Interindividual Brain and Behavior Differences in Adaptation to Unexpected Uncertainty

SIMPLE SUMMARY: To adapt to a new environment, people must choose between using strategies that previously produced the expected effect in a similar context and trying new strategies with no certainty of achieving the expected effect. This is known as the exploration/exploitation trade-off. Its underlying brain mechanisms and factors accounting for interindividual differences have been overlooked. Resting-state functional connectivity highlights the synchronicity of different brain regions at rest, i.e., basal or intrinsic connectivity. Here, we investigated the evolution of this synchronicity before/after a task involving environmental uncertainty. To study the trade-off, we introduced uncertainty and cheated participants by introducing false feedbacks during an associative learning task. We examined the associations among the participants’ behaviors, changes in the brain intrinsic functional connectivity, and psychological factors. The sensitivity to uncertainty was used to create two groups. The groups displayed different patterns of evolution of regional connectivity from before to after the task. We also found a trend whereby higher scores of anxiety and greater propensity to doubt about actions were positively linked to these patterns. These results provide additional arguments in favor of short-term plasticity in basal brain connectivity and clues about the interindividual factors influencing neural and behavioral adaptation. ABSTRACT: To adapt to a new environment, individuals must alternate between exploiting previously learned “action–consequence” combinations and exploring new actions for which the consequences are unknown: they face an exploration/exploitation trade-off. The neural substrates of these behaviors and the factors that may relate to the interindividual variability in their expression remain overlooked, in particular when considering neural connectivity patterns. Here, to trigger environmental uncertainty, false feedbacks were introduced in the second phase of an associative learning task. Indices reflecting exploitation and cost of uncertainty were computed. Changes in the intrinsic connectivity were determined using resting-state functional connectivity (rFC) analyses before and after performing the “cheated” phase of the task in the MRI. We explored their links with behavioral and psychological factors. Dispersion in the participants’ cost of uncertainty was used to categorize two groups. These groups showed different patterns of rFC changes. Moreover, in the overall sample, exploitation was correlated with rFC changes between (1) the anterior cingulate cortex and the cerebellum region 3, and (2) the left frontal inferior gyrus (orbital part) and the right frontal inferior gyrus (triangular part). Anxiety and doubt about action propensity were weakly correlated with some rFC changes. These results demonstrate that the exploration/exploitation trade-off involves the modulation of cortico-cerebellar intrinsic connectivity.