Structural connectivity profile supports laterality of the salience network

Abstract

The salience network (SN) is mainly involved in detecting and filtering multimodal salient stimuli, and mediating the switch between the default mode network and central executive network. Early studies have indicated a right-sided dominance in the functional organization of the SN; however, the anatomical basis of the functional lateralization remains unclear. Here, we hypothesized that the structural connectivity profile between the frontoinsular cortex (FIC) and dorsal anterior cingulate cortex (dACC), which are two core hubs of the SN, is also dominant in the right hemisphere. Based on diffusion and resting-state functional magnetic resonance imaging (rfMRI) of adult healthy volunteers in independent datasets, we found a stable right-sided laterality of both the FIC-dACC structural and functional connectivity in both the human connectome project cohort and a local Chinese cohort. Furthermore, a significant effect of aging on the integrity of the right FIC-dACC structural connectivity was also identified. The right-sided laterality of the structural organization of the SN may help us to better understand the functional roles of the SN in the normal human brain.

Keywords: aging; diffusion magnetic resonance imaging; dorsal anterior cingulate cortex; frontal insula cortex; laterality; salience network; structural connectivity.

Figure 1

Flow diagram of the study. ① The FIC and dACC defined by HCP rfMRI dataset were used as the seeds to track the fiber bundles in the Chinese young cohort. ② The fiber probability map created using the HCP dMRI dataset was used to extract the FA values along the right FIC‐dACC fiber trajectory in the Chinese elder cohort. Abbreviations: dACC, dorsal anterior cingulate cortex; dMRI, diffusion magnetic resonance imaging; FA, fractional anisotropy; FIC, frontoinsular cortex; HCP, human connectome project; FIC, frontoinsular cortex; rfMRI, resting‐state functional magnetic resonance imaging; SN, salience network

Figure 2

Spatial distribution of the salience network as identified by functional connectivity. Mapping of the SN is reconstructed by conjunction analysis (q < 0.001, FDR corrected) of functional connectivity of three SN core hubs (the bilateral FIC and the dACC) from each run of the HCP rfMRI dataset (a–d), and from the Chinese young dataset (e). The color bar represents the t‐value of conjunction analysis. The right panels represent the volume ratio of the identified SN in the left (orange) and right (blue) hemisphere, respectively. Abbreviations: dACC, dorsal anterior cingulate cortex; FDR, false discovery rate; FIC, frontoinsular cortex; rfMRI, resting‐state functional magnetic resonance imaging; HCP, human connectome project; SN, salience network

Figure 3

Examples of FIC‐dACC structure connectivity. Three examples of the FIC‐dACC fiber bundles are present: (a) left–right balanced; (b) right‐dominant, and (c) right‐only. All of these examples were obtained from the HCP datasets with generalized q‐sampling imaging reconstruction and deterministic streamline fiber tracking. Abbreviations: dACC, dorsal anterior cingulate cortex; FIC, frontoinsular cortex; HCP, human connectome project

Figure 4

Quantification of the FIC‐dACC structural connectivity in each hemisphere. The fiber numbers of each individual (right panel) are shown and their averages (left panel) are calculated based on: (a) HCP dataset using original FIC and dACC seeds deriving from the conjunction analysis; (b) HCP dataset using the eroded seeds to ensure the cluster sizes between the left and right side are comparable; (c) Chinese dataset using original seeds from the conjunction analysis; and (d) Chinese dataset using the eroded seeds. Abbreviations: dACC, dorsal anterior cingulate cortex; FIC, frontoinsular cortex; HCP, human connectome project

Figure 5

Group probability map of the FIC‐dACC fiber trajectory. The group probability map is created by averaging the individual fiber trajectory of the 100 HCP subjects. The color bar represents the probability value along the FIC‐dACC fiber trajectory. Abbreviations: dACC, dorsal anterior cingulate cortex; FIC, frontoinsular cortex; HCP, human connectome project

Figure 6

The laterality index of the FIC‐dACC structural connectivity. The structural laterality index of the HCP and Chinese dataset are calculated based on fiber tracking using: (a) the original FIC and dACC seeds deriving from the conjunction analysis and (b) the eroded seeds to ensure the cluster sizes between the left and right side are comparable. Abbreviations: dACC, dorsal anterior cingulate cortex; FIC, frontoinsular cortex; HCP, human connectome project

Figure 7

The laterality index of the FIC‐dACC functional connectivity. The functional laterality index of the HCP and Chinese dataset are calculated based on the functional connectivity using: (a) the original FIC and dACC seeds deriving from the conjunction analysis and (b) the eroded seeds to ensure the cluster sizes between the left and right side are comparable. HCP 1–4 represents each of the four runs of the HCP datasets, respectively. Abbreviations: dACC, dorsal anterior cingulate cortex; FIC, frontoinsular cortex; HCP, human connectome project

Figure 8

The association between aging and FA of right FIC‐dACC structural connectivity. Partial correlation analysis demonstrated a significant negative association between age and FA of the right FIC‐dACC (p < .003). Abbreviations: dACC, dorsal anterior cingulate cortex; FA, fractional anisotropy; FIC, frontoinsular cortex [Color figure can be viewed at http://wileyonlinelibrary.com]