Adaptation to changing environments involves the appropriate extraction of environmental information to achieve a behavioral goal. It remains unclear how behavioral flexibility is guided under situations where the relevant behavior is ambiguous. Using functional brain mapping of machine learning decoders and directional functional connectivity, we show that brain-wide reversible neural signaling underpins task encoding and behavioral flexibility in ambiguously changing environments. When relevant behavior is cued ambiguously during behavioral shifting, neural coding is attenuated in distributed cortical regions, but top-down signals from the prefrontal cortex complement the coding. When behavioral shifting is cued more explicitly, modality-specialized occipitotemporal regions implement distinct neural coding about relevant behavior, and bottom-up signals from the occipitotemporal region to the prefrontal cortex supplement the behavioral shift. These results suggest that our adaptation to an ever-changing world is orchestrated by the alternation of top-down and bottom-up signaling in the fronto-occipitotemporal circuit depending on the availability of environmental information.

Flexible adaptation to changing environments is one of the representative executive control functions, and requires appropriate extraction of environmental information to achieve a behavioral goal. It still remains unclear however, how the behavioral flexibility is guided under situations where the relevant behavior is ambiguous. Using functional brain mapping of machine-learning decoders and directional functional connectivity, we show that brain-wide reversible neural signaling underpins behavioral flexibility in ambiguously changing environments. When relevant behavior is cued ambiguously during behavioral shifting, neural coding of the behavior is attenuated in distributed cortical regions, but top-down signals from the prefrontal cortex complements the coding. On the other hand, when shifting to the alternative behavior is cued more explicitly, modality-specialized occipitotemporal regions implement distinct neural coding about the relevant behavior, and bottom-up signals from the occipitotemporal region to the prefrontal cortex supplements the behavioral shift. These results suggest that our adaptation to an ever-changing world is orchestrated by the alternation of top-down and bottom-up signaling in the fronto-occipitotemporal circuit depending on the availability of environmental evidences.Significance statementHow does the brain work when appropriate behavior is unclear? We found that when proper behavior was cued ambiguously, the prefrontal cortex signaled toward occipitotemporal regions. Functional brain mapping based on deep neural network revealed that neural coding of appropriate task was diminished in the occipitotemporal regions, which was complemented by the prefrontal signal. When the proper behavior was cued unambiguously, the occipitotemporal regions signaled the prefrontal cortex, which increased efficiency of the flexibility. Our results suggest that dynamic reversal of prefrontal-occipitotemporal signaling optimizes the behavioral flexibility depending on the perceptual ambiguity of the external world.