Region- and stage-specific cortical plasticity shapes the multifaceted process of habit formation

Habits are crucial for shaping our normal and pathological behaviors. They emerge through a transition in decision-making strategy, from flexible adaptation to current demands (goal-directed behavior) to automatic repeats of previous behaviors (habitual behavior). This transition of decision-making strategy induces changes in an underlying cognitive process for selecting an action while superficially maintaining the execution of the selected action. However, the neurocircuit mechanisms supporting these changes remain unexplored. By developing a behavioral paradigm capable of inducing this transition within a defined time window, we performed a longitudinal analysis of the neuronal circuits involved in this process usingex vivoelectrophysiology, optogenetic erasure of synaptic plasticity andin vivoCa²⁺-imaging. We found that the decision-making strategy and action execution are orthogonally controlled by plasticity in distinct cortical pathways. Erasure of these changes independently alter the decision-making strategy or the action execution without influencing each other, supporting a dichotomous circuit mechanism. This study underscores the critical role of pathway-specific cortical plasticity in regulating the multifaceted process shaping habitual behavior, offering valuable insights into the pathological mechanisms of maladaptive habits, such as compulsive disorders.