Bringing language to dynamic brain states: the default network dominates neural responses to evolving movie stories

Abstract

Naturalistic neuroscience opened the door to new insights into neural circuits that serve real-world dynamic perception. Such studies have often neglected the rich texture of the movie narrative itself, but semantic content can be used to contextualize the induced neural responses. Here, we translated natural language processing tools from machine learning to characterize brain states estimated from hidden Markov models. Our analytical strategy allowed pitting shallow unimodal against the deep associative brain network layers in explaining how semantic content of the movie links to observed neural activity. Pooling information across >53,000 brain image time points watching Forrest Gump, we could show that distinct dynamic brain states capture unique semantic facets along the unfolding movie narrative. The spatiotemporal dynamics of brain states explicitly captured subject-level responses throughout the brain network hierarchy. Across all analyses, the default network was most intimately linked to semantic information integration, and this neural system switched online for longest durations during movie watching. Further, we identified and described two mechanisms of how the default network liaises dynamically with microanatomically defined subregion partners: the amygdala and the hippocampus. Our study thus unlocks the potential of natural language processing to explore neural processes in everyday life situations that engage key aspects of conscious awareness.