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 motivational state. Clark Hull's question from 1943 still resonates today: "Is this transition abrupt, or is it gradual and progressive?"¹ Despite a century-long belief in gradual transitions, this question remains unanswered^2,3 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. Offering less palatable water in the home cage^4,5 reduced motivation to 'work' for plain water in an auditory discrimination task when compared to water-restricted animals. Using quantitative behavior and computational modeling⁶, 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. These fluctuations spontaneously and abruptly ceased after thousands of trials, with animals now 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 outcome devaluation. Bilateral lesions of the habit-related dorsolateral striatum⁷ blocked transitions to habitual behavior. Thus, 'volitional engagement' reveals spontaneous and abrupt transitions from goal-directed to habitual behavior, suggesting the involvement of a higher-level process that arbitrates between the two.