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.

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In real life, humans make decisions by taking into account multiple independent factors, such as delay and probability. Cognitive psychology suggests that cognitive control mechanisms play a key role when facing such complex task conditions. However, in value-based decision-making, it still remains unclear to what extent cognitive control mechanisms become essential when the task condition is complex. In this study, we investigated decision-making behaviors and underlying neural mechanisms using a multifactor gambling task where participants simultaneously considered probability and delay. Decision-making behavior in the multifactor task was modulated by both probability and delay. The behavioral effect of probability was stronger than delay, consistent with previous studies. Furthermore, in a subset of conditions that recruited fronto-parietal activations, reaction times were paradoxically elongated despite lower probabilistic uncertainty. Notably, such a reaction time elongation did not occur in control tasks involving single factors. Meta-analysis of brain activations suggested an association between the paradoxical increase of reaction time and strategy switching. Together, these results suggest a novel aspect of complex value-based decision-makings that is strongly influenced by fronto-parietal cognitive control.Highlights•A value-based decision task with concurrent delay and probabilistic uncertainty•Stronger behavioral effect of probability than delay•Paradoxically long reaction time despite low probabilistic uncertainty•The task activated fronto-parietal cognitive control network•Reaction time elongation coincided with activation similar to strategy switching