Causal roles of prefrontal cortex during spontaneous perceptual switching are determined by brain state dynamics

Abstract

The prefrontal cortex (PFC) is thought to orchestrate cognitive dynamics. However, in tests of bistable visual perception, no direct evidence supporting such presumable causal roles of the PFC has been reported. Here, using a novel brain-state-dependent neural stimulation system, we found that three PFC regions—right frontal eye fields and anterior/posterior dorsolateral PFCs (a/pDLPFCs)—have causal effects on perceptual dynamics but the behavioural effects are detectable only when we modulated the PFC activity in brain-state-/state-history-dependent manners. Also, we revealed that the brain-dynamics-dependent behavioural causality is underpinned by transient changes in the brain state dynamics, and such neural changes are determined by structural transformations of hypothetical energy landscapes. Moreover, we identified different functions of the three PFC areas: in particular, we found that aDLPFC enhances the integration of the two PFC-active brain states, whereas pDLPFC promotes the diversity between them. This work resolves the controversy over the PFC roles in spontaneous perceptual switching and underlines brain state dynamics in fine investigations of brain-behaviour causality. Impact statement Prefrontal causal roles are changing during bistable visual perception, which was determined by large-scale brain state dynamics and attributable to hypothetical energy landscapes that underpin the brain state dynamics.