. The unsmoothed fMRI data was mapped and analyzed on a standardized cortical surface model (above), and statistical maps were cluster‐size corrected for multiple comparisons at P < 0.05. (A) Within the insula, interoceptive attention (yellow‐orange) resulted in significantly greater activation than exteroceptive attention (blue) bilaterally in mid and posterior regions of the insula. (B) Bilateral regions of the dorsal mid‐insula also exhibited a reliably greater response to the sweet vs. the neutral tastant. (C) A union of the statistical maps in A and B. Gustation and interoception tasks coactivated a region of right dorsal mid‐insula, situated at the dorsal margin of the posterior short insular gyrus. (Bottom left and right) Volume renderings of the surface figures in C. Gil—long insular gyri, Gis—short insular gyri, L—left, R—right, Sia—anterior insular sulcus, Sii—inferior insular sulcus, Sis—superior insular sulcus. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Gustatory ROI analyses. The regions of the insula identified in Figure 2a were used to examine the gustatory response profile across posterior, mid, and anterior regions of the insula. Only the bilateral dorsal mid‐insula exhibited both a significant response to sweet and neutral tastants individually, as well as a significant difference between those responses. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]