Brain states recur across diverse narrative contexts during longitudinal viewing

Abstract

What does the brain do during the continuous, varied experience of watching a story unfold? One account holds that the brain traverses a finite repertoire of recurring states, but whether that repertoire is a stable property of the individual or is reshaped by each new experience has not been tested across diverse naturalistic content within the same person. We characterized the dynamic brain-state repertoire in six individuals who watched the television series Friends across its six seasons during fMRI (up to [~]146 episodes, [~]54 hours per person). For each individual we fit a sticky hierarchical Dirichlet process hidden Markov model across all episodes, discovering brain states (recurring whole-brain activity patterns with characteristic coupling) without pre-specifying their number. Each individuals brain visited roughly forty-five states arrayed along a continuous recurrence gradient, from states active in nearly every episode to episode-specific ones, with no sharp division between them. The repertoire was heterogeneous in why its states recurred: a minority locked to scan-run structure, the majority remaining eligible for content. Transitions were organized by the functional-connectivity similarity between states (per-individual Spearman {rho} = 0.33-0.55) and, in most individuals, respected resting-state network boundaries. Episode content was associated with which states the brain occupied moment to moment. The recurrence ordering discovered in Friends transferred to state occupancy during other social-narrative films (five of six individuals) and attenuated as stimuli departed from that class, weakening for visual-only reading and audio-only listening. Across diverse narrative experience, the dynamic repertoire is a property of the individual: content varies which states are visited and when, not which states exist.