Inter-subject Functional Correlation Reveal a Hierarchical Organization of Extrinsic and Intrinsic Systems in the Brain

Yudan Ren,Lei Guo,Vinh Thai Nguyen,Christine Cong Guo

doi:10.1038/s41598-017-11324-8

Abstract

The brain is constantly monitoring and integrating both cues from the external world and signals generated intrinsically. These extrinsically and intrinsically-driven neural processes are thought to engage anatomically distinct regions, which are thought to constitute the extrinsic and intrinsic systems of the brain. While the specialization of extrinsic and intrinsic system is evident in primary and secondary sensory cortices, a systematic mapping of the whole brain remains elusive. Here, we characterized the extrinsic and intrinsic functional activities in the brain during naturalistic movie-viewing. Using a novel inter-subject functional correlation (ISFC) analysis, we found that the strength of ISFC shifts along the hierarchical organization of the brain. Primary sensory cortices appear to have strong inter-subject functional correlation, consistent with their role in processing exogenous information, while heteromodal regions that attend to endogenous processes have low inter-subject functional correlation. Those brain systems with higher intrinsic tendency show greater inter-individual variability, likely reflecting the aspects of brain connectivity architecture unique to individuals. Our study presents a novel framework for dissecting extrinsically- and intrinsically-driven processes, as well as examining individual differences in brain function during naturalistic stimulation.

Highlights

Psychologists and philosophers have long postulated that exogenous and endogenous processes are supported by different brain systems, namely the extrinsic and intrinsic systems, respectively[1,2,3,4]
We here adopted a novel approach to assess the network characteristics that are primarily influenced by external stimuli (See Methods for detail). This approach first computed inter-subject functional correlation (ISFC) – high scores indicate connections that are consistent across subjects and time-locked to the external stimuli[32]
The distribution of inter-subject degree centrality resembles that of Inter-subject correlation (ISC) map, that is, brain regions with high ISC tend to show a high level of inter-subject degree centrality (Fig. 2B, Supplementary Fig. S10)

Summary

Introduction

Psychologists and philosophers have long postulated that exogenous and endogenous processes are supported by different brain systems, namely the extrinsic and intrinsic systems, respectively[1,2,3,4]. A major discovery from the resting state literature is the characterization of large-scale, distributed connectivity networks in the absence of external stimuli[10, 11]. These resting state networks were regarded as an intrinsic or endogenous system of the brain, referred to as the default mode network[12,13,14,15,16]. Reactivity to external stimuli, does not necessarily reflect an involvement with endogenous processes This binary division based on a statistical threshold might oversimplify the organization of intrinsic and extrinsic systems in the brain. A quantitative metric that could reflect both extrinsically- and intrinsically-oriented processes is needed

Methods

Results

Conclusion