The metastable brain associated with autistic-like traits of typically developing individuals.

Takumi Sase,Keiichi Kitajo,Boris S Gutkin

doi:10.1371/journal.pcbi.1008929

Abstract

Metastability in the brain is thought to be a mechanism involved in the dynamic organization of cognitive and behavioral functions across multiple spatiotemporal scales. However, it is not clear how such organization is realized in underlying neural oscillations in a high-dimensional state space. It was shown that macroscopic oscillations often form phase-phase coupling (PPC) and phase-amplitude coupling (PAC), which result in synchronization and amplitude modulation, respectively, even without external stimuli. These oscillations can also make spontaneous transitions across synchronous states at rest. Using resting-state electroencephalographic signals and the autism-spectrum quotient scores acquired from healthy humans, we show experimental evidence that the PAC combined with PPC allows amplitude modulation to be transient, and that the metastable dynamics with this transient modulation is associated with autistic-like traits. In individuals with a longer attention span, such dynamics tended to show fewer transitions between states by forming delta-alpha PAC. We identified these states as two-dimensional metastable states that could share consistent patterns across individuals. Our findings suggest that the human brain dynamically organizes inter-individual differences in a hierarchy of macroscopic oscillations with multiple timescales by utilizing metastability.

Highlights

The human brain can spontaneously yield transition dynamics across oscillatory states and organize a variety of events in a hierarchy of oscillations
The dynamic organization of underlying neural oscillations has been a fundamental topic in neuroscience research
Macroscopic oscillations often form phase-phase coupling and phase-amplitude coupling (PAC) that result in synchronization and amplitude modulation, respectively, and can make spontaneous transitions across synchronous states at rest

Summary

Introduction

The human brain can spontaneously yield transition dynamics across oscillatory states and organize a variety of events in a hierarchy of oscillations. Such spontaneous dynamics, at rest, have been intensively observed and analyzed over many years, and attempts to model them have been made using dynamical systems theory, to achieve a better prediction of brain activity [1,2,3,4,5]. There is a lack of direct evidence that resting-state brain dynamics can originate from the underlying nonlinear states, and little is known about the kind of states that may have functional roles in the dynamic organization of spontaneous activity in a way utilizing oscillatory hierarchy. The peak frequency of neural activity shows either a higher or lower value depending on brain function [6] and cognitive and behavioral performance [7]; for example, alpha-band activity can be enhanced or suppressed by attention, and its peak frequency can vary with age [7]

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