Revealing abrupt transitions from goal-directed to habitual behavior

A fundamental tenet of animal behavior is that decision-making involves multiple ‘controllers.’ Initially, behavior is goal-directed, driven by desired outcomes, shifting later to habitual control, where cues trigger actions independent of the motivational state. Clark Hull’s question from 1943 still resonates today: “Is this transition [to habit] abrupt, or is it gradual and progressive?” Despite a century-long belief in gradual transitions, this question remains unanswered as current methods cannot disambiguate goal-directed versus habitual control in real time. Here, we introduce a novel ‘volitional engagement’ approach, motivating animals by palatability rather than biological need. Providing less palatable water in the home cage reduced motivation to ‘work’ for plain water in an auditory discrimination task compared to water-restricted animals. Using quantitative behavior and computational modeling, we found that palatability-driven animals learned to discriminate as quickly as water-restricted animals but exhibited state-like fluctuations when responding to the reward-predicting cue-reflecting goal-directed behavior. After thousands of trials, these fluctuations spontaneously and abruptly ceased, with animals always responding to the reward-predicting cue. In line with habitual control, post- transition behavior displayed motor automaticity, decreased error sensitivity (assessed via pupillary responses), and insensitivity to sensory-specific outcome devaluation. Bilateral lesions of the habit-related dorsolateral striatum (DLS) blocked transitions to habitual behavior. Finally, we used bilateral fiber photometry in the putative controllers of goal-directed (dorsomedial striatum, DMS) and habitual (DLS) behavior to monitor the evolution of neural activity across learning. Both the DMS and DLS exhibited learning- related signatures in cue, lick, and outcome-related signaling at similar timescales in parallel. Immediately after transitioning to habitual behavior, outcome-related signaling was suppressed in the DLS and, to a lesser extent, in the DMS, while cue-evoked responses further sharpened. This abrupt shift (reduction in outcome signaling and sharpening of cue-evoked responses) suggests that sensory cues rather than outcomes drive habitual responding. Our results demonstrate that both controllers (DMS and DLS) exhibit learning-related plasticity in parallel but that the behavioral manifestation of habits emerges spontaneously and abruptly in a DLS-dependent manner, suggesting the involvement of a higher-level process that arbitrates between the two.
 

Sharlen Moore est invitée par Robin Magnard.