Revealing abrupt transitions from goal-directed to habitual behavior

Abstract

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?" 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. Offering less palatable water in the home cage reduced motivation to 'work' for plain water in an auditory discrimination task when 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. 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 striatum 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.