Human cognition is influenced not only by external task demands but also latent mental processes and brain states that change over time. Here, we use novel Bayesian switching dynamical systems algorithm to identify hidden brain states and determine that these states are only weakly aligned with external task conditions. We compute state transition probabilities and demonstrate how dynamic transitions between hidden states allow flexible reconfiguration of functional brain circuits. Crucially, we identify latent transient brain states and dynamic functional circuits that are optimal for cognition and show that failure to engage these states in a timely manner is associated with poorer task performance and weaker decision-making dynamics. We replicate findings in a large sample (N = 122) and reveal a robust link between cognition and flexible latent brain state dynamics. Our study demonstrates the power of switching dynamical systems models for investigating hidden dynamic brain states and functional interactions underlying human cognition.

Little is currently known about dynamic brain networks involved in high-level cognition and their ontological basis. Here we develop a novel Variational Bayesian Hidden Markov Model (VB-HMM) to investigate dynamic temporal properties of interactions between salience (SN), default mode (DMN), and central executive (CEN) networks—three brain systems that play a critical role in human cognition. In contrast to conventional models, VB-HMM revealed multiple short-lived states characterized by rapid switching and transient connectivity between SN, CEN, and DMN. Furthermore, the three “static” networks occurred in a segregated state only intermittently. Findings were replicated in two adult cohorts from the Human Connectome Project. VB-HMM further revealed immature dynamic interactions between SN, CEN, and DMN in children, characterized by higher mean lifetimes in individual states, reduced switching probability between states and less differentiated connectivity across states. Our computational techniques provide new insights into human brain network dynamics and its maturation with development.

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A key question in decision making is how humans arbitrate between competing learning and memory systems to maximize reward. We address this question by probing the balance between the effects, on choice, of incremental trial-and-error learning versus episodic memories of individual events. Although a rich literature has studied incremental learning in isolation, the role of episodic memory in decision making has only recently drawn focus, and little research disentangles their separate contributions. We hypothesized that the brain arbitrates rationally between these two systems, relying on each in circumstances to which it is most suited, as indicated by uncertainty. We tested this hypothesis by directly contrasting contributions of episodic and incremental influence to decisions, while manipulating the relative uncertainty of incremental learning using a well-established manipulation of reward volatility. Across two large, independent samples of young adults, participants traded these influences off rationally, depending more on episodic information when incremental summaries were more uncertain. These results support the proposal that the brain optimizes the balance between different forms of learning and memory according to their relative uncertainties and elucidate the circumstances under which episodic memory informs decisions.