Precuneus shares intrinsic functional architecture in humans and monkeys

Abstract

Evidence from macaque monkey tracing studies suggests connectivity-based subdivisions within the precuneus, offering predictions for similar subdivisions in the human. Here we present functional connectivity analyses of this region using resting-state functional MRI data collected from both humans and macaque monkeys. Three distinct patterns of functional connectivity were demonstrated within the precuneus of both species, with each subdivision suggesting a discrete functional role: (i) the anterior precuneus, functionally connected with the superior parietal cortex, paracentral lobule, and motor cortex, suggesting a sensorimotor region; (ii) the central precuneus, functionally connected to the dorsolateral prefrontal, dorsomedial prefrontal, and multimodal lateral inferior parietal cortex, suggesting a cognitive/associative region; and (iii) the posterior precuneus, displaying functional connectivity with adjacent visual cortical regions. These functional connectivity patterns were differentiated from the more ventral networks associated with the posterior cingulate, which connected with limbic structures such as the medial temporal cortex, dorsal and ventromedial prefrontal regions, posterior lateral inferior parietal regions, and the lateral temporal cortex. Our findings are consistent with predictions from anatomical tracer studies in the monkey, and provide support that resting-state functional connectivity (RSFC) may in part reflect underlying anatomy. These subdivisions within the precuneus suggest that neuroimaging studies will benefit from treating this region as anatomically (and thus functionally) heterogeneous. Furthermore, the consistency between functional connectivity networks in monkeys and humans provides support for RSFC as a viable tool for addressing cross-species comparisons of functional neuroanatomy.

Fig. 1.

(Top) Schematic diagram illustrating the human PMC including the precuneus, the posterior cingulate cortex (area 23), the retrosplenial cortex in the posterior callosal sulcus (areas 29 and 30), and the transitional zone (area 31) that separates the precuneus from the cingulate cortex. The precuneus is located between the marginal ramus of the cingulate sulcus and the parieto-occipital fissure. (Bottom Left) The macaque monkey PMC with divisions primarily delineated from anatomical connectivity studies. (Bottom Right) Architectonic anatomical maps and their proposed subdivisions of the human precuneus.

Fig. 2.

Placement of 21 seed regions in monkeys (Left) and humans (Right). Descriptions of the seeds in relation to sulcal landmarks and average coordinates in the MNI152 space are provided in SI Materials and Methods and Table S1.

Fig. 3.

Four seed regions were selected that exemplified the markedly different patterns described in Results. (The results of voxelwise analyses for all seeds are given in SI Appendix, Figs. S1–S3, and statistical results for human seeds are given in Table S1.) The 4 specific seed regions presented here (left column) have been classified by the functional roles implied by their functional connectivity patterns, and the results are compared with anatomical connectivity findings from macaque monkeys after injection of tracers within a location comparable to the respective seed region.

Fig. 4.

Summary of functional connectivity patterns emerging from the 3 precuneus subdivisions and the posterior cingulate. At the bottom are select coronal slices, designated A–H to clarify characteristic delineations between PMC subdivisions.