Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness

Abstract

Relatively discrete experimental literatures have grown to support the insula's role in the domains of interoception, focal exteroceptive attention and cognitive control, and the experience of anxiety, even as theoretical accounts have asserted that the insula is a critical zone for integrating across these domains. Here we provide the first experimental demonstration that there exists a functional topography across the insula, with distinct regions in the same participants responding in a highly selective fashion for interoceptive, exteroceptive, and affective processing. Although each insular region is associated with areas of differential resting state functional connectivity relative to the other regions, overall their functional connectivity profiles are quite similar, thereby providing a map of how interoceptive, exteroceptive, and emotional awareness are integrated within the insular cortex.

Keywords: anxiety; exteroception; insula; interoception.

Figure 1

Random effects group conjunction analyses reveals insular regions responding selectively during interoception (orange), exteroception (blue), and anxiety (green). The coronal slices show the four regions of the insula exhibiting functionally selective responses as defined in the random effects conjunction analyses. For example, the two orange clusters at Y = −2 show regions in the right mid‐insula where activity during the interoception condition was greater than during the exteroception condition (P < 0.05 corrected) AND activity during interoception condition was greater than during the anxiety condition (P < 0.05 corrected) AND no reliable differences were observed in the activity during the exteroception and anxiety conditions. The bar graphs show the average percent signal change across participants in the four functionally selective clusters relative to the signal baseline. The colored planes running through the rendered brain in the top left corner of the figure show the locations of the three coronal slices. The color intensity gradations in each cluster represent the average t‐statistic at that voxel across all t‐maps included in the conjunction analysis.

Figure 2

Random effects group conjunction analyses demonstrating regions of selective resting‐state functional connectivity to either the interoception, exteroception, or anxiety insular seed regions. Regions in the mid‐ and posterior‐insula and somatosensory cortex highlighted in gold exhibited greater resting‐state functional connectivity to the dorsal mid‐insula cluster that responded selectively during the interoception condition in the task data, than to each of the other three seed regions defined in the task data (with each statistical contrast separately thresholded at P < 0.005). Regions in the ventral insula and subgenual anterior cingulate highlighted in red exhibited greater resting state functional connectivity to the ventral mid‐insula cluster that responded selectively during the interoception condition in the task data, relative to each of the other seed regions (again, with each statistical test separately thresholded at P < 0.005). Likewise, green and blue highlights show regions of selective functional connectivity to the anxiety‐ and exteroception‐selective clusters defined in the task data. The color intensity gradations in each cluster represent the average t‐statistic at that voxel across all t‐maps included in the conjunction analysis.

Figure 3

Random effects group conjunction analyses demonstrating regions of overlapping resting‐state functional connectivity to the interoception, exteroception, or anxiety insular seed regions. (a) Sagittal images show regions exhibiting resting‐state functional connectivity (P < 0.005) to the dorsal mid‐insula interoception seed region (gold), ventral mid‐insula interoception seed (red), ventral anterior insula anxiety seed (green), and dorsal anterior insula exteroception seed region. (b) Sagittal images showing regions of overlapping resting‐state functional connectivity (i.e., the conjunction of all four maps in Fig. 3a). The color intensity gradations in this figure represent the average t‐statistic at a voxel across all t‐maps included in the union of the t‐images. (c) eta² heat map demonstrating high overall similarity in the whole‐brain resting‐state functional connectivity maps for the interoception, exteroception, or anxiety insular seed regions. The color of each triangle indicates the average eta² value across all participants, with the individual participants' values indicated by the colors along the hypotenuse of each triangle.