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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 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.

SUBMITTER: Watanabe T

PROVIDER: S-EPMC8631941 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAnxiety and stress reactivity are risk factors for the development of affective disorders. However, the behavioral and neurocircuit mechanisms that potentiate maladaptive emotion regulation are poorly understood. Neuroimaging studies have implicated the amygdala and dorsolateral prefrontal cortex (DLPFC) in emotion regulation, but how anxiety and stress alter their context-specific causal circuit interactions is not known. Here, we use computational modeling to inform affective pathophysiology, etiology, and neurocircuit targets for early intervention.MethodsForty-five children (10-11 years of age; 25 boys) reappraised aversive stimuli during functional magnetic resonance imaging scanning. Clinical measures of anxiety and stress were acquired for each child. Drift-diffusion modeling of behavioral data and causal circuit analysis of functional magnetic resonance imaging data, with a National Institute of Mental Health Research Domain Criteria approach, were used to characterize latent behavioral and neurocircuit decision-making dynamics driving emotion regulation.ResultsChildren successfully reappraised negative responses to aversive stimuli. Drift-diffusion modeling revealed that emotion regulation was characterized by increased initial bias toward positive reactivity during viewing of aversive stimuli and increased drift rate, which captured evidence accumulation during emotion evaluation. Crucially, anxiety and stress reactivity impaired latent behavioral dynamics associated with reappraisal and decision making. Anxiety and stress increased dynamic casual influences from the right amygdala to DLPFC. In contrast, DLPFC, but not amygdala, reactivity was correlated with evidence accumulation and decision making during emotion reappraisal.ConclusionsOur findings provide new insights into how anxiety and stress in children impact decision making and amygdala-DLPFC signaling during emotion regulation, and uncover latent behavioral and neurocircuit mechanisms of early risk for psychopathology.

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

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