Spontaneous resting-state BOLD fluctuations reveal persistent domain-specific neural networks

Abstract

Resting-state functional connectivity MRI (rs-fcMRI) analyses have identified intrinsic neural networks supporting domain-general cognitive functions including language, attention, executive control and memory. The brain, however, also has a domain-specific organization, including regions that contribute to perceiving and knowing about others (the 'social' system) or manipulable objects designed to perform specific functions (the 'tool' system). These 'social' and 'tool' systems, however, might not constitute intrinsic neural networks per se, but rather only come online as needed to support retrieval of domain-specific information during social- or tool-related cognitive tasks. To address this issue, we functionally localized two regions in lateral temporal cortex activated when subjects perform social- and tool conceptual tasks. We then compared the strength of the correlations with these seed regions during rs-fcMRI. Here, we show that the 'social' and 'tool' neural networks are maintained even when subjects are not engaged in social- and tool-related information processing, and so constitute intrinsic domain-specific neural networks.

Fig. 1

Resting-state time course graphs illustrating correlated spontaneous BOLD fluctuations in an individual participant. The black lines in the graphs indicate the BOLD activity time courses across the 8-min resting-state scan at the left ventral premotor cortex (top), left pSTS (middle) and medial PFC (bottom). Black circles on the adjacent brain images indicate the locations of the target regions from which these signals were extracted. The locations of the seed voxels are not shown, although the images do show regions of differential connectivity in the left pMTG and right pSTS that are adjacent to the seed voxels. The colors on the brain maps indicate regions exhibiting differential functional connectivity to either the pMTG (cool colors) or pSTS (warm colors), with P < 0.005. The blue and orange lines in the graphs show the corresponding time courses at the left pMTG (‘tool’) and right pSTS (‘social’) seed voxels, respectively. The time course graphs are presented here for expository purposes to help the reader understand the analyses—namely that differential functional connectivity assesses whether a voxel is reliably more correlated with one seed region than another. The reader should note that the values in these specific graphs are overdetermined because we selected which voxels to plot by first testing for regions exhibiting differential functional connectivity to the pSTS/pMTG. The dashed lines across each of the individual brain images indicate the slice locations of the other brain images depicted in the figure. The y-axes on the graphs indicate percent signal change from signal baseline.

Fig. 2

Random effects group analyses demonstrating regions of differential functional connectivity to the left pMTG (‘tool’) and right pSTS (‘social’) seed voxels. Each pair of sagittal brain images shows remarkably similar regions of differential functional connectivity in the System Identification data set (left row, P < 0.05 corrected) and Replication data set (right row, P < 0.005, cluster size > 476 mm³). Cool colors indicate higher resting-state BOLD correlations with the left pMTG (‘tool’) seed voxel than the right pSTS (‘social) seed voxel, and warm colors indicate higher correlations with the right pSTS (‘social’) seed voxel. The exact locations of the seed voxels are not shown in these slices, although the images do show regions of differential connectivity in the left pMTG and right pSTS that are adjacent to the seed voxels.

Fig. 3

Evidence of differential fusiform functional connectivity in both data sets. The top coronal image shows a region of the fusiform gyrus that exhibited stronger functional connectivity to the right pSTS (‘social’) seed voxel than to the left pMTG (‘tool’) seed voxel (P < 0.05 corrected). Although differential functional connectivity was not observed in the fusiform at the threshold prescribed for the Replication data set analyses, it was present at a somewhat less stringent threshold, as illustrated in the bottom coronal image. The bottom image depicts regions of direct overlap between the two data sets within the fusiform gyrus. The red dotted line on the bottom image indicates the spatial extent of the fusiform cluster in the brain image at the top of the figure exhibiting differential functional connectivity to the ‘social’ seed in the System Identification data set.