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 crossspecies comparisons of functional neuroanatomy.brain connectivity ͉ functional MRI ͉ posteromedial cortex ͉ resting state C ompared with the lateral surface of the parietal lobe, the functional organization of the medial parietal wall has been relatively neglected. Often referred to as the precuneus, this region has been implicated in high-level cognitive functions, including episodic memory, self-related processing, and aspects of consciousness (1-3). Located in the dorsal portion of the posteromedial cortex (PMC) between the somatosensory and visual cortex, superior to the posterior cingulate and retrosplenial cortex, the precuneus is well situated to play a multimodal, integrative functional role (Fig. 1, Top). Its implication in many higher cognitive functions strongly suggests the presence of functional subdivisions (2, 4), although the neuroimaging literature traditionally has treated it as a homogeneous structure and typically has failed to distinguish between the precuneus and the neighboring posterior cingulate/ retrosplenial cortex.The question of how best to subdivide the human precuneus has been a source of controversy for almost a century. The cytoarchitectonic map of Brodmann (5, 6) as it appears in the atlas of Talairach and T...

Network structure and dynamics of the mental workspace

“…Margulies et al (20) reported that the precuneus in humans is functionally connected to the lateral frontal, posterior parietal, and occipital cortices. The precuneus is one of the most connected regions of the cortex, suggesting that it may serve as a hub in several cortical networks.…”

Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited

“…Granted, the use of animal models is somewhat limited because of interspecies differences in neuroanatomy (45,46). However, given the similarities in the connectivity profile between the monkey and human brain (47,48), macaque models will continue to serve as an indispensable tool for explicating general organizational principles of brain networks such as characterization of the directional transitions that axons make when entering or exiting gray matter (35,49,50). Insights from such studies may help improve the accuracy of tractography techniques.…”

Toward discovery science of human brain function

“…Recent R-fMRI studies have identified putative biomarkers of neuropsychiatric illness (12,(15)(16)(17)(18), provided insight into the development of functional networks in the maturing and aging brain (19)(20)(21)(22), demonstrated a shared intrinsic functional architecture (23) between humans and nonhuman primates (24,25), and delineated the effects of sleep (26), anesthesia (27), and pharmacologic agents on R-fMRI measures (28,29). Given the many sources of variability inherent in fMRI, the remaining challenge is to demonstrate the feasibility and utility of adopting a high-throughput model for RfMRI, commensurate with the scale used by human genetics studies to have the power to detect both single gene and combinatorial genetic and environmental effects on complex phenotypes.…”