Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans

Dazhi Yin,Zheng Wang,Zhiwei Wang,Zhao Zhang,Danchao Cai,Kristina Zeljic,Yingwei Wang,Qian Lv

doi:10.3389/fnins.2019.00174

Abstract

Emerging neuroimaging studies emphasize the dynamic organization of spontaneous brain activity in both human and non-human primates, even under anesthesia. In a recent study, we were able to characterize the heterogeneous architecture of intrinsic functional flexibility in the awake, resting human brain using time-resolved analysis and a probabilistic model. However, it is unknown whether this organizational principle is preserved in the anesthetized monkey brain, and how anesthesia affects dynamic and static measurements of spontaneous brain activity. To investigate these issues, we collected resting-state functional magnetic resonance imaging (fMRI) datasets from 178 awake humans and 11 anesthetized monkeys (all healthy). Our recently established method, a complexity measurement (i.e., Shannon entropy) of dynamic functional connectivity patterns of each brain region, was used to map the intrinsic functional flexibility across the cerebral cortex. To further explore the potential effects of anesthesia, we performed time series analysis and correlation analysis between dynamic and static measurements within awake human and anesthetized monkey brains, respectively. We observed a heterogeneous profile of intrinsic functional flexibility in the anesthetized monkey brain, which showed some similarities to that of awake humans (r = 0.30, p = 0.007). However, we found that brain activity in anesthetized monkeys generally shifted toward random fluctuations. Moreover, there is a negative correlation between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength in anesthetized monkeys, but not in awake humans. Our findings indicate that the heterogeneous architecture of intrinsic functional flexibility across cortex probably reflects an evolutionarily conserved aspect of functional brain organization, which persists across levels of cognitive processing (states of consciousness). The coupling between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength may serve as a potential signature of anesthesia. This study not only offers fresh insight into the evolution of brain functional architecture, but also advances our understanding of the dynamics of spontaneous brain activity.

Highlights

A fundamental goal of comparative neuroscience is to determine conservation and evolution-driven changes in functional brain organization between species
Cross-species comparison suggests that the heterogeneous brain map of intrinsic functional flexibility persists during primate evolution and transcends levels of consciousness, remaining present under anesthesia
The coupling between dynamic and static measurements can provide a potential signature of loss of consciousness due to anesthesia

Summary

Introduction

A fundamental goal of comparative neuroscience is to determine conservation and evolution-driven changes in functional brain organization between species. Functional magnetic resonance imaging (fMRI), a non-invasive technique, has been utilized to identify functionally homologous or unique areas across primate species based on specific experimental tasks (Nakahara et al, 2002; Vanduffel et al, 2002; Wang et al, 2015). Resting-state functional connectivity (FC) is typically used to index the interregional coherence in spontaneous low-frequency fluctuations (e.g., 0.01∼0.1 Hz) of BOLD signals (Biswal et al, 1995; Fox and Raichle, 2007) Through this approach, many functional brain networks such as the sensorimotor and default mode networks have been identified in both human and non-human primates (Vincent et al, 2007; Margulies et al, 2009; Hutchison et al, 2011; Hutchison and Everling, 2012; Mantini et al, 2013; MirandaDominguez et al, 2014; Neubert et al, 2014). The origins and functional significance of resting-state FC patterns remain to be further understood

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