Beyond the tripartite cognition-emotion-interoception model of the human insular cortex

Abstract

Functional MRI studies report insular activations across a wide range of tasks involving affective, sensory, and motor processing, but also during tasks of high-level perception, attention, and control. Although insular cortical activations are often reported in the literature, the diverse functional roles of this region are still not well understood. We used a meta-analytic approach to analyze the coactivation profiles of insular subdivisions-dorsal anterior, ventral anterior, and posterior insula-across fMRI studies in terms of multiple task domains including emotion, memory, attention, and reasoning. We found extensive coactivation of each insular subdivision, with substantial overlap between coactivation partners for each subdivision. Functional fingerprint analyses revealed that all subdivisions cooperated with a functionally diverse set of regions. Graph-theoretical analyses revealed that the dorsal anterior insula was a highly "central" structure in the coactivation network. Furthermore, analysis of the studies that activate the insular cortex itself showed that the right dorsal anterior insula was a particularly "diverse" structure in that it was likely to be active across multiple task domains. These results highlight the nuanced functional profiles of insular subdivisions and are consistent with recent work suggesting that the dorsal anterior insula can be considered a critical functional hub in the human brain.

Figure 1. Insula subdivisions

The insula was divided following the parcellation scheme reported by (Deen et al., 2010) into three subdivisions: dorsal anterior (blue), ventral anterior (green), and posterior (red).

Figure 2. Determination of functional fingerprints

To illustrate the process, only three task domains are shown. The actual fingerprints used in the paper were 32-dimensional. The label “regional” refers to voxels (via the searchlight) or regions of interest. The final normalization step ensures that the fingerprint values all sum to 1.

Figure 3. Schematic diagram of data analysis

(A) Coactivation maps and functional fingerprints. Using data from the Neurosynth database, task-based coactivations were determined for each insular subdivision by moving a searchlight in a voxel-wise manner. The blue arrows denote the strength of partial correlation between an insular subdivision and specific voxels on the surface. All significant voxels contributed to the functional fingerprint of the “partner” regions that coactivated with the specific insular subregion. Their contribution was proportional to the value of the partial correlation (as indicated by the green arrow widths). To determine the fingerprints BrainMap data that includes task domain classification was used. (B) Network analysis. Using NeuroSynth data, pairwise correlations between a set of ROIs were computed and used in the graph-theoretic analysis.

Figure 4. Coactivation of insula subdivisions

Using data from the Neurosynth database, task-based coactivation profiles were determined for each insular subdivision by moving a searchlight in a voxel-wise manner. The color bar indicates the partial correlation value with the specific insular subregion “seed” when all other subdivisions were also considered.

Figure 5. Overlap between connection partners of each insular subdivision

To facilitate displaying overlap, the corresponding right and left insular subregions were pooled together resulting in three insular subregions (dorsal anterior, ventral anterior, posterior insula). Voxels shown in green-to-red colors were coactive with two out of the three subregions (the color bar indicates the strength of overlap, specifically, the smallest value of the two strongest partial correlations). Voxels in blue were coactive across all three subdivisions.

Figure 6. Overlap between connection partners of each insular subdivision

As in Figure 5, voxels in blue were coactive across all three subdivisions. The slices shown highlight several notable brain regions, including thalamus, caudate, putamen, anterior cingulate cortex, left temporo-parietal junction, and right lateral PFC.

Figure 7. “Common” functional fingerprint of insular subdivisions

The common fingerprint was determined by combining all six insular subregion (see text). All task domains were engaged by each subregion at least some of the time. TOM: theory of mind; MemWork: working memory; MemOther: long-term memory.

Figure 8. “Specific” functional fingerprints of insular subdivisions

When the “average profile” (not shown) is subtracted out, particular features are observed in the fingerprints. L: left; R: right; d: dorsal; v: ventral; P: posterior; AI: anterior insula; I: insula. The black circle represents zero, with points outside representing features found more in the given subdivision than the overall insula, and points within the black circle representing features found less in the given subdivision than the overall insula. Other abbreviations as in Figure 7.