Mark E. Bouton’s research while affiliated with University of Vermont and other places

Habits are important in everyday life and are thought to be involved in several human behavioral pathologies, including addictions. Experiments with rats suggest that habit, as indexed by insensitivity of an instrumental response to separate devaluation of its outcome, develops with extended practice. Motivated behavior often involves a sequence or chain of behaviors (Rs), with each cued by a different discriminative stimulus (S). We therefore examined performance of a two-response discriminated heterogeneous behavior chain (R1–R2) in which R1 and R2 were occasioned by different Ss and were both required to earn a reinforcer. We further asked whether extended training decreases the sensitivity of R1 to the extinction of R2, which is known to decrease R1 and is analogous to an outcome devaluation effect. In Experiment 1 with rats, R1 was sensitive to extinction of R2 after moderate but not extended training, suggesting the development of habit. In Experiment 2, human participants learned three R1–R2 chains before one “R2” was extinguished. Extinction of R2 specifically decreased performance of the R1 that had been associated with it, but extended training did not reduce this effect. Based on findings in the nonhuman literature, Experiment 3 then had human participants learn only one R1–R2 chain before R2 was extinguished. Under these conditions, R1 became insensitive to extinction of R2 after extended training, consistent with the idea that habit can develop in a laboratory experiment with humans. The findings are discussed relative to difficulties demonstrating habits in humans.

This chapter reviews recent research from the author’s laboratory on habit and goal-direction in instrumental learning and then considers some of its implications for a general view of instrumental behavior and addiction. Results suggest that habit develops under conditions that allow the individual to pay less attention to its behavior, i.e., when the habit’s trigger cue reliably predicts the reward. Other results suggest that a behavior’s status as a habit is not necessarily fixed or permanent; several environmental manipulations can make a habitual behavior become goal-directed again. Habit is more context-specific than goal-direction. The perspective that emerges suggests that habit may have an important but perhaps more circumscribed role in instrumental behavior (and addiction) than might often be assumed. For example, drug seeking can appear adaptable and flexible because behaviors that are more distal to the goal (e.g., general search behaviors) may be goal-directed at the same time behaviors that are more proximal to the goal (e.g., actual drug-taking responses) are habitual. And individuals with substance use habits might not appear more habit-prone than controls when they are tested for habit in the context of the lab. These and other challenges that have been raised for the role of habit in addiction are discussed.

Taste aversion learning has sometimes been considered a specialized form of learning. In several other conditioning preparations, after a conditioned stimulus (CS) is conditioned and extinguished, reexposure to the unconditioned stimulus (US) by itself can reinstate the extinguished conditioned response. Reinstatement has been widely studied in fear and appetitive Pavlovian conditioning, as well as operant conditioning, but its status in taste aversion learning is more controversial. Six taste-aversion experiments with rats therefore sought to discover conditions that might encourage it there. The results often yielded little to no evidence of reinstatement, and we also found no evidence of concurrent recovery, a related phenomenon in which responding to a CS that has been conditioned and extinguished is restored if a second CS is separately conditioned. However, a key result was that reinstatement occurred when the conditioning procedure involved multiple closely spaced conditioning trials that could have allowed the animal to learn that a US presentation signaled or set the occasion for another trial with a US. Such a mechanism is precluded in many taste aversion experiments because they often use very few conditioning trials. Overall, the results suggest that taste aversion learning is experimentally unique, though not necessarily biologically or evolutionarily unique.

Previous work has demonstrated the importance of the prelimbic cortex (PL) in contextual control of operant behavior. However, the associated neural circuitry responsible for providing contextual information to the PL is not well understood. In Pavlovian fear conditioning the ventral hippocampus (vH) and its projection to the PL have been shown to be important in supporting the effects of context on learning. The present experiments used chemogenetic inhibition of the direct vH-PL projection or the vH to determine involvement in expression of context-specific operant behavior. Rats were injected with an inhibitory DREADD (hM4Di) or mCherry-only into the vH, and subsequently trained to perform a lever press response for a food pellet in a distinct context. The DREADD ligand clozapine-n-oxide (CNO) was then delivered directly into the PL (experiment 1) and then systemically (experiment 2) prior to tests of the response in the training context as well as an equally familiar but untrained context. vH (systemic CNO) but not vH-PL (intra-PL CNO) inhibition was found to attenuate operant responding in its acquisition context. A third experiment, using the same rats, showed that chemogenetic inhibition of vH also reduced Pavlovian contextual fear. The present results suggest that multisynapatic connections between the vH and PL may be responsible for integration of contextual information with operant behavior.

Voluntary behaviors (operants) can come in two varieties: Goal‐directed actions, which are emitted based on the remembered value of the reinforcer, and habits, which are evoked by antecedent cues and performed without the reinforcer's value in active memory. The two are perhaps most clearly distinguished with the reinforcer‐devaluation test: Goal‐directed actions are suppressed when the reinforcer is separately devalued and responding is tested in extinction, and habitual behaviors are not. But what is the function of habit learning? Habits are often thought to be strong and unusually persistent. The present selective review examines this idea by asking whether habits identified by the reinforcer‐devaluation test are more resistant to extinction, resistant to the effects of other contingency change, vulnerable to relapse, resistant to the weakening effects of context change, or permanently in place once they are learned. Surprisingly little evidence supports the idea that habits are permanent or more persistent. Habits are more context‐specific than goal‐directed actions are. Methods that make behavior persistent do not necessarily work by encouraging habit. The function of habit learning may not be to make a behavior strong or more persistent but to make it automatic and efficient in a particular context.

Our recent research suggests that the interoceptive state associated with stress can function as a contextual stimulus for operant behavior. In the present experiment, we investigated the role of the rodent prelimbic cortex (PL), a brain region that is critical in contextual control of operant behavior, in the ability of a stressed state to produce ABA renewal of an extinguished operant response. Rats were trained to perform a lever press response for a food pellet reward during daily sessions that followed exposure to a stressor that changed each day. The response was then extinguished in the absence of stress. ABA renewal of extinguished responding occurred following exposure to another stressor (different from any used during acquisition) in control rats but not in rats that received a PL-inactivating infusion (baclofen/muscimol). Results confirm that the interoceptive state of stress can play the role of a contextual stimulus and initiate renewal (relapse) of an inhibited behavior when stress has previously been associated with the behavior. In conjunction with our previous work, the present results support the hypothesis that the PL is important for contexts, both exteroceptive and interoceptive, to exert such control over operant behavior.

Obsessive compulsive disorder (OCD) can occur comorbidly with epilepsy; both are complex, disruptive disorders that lower quality of life. Both OCD and epilepsy are disorders of hyperexcitable circuits, but it is unclear whether common circuit pathology may underlie the co-occurrence of these two neuropsychiatric disorders. Here, we induced early-life seizures (ELS) in rats to examine habit formation as a model for compulsive behaviors. Compulsive, repetitive behaviors in OCD utilize the same circuitry as habit formation. We hypothesized that rats with ELS could be more susceptible to habit formation than littermate controls, and that altered behavior would correspond to altered signaling in fronto-striatal circuits that underlie decision-making and action initiation. Here, we show instead that rats with ELS were significantly less likely to form habit behaviors compared with control rats. This behavioral difference corresponded with significant alterations to temporal coordination within and between brain regions that underpin the action to habit transition: 1) phase coherence between the lateral orbitofrontal cortex and dorsomedial striatum (DMS) and 2) theta-gamma coupling within DMS. Finally, we used cortical electrical stimulation as a model of transcranial magnetic stimulation (TMS) to show that temporal coordination of fronto-striatal circuits in control and ELS rats are differentially susceptible to potentiating and suppressive stimulation, suggesting that altered underlying circuit physiology may lead to altered response to therapeutic interventions such as TMS.