Differential structural and resting state connectivity between insular subdivisions and other pain-related brain regions

K Wiech,S Jbabdi,C.S Lin,J Andersson,I Tracey

doi:10.1016/j.pain.2014.07.009

Abstract

Functional neuroimaging studies suggest that the anterior, mid, and posterior division of the insula subserve different functions in the perception of pain. The anterior insula (AI) has predominantly been associated with cognitive–affective aspects of pain, while the mid and posterior divisions have been implicated in sensory-discriminative processing. We examined whether this functional segregation is paralleled by differences in (1) structural and (2) resting state connectivity and (3) in correlations with pain-relevant psychological traits. Analyses were restricted to the 3 insular subdivisions and other pain-related brain regions. Both type of analyses revealed largely overlapping results. The AI division was predominantly connected to the ventrolateral prefrontal cortex (structural and resting state connectivity) and orbitofrontal cortex (structural connectivity). In contrast, the posterior insula showed strong connections to the primary somatosensory cortex (SI; structural connectivity) and secondary somatosensory cortex (SII; structural and resting state connectivity). The mid insula displayed a hybrid connectivity pattern with strong connections with the ventrolateral prefrontal cortex, SII (structural and resting state connectivity) and SI (structural connectivity). Moreover, resting state connectivity revealed strong connectivity of all 3 subdivisions with the thalamus. On the behavioural level, AI structural connectivity was related to the individual degree of pain vigilance and awareness that showed a positive correlation with AI-amygdala connectivity and a negative correlation with AI–rostral anterior cingulate cortex connectivity. In sum, our findings show a differential structural and resting state connectivity for the anterior, mid, and posterior insula with other pain-relevant brain regions, which might at least partly explain their different functional profiles in pain processing.

Highlights

Of the various brain regions that have been implicated in the perception of pain, the insula has most consistently been reported across studies [17]
The anterior insula (AI) showed a significant interaction between TARGET and HEMISPHERE (F(1.95,27.31) = 8.27, P = .002), suggesting that the differential connectivity with pain-related brain regions varied between hemispheres
Our data indicate that AI, mid insula (MI), and PI are differentially connected with pain-related brain regions and that their connectivity is linked to pain-relevant behaviour

Summary

Introduction

Of the various brain regions that have been implicated in the perception of pain, the insula has most consistently been reported across studies [17]. Often referred to as the insula or the insular cortex, studies in primates indicate that this structure consists of an anterior, mid, and posterior part, which differ considerably in anatomy and cytoarchitecture [5]. In accordance with these findings, functional neuroimaging studies on pain (and other sensory experiences) in humans suggest a. Activity in the posterior (PI) and mid insula (MI) predominantly reflects sensory aspects of pain [1,35,44]. The anterior insula (AI), in contrast, has been associated with the cognitive–affective dimension of pain that is sensitive to contextual manipulations [40,62]

Methods

Results

Discussion

Conclusion