Flexible Sensory-Motor Mapping Rules Manifest in Correlated Variability of Stimulus and Action Codes Across the Brain

Abstract

Humans and non-human primates can acquire, and rapidly switch between, arbitrary rules that govern the mapping from sensation to action. It has remained unknown if and how the brain configures large-scale sensory-motor circuits to establish such flexible information flow. Here, we developed an approach that elucidates the dynamic configuration of task-specific sensory-motor circuits in humans. Participants switched between arbitrary mapping rules for reporting visual orientation judgments during fMRI. Rule switches were either signaled explicitly or inferred by the participants from ambiguous cues, and we used behavioral modeling to reconstruct the time course of their belief about the active rule. In both contexts, patterns of correlations between ongoing fluctuations in feature-specific activity across visual and action-related brain regions tracked participants' belief about the active rule. These rule-specific, intrinsic correlation patterns broke down on error trials and predicted individuals' model-inferred internal noise. Our findings indicate that internal beliefs about task state are instantiated in specific large-scale patterns of selective, correlated neural variability.