Two systems of resting state connectivity between the insula and cingulate cortex

Abstract

The insula and cingulate cortices are implicated in emotional, homeostatic/allostatic, sensorimotor, and cognitive functions. Non-human primates have specific anatomical connections between sub-divisions of the insula and cingulate. Specifically, the anterior insula projects to the pregenual anterior cingulate cortex (pACC) and the anterior and posterior mid-cingulate cortex (aMCC and pMCC); the mid-posterior insula only projects to the posterior MCC (pMCC). In humans, functional neuroimaging studies implicate the anterior insula and pre/subgenual ACC in emotional processes, the mid-posterior insula with awareness and interoception, and the MCC with environmental monitoring, response selection, and skeletomotor body orientation. Here, we tested the hypothesis that distinct resting state functional connectivity could be identified between (1) the anterior insula and pACC/aMCC; and (2) the entire insula (anterior, middle, and posterior insula) and the pMCC. Functional connectivity was assessed from resting state fMRI scans in 19 healthy volunteers using seed regions of interest in the anterior, middle, and posterior insula. Highly correlated, low-frequency oscillations (< 0.05 Hz) were identified between specific insula and cingulate subdivisions. The anterior insula was shown to be functionally connected with the pACC/aMCC and the pMCC, while the mid/posterior insula was only connected with the pMCC. These data provide evidence for a resting state anterior insula-pACC/aMCC cingulate system that may integrate interoceptive information with emotional salience to form a subjective representation of the body; and another system that includes the entire insula and MCC, likely involved in environmental monitoring, response selection, and skeletomotor body orientation.

2008 Wiley-Liss, Inc.

Figures

Figure 1

Whole brain multisubject conjunction analysis showing anterior insula connectivity with the cingulate cortex. The spectral analysis and ROI time course from a single subject is shown for the left (A, B) and right (D, E) anterior insula (aIC). These regions had tight correlations of low‐frequency oscillations (B, E) with the pregenual and mid‐cingulate cortex (C, F).

Figure 2

Whole brain multisubject conjunction analysis showing mid‐insula connectivity with the cingulate cortex. The spectral analysis and ROI time course from a single subject is shown for the left (A, B) and right (D, E) mid‐insula (mIC). These regions had tight correlations of low frequency oscillations (B, E) with the mid‐cingulate cortex (C, F).

Figure 3

Whole brain multisubject conjunction analysis showing posterior insula connectivity with the cingulate cortex. The spectral analysis and ROI time course from a single subject is shown for the left (A, B) and right (D, E) posterior insula (pIC). These regions had tight correlations of low frequency oscillations (B, E) with the mid‐cingulate cortex (C, F).

Figure 4

Insula connectivity fingerprints. (A) ROI's placed in the anterior (red), mid (blue), and posterior (green) insula are shown for a single subject. (B) Polar plots illustrating patterns of connectivity of each insula subdivision with the cingulate cortex and also key somatosensory brain areas. These fingerprints are based on the correlations between pairs of brain areas. Concentric circles represent increasing t‐values of the correlation between resting activity of an insula ROI and the pregenual/anterior mid‐cingulate (pACC/aMCC), posterior mid‐cingulate cortex (pMCC), primary somatosensory (S1), and secondary somatosensory (S2) cortex. The lighter outer circle denotes the region of statistical significance at t > 4. R, right; L, left.

Figure 5

Random effects contrast maps. All 19 subjects and their insula ROIs were included in the statistical model. Contrasts were made between: (1) bilateral anterior IC minus bilateral posterior (first column); (2) bilateral anterior IC minus bilateral mid‐IC (second column); (3) bilateral mid‐IC minus bilateral posterior IC (third column). Maps were thresholded at corrected P < 0.05. Anterior insula demonstrates stronger connectivity with the pACC/aMCC than either the mid or posterior insular cortex. No significant differences were identified for the pMCC, S1 or S2. IC = insular cortex.