The metastable human brain associated with autistic-like traits

Abstract

Metastability in the brain is thought to be a mechanism involved in 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. Author SummaryThe human brain organizes cognitive and behavioral functions dynamically. For decades, the dynamic organization of underlying neural oscillations has been a fundamental topic in neuroscience research. Even without external stimuli, 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. Using resting-state electroencephalography signals acquired from healthy humans, we show evidence that these two neural couplings enable amplitude modulation to be transient, and that this transient modulation can be viewed as the transition among oscillatory states with different PAC strengths. We also demonstrate that such transition dynamics are associated with the ability to maintain attention to detail and to switch attention, as measured by autism-spectrum quotient scores. These individual dynamics were visualized as a trajectory among states with attracting tendencies, and involved consistent brain states across individuals. Our findings have significant implications for unraveling variability in the individual brains showing typical and atypical development.