A ventral salience network in the macaque brain

Abstract

Successful navigation of the environment requires attending and responding efficiently to objects and conspecifics with the potential to benefit or harm (i.e., that have value). In humans, this function is subserved by a distributed large-scale neural network called the "salience network". We have recently demonstrated that there are two anatomically and functionally dissociable salience networks anchored in the dorsal and ventral portions of the human anterior insula (Touroutoglou et al., 2012). In this paper, we test the hypothesis that these two subnetworks exist in rhesus macaques (Macaca mulatta). We provide evidence that a homologous ventral salience network exists in macaques, but that the connectivity of the dorsal anterior insula in macaques is not sufficiently developed as a dorsal salience network. The evolutionary implications of these finding are considered.

Keywords: Intrinsic functional connectivity; Resting state fMRI; Rhesus macaques; Salience network.

Figure 1

Dissociable dorsal and ventral salience networks (right dorsal anterior insula seed, blue; right ventral anterior insula seed, red) in humans previously published by our laboratory (Touroutoglou et al., 2012). In B, C and D regions that preferentially correlate with the right dAI seed are shown in blue, regions that preferentially correlate with the right vAI seed are shown in red, and regions that correlate with both seeds are shown in purple. For display purposes, the binarized correlation maps, z(r)>0.2, were overlaid on (B) the inflated cortical surfaces of the left and right hemisphere (the fsaverage template in FreeSurfer) and (C and D) the 1mm MNI152 T1-standard template image in FSL (Adapted figure from Touroutoglou et al., 2012).

Figure 2

A ventral salience network in macaques. Regions that correlate with the right vAI seed (A) are shown in B, C, and D. Color bars displayed at the bottom of the figure indicate the z-values of correlated voxels. For display purposes, the correlation maps, z > 2, were overlaid on (B) the inflated cortical surfaces of the left and right hemisphere (the surface template in Caret 5.61) and (C and D) the F99 T1 template in neurological convention.

Figure 3

A dorsal anterior insula network in macaques. Regions that correlate with the right dAI seed (A) are shown in B, C, and D. Color bars displayed at the bottom of the figure indicate the z-values of correlated voxels. For display purposes, the correlation maps, z > 2, were overlaid on (B) the inflated cortical surfaces of the left and right hemisphere (the surface template in Caret 5.61) and (C and D) the F99 T1 template in neurological convention.

Figure 4

The distributions of within- and between-network connectivity for each pair. In (A) the central tendencies of the connectivity distributions between the right vAI seed and the vAI targets (red) and between the right dAI seed and the nodes of the ventral salience network (vAI targets) (yellow) are non-overlapping. Similarly, in (B) the central tendencies of the connectivity distributions between the right dAI seed and the nodes of the dorsal anterior insula network (dAI targets) (blue) and between the right vAI seed and the dAI targets (yellow) are not overlapping. ROI pairs that are present in both the right dorsal and right ventral salience networks are indicated in dark yellow.

Figure 5

The monkey ventral salience network and dorsal anterior insula network are represented over flattened cortical surfaces (threshold at z > 2) (Caret 5.61).

Figure 6

The monkey dorsal anterior insula network and ventral salience network are represented on the inflated cortical surfaces of the left and right hemisphere at z = 2 (the surface template in Caret 5.61). Regions that preferentially correlate with the right dAI seed are shown in blue, regions that preferentially correlate with the right vAI seed are shown in red, and regions that correlate with both seeds are shown in purple.

Figure 7

A homologous ventral salience network in the human and macaque. Folded cortical maps of the ventral salience network in humans (z > .2) and monkeys (z > 2) plotted over a representative cortical surface in lateral and medial views.