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

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 except for a recent work. Here, using a novel brain-state-dependent neural stimulation system, we identified causal effects on percept dynamics in three PFC activities—right frontal eye fields, dorsolateral PFC (DLPFC), and inferior frontal cortex (IFC). The causality is behaviourally detectable only when we track brain state dynamics and modulate the PFC activity in brain-state-/state-history-dependent manners. The behavioural effects are underpinned by transient neural changes in the brain state dynamics, and such neural effects are quantitatively explainable by structural transformations of the hypothetical energy landscapes. Moreover, these findings indicate distinct functions of the three PFC areas: in particular, the DLPFC enhances the integration of two PFC-active brain states, whereas IFC promotes the functional segregation 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.
eLife digest A cube that seems to shift its spatial arrangement as you keep looking; the elegant silhouette of a pirouetting dancer, which starts to spin in the opposite direction the more you stare at it; an illustration that shows two profiles – or is it a vase? These optical illusions are examples of bistable visual perception. Beyond their entertaining aspect, they provide a way for scientists to explore the dynamics of human consciousness, and the neural regions involved in this process. Some studies show that bistable visual perception is associated with the activation of the prefrontal cortex, a brain area involved in complex cognitive processes. However, it is unclear whether this region is required for the illusions to emerge. Some research has showed that even if sections of the prefrontal cortex are temporally deactivated, participants can still experience the illusions. Instead, Takamitsu Watanabe proposes that bistable visual perception is a process tied to dynamic brain states – that is, that distinct regions of the prefontal cortex are required for this fluctuating visual awareness, depending on the state of the whole brain. Such causal link cannot be observed if brain activity is not tracked closely. To investigate this, the brain states of 65 participants were recorded as individuals were experiencing the optical illusions; the activity of their various brain regions could therefore be mapped, and then areas of the prefrontal cortex could precisely be inhibited at the right time using transcranial magnetic stimulation. This revealed that, indeed, prefrontal cortex regions were necessary for bistable visual perception, but not in a simple way. Instead, which ones were required and when depended on activity dynamics taking place in the whole brain. Overall, these results indicate that monitoring brain states is necessary to better understand – and ultimately, control – the neural pathways underlying perception and behaviour.