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Neural mechanisms of action learning and action selection: from intent to habit

Final Report Summary - NEUROHABIT (Neural mechanisms of action learning and action selection: from intent to habit)

In every day life, we constantly have to select the appropriate actions to obtain specific outcomes. Actions can be selected based on their consequences, for example when we press an elevator button to get to the particular floor where we live. This goal-directed behaviour is crucial to face the ever-changing environment but demands an effortful control and monitoring of the response; one way to balance the need for flexibility and efficiency is through automatization of recurring decision processes as a habit. Habitual responses no longer need the evaluation of their consequences, and can be elicited by particular situations or stimuli, for example when we press the button for our home floor in a building that we are visiting for the first time. There is growing evidence that the neural circuits underlying intentional or goal-directed actions are different from those underlying habits; associative corticostriatal circuits have been implicated in goal-directed actions, and sensorimotor circuits in habit formation. Dopamine (DA) has been implicated in both voluntary actions and habits. However, DA neurons from the VTA and the SNc project to different cortical and striatal regions, and the specific role of VTA and SNc DA in goal-directed actions and habits has not been clarified. We propose to: 1) use cell-type and region specific genetic manipulations to test if phasic firing in VTA or SNc DA neurons is necessary for goal-directed actions or habits, respectively, 2) generate cell-type specific channelrodhopsin transgenic mice to test if phasic DA neuron firing in these areas is sufficient to produce goal-directed actions or habits, and 3) selectively manipulate striatal neurons modulated by VTA or SNc phasic DA to test if they are necessary for goal-directed actions or habits. The dissection of the molecular and circuit mechanisms underlying goal-directed and habitual responses will be critical to understand decision-making, and the origins of compulsive behaviour.
This ERC project has revealed that different dopaminergic and corticostriatal circuits are involved in intentional vs habitual actions. Furthermore, in contrast with the classical textbook view, it revealed that both direct and indirect the basal ganglia pathways are required for the initiation and execution of action. Finally, it revealed that plasticity in corticostriatal circuits is necessary for the selection of behavioural and neural patterns and their crystallization. These findings have important implications for understanding basal ganglia disorders.