Energy Landscape Analysis Reveals Thalamic Modulation of Brain State Transitions During Movie Watching

Abstract

Understanding how large-scale brain networks dynamically coordinate during complex, real-world experiences remains a crucial topic in contemporary neuroscience. Leveraging naturalistic paradigm, this study employed energy landscape modeling to characterize the temporal dynamics of brain state transitions and their functional significance. Using the Sherlock fMRI dataset, we identified two dominant brain states: a perception- and attention-oriented state, and an introspective, integrative state, each associated with distinct canonical brain networks. State transitions were differentially associated with the recruitment of these networks and manifested as either the "easy" or "hard" route, depending on the energy required for the transition. Notably, we demonstrated that the probability of specific state transitions robustly predicted inter-subject correlation within three clusters: subcortical-rich, salience/attention-rich, and DMN-rich regions. This indicates that flexible reorganization of cortical networks underlies shared neural engagement during ecologically valid experiences. Critically, the thalamus emerged as a central modulator, displaying activity changes and dynamic nucleus-specific thalamocortical connectivity changes tied to distinct transition profiles. Together, our findings shed light on the energetic and network mechanisms that orchestrate brain dynamics during naturalistic cognition and underscore the pivotal role of cortico-thalamo-cortical circuits in governing flexible, collective neural responses to richly structured real-life stimuli.