Context, attention, and the switch between habit and goal-direction in behavior

This article reviews recent findings from the author’s laboratory that may provide new insights into how habits are made and broken. Habits are extensively practiced behaviors that are automatically evoked by antecedent cues and performed without their goal (or reinforcer) “in mind.” Goal-directed actions, in contrast, are instrumental behaviors that are performed because their goal is remembered and valued. New results suggest that actions may transition to habit after extended practice when conditions encourage reduced attention to the behavior. Consistent with theories of attention and learning, a behavior may command less attention (and become habitual) as its reinforcer becomes well-predicted by cues in the environment; habit learning is prevented if presentation of the reinforcer is uncertain. Other results suggest that habits are not permanent, and that goal-direction can be restored by several environmental manipulations, including exposure to unexpected reinforcers or context change. Habits are more context-dependent than goal-directed actions are. Habit learning causes retroactive interference in a way that is reminiscent of extinction: It inhibits, but does not erase, goal-direction in a context-dependent way. The findings have implications for the understanding of habitual and goal-directed control of behavior as well as disordered behaviors like addictions.

Inhibition of vascular adhesion protein 1 protects dopamine neurons from the effects of acute inflammation and restores habit learning in the striatum

Background Changes in dopaminergic neural function can be induced by an acute inflammatory state that, by altering the integrity of the neurovasculature, induces neuronal stress, cell death and causes functional deficits. Effectively blocking these effects of inflammation could, therefore, reduce both neuronal and functional decline. To test this hypothesis, we inhibited vascular adhesion protein 1 (VAP-1), a membrane-bound protein expressed on the endothelial cell surface, that mediates leukocyte extravasation and induces oxidative stress. Method We induced dopaminergic neuronal loss by infusing lipopolysaccharide (LPS) directly into the substantia nigra (SN) in rats and administered the VAP-1 inhibitor, PXS-4681A, daily. Results LPS produced: an acute inflammatory response, the loss of dopaminergic neurons in the SN, reduced the dopaminergic projection to SN target regions, particularly the dorsolateral striatum (DLS), and a deficit in habit learning, a key function of the DLS. In an attempt to protect SN neurons from this inflammatory response we found that VAP-1 inhibition not only reduced neutrophil infiltration in the SN and striatum, but also reduced the associated striatal microglia and astrocyte response. We found VAP-1 inhibition protected dopamine neurons in the SN, their projections to the striatum and promoted the functional recovery of habit learning. Thus, we reversed the loss of habitual actions, a function usually dependent on dopamine release in DLS and sensitive to striatal dysfunction. Conclusions We establish, therefore, that VAP-1 inhibition has an anti-inflammatory profile that may be beneficial in the treatment of dopamine neuron dysfunction caused by an acute inflammatory state in the brain.

Inhibition of Vascular Adhesion Protein 1 Protects Dopamine Neurons From the Effects of Acute Inflammation and Restores Habit Learning in the Striatum

BackgroundChanges in dopaminergic neural function can be induced by an acute inflammatory state that, by altering the integrity of the neurovasculature, induces neuronal stress, cell death and causes functional deficits. Effectively blocking these effects of inflammation could, therefore, reduce both neuronal and functional decline. To test this hypothesis, we inhibited vascular adhesion protein 1 (VAP-1), a membrane bound protein expressed on endothelial cell surface, that mediates leukocyte extravasation and induces oxidative stress. MethodWe induced dopaminergic neuronal loss by infusing lipopolysaccharide (LPS) directly into the substantia nigra (SN) in rats and administered the VAP-1 inhibitor, PXS-4681A, daily. ResultsLPS resulted in an acute inflammatory response, the loss of dopaminergic neurons in the SN, reduced dopaminergic projection to SN target regions, particularly the dorsolateral striatum (DLS), and a deficit in habit learning, a key function of the DLS. In an attempt to protect SN neurons from this inflammatory response we found that VAP-1 inhibition not only reduced neutrophil infiltration in the SN and striatum but also reduced the associated microglia and astrocyte response in the striatum. We found VAP-1 inhibition protected dopaminergic neurons in the SN, their projections to the striatum and promoted the functional recovery of habit learning. Thus, we reversed the loss of habitual actions, a function usually dependent on dopamine release in DLS and sensitive to striatal dysfunction. ConclusionsWe establish, therefore, that VAP-1 inhibition has an anti-inflammatory profile that may have beneficial in the treatment of dopaminergic dysfunction caused by an acute inflammatory state in the brain.

Individual differences in the engagement of habitual control over alcohol seeking predicts the development of compulsive alcohol seeking and drinking

Excessive drinking is an important behavioural characteristic of alcohol addiction, but not the only one. Individuals addicted to alcohol crave alcoholic beverages, spend time seeking alcohol despite negative consequences, and eventually drink to intoxication. With prolonged use, control over alcohol seeking devolves to anterior dorsolateral striatum, dopamine-dependent mechanisms implicated in habit learning and individuals in whom alcohol-seeking relies more on these mechanisms are more likely to persist in seeking alcohol despite the risk of punishment. Here, we tested the hypothesis that the development of habitual alcohol-seeking predicts the development of compulsive seeking and that, once developed, it is associated with compulsive alcohol drinking. Male alcohol-preferring rats were pre-exposed intermittently to a two-bottle choice procedure, and trained on a seeking–taking chained schedule of alcohol reinforcement until some individuals developed punishment-resistant seeking behaviour. The associative basis of their seeking responses was probed with an outcome-devaluation procedure, early or late in training. After seeking behaviour was well established, subjects that had developed greater resistance to outcome-devaluation (were more habitual) were more likely to show punishment-resistant (compulsive) alcohol seeking. These individuals also drank more alcohol, despite quinine adulteration, even though having similar alcohol preference and intake before and during instrumental training. They were also less sensitive to changes in the contingency between seeking responses and alcohol outcome, providing further evidence of recruitment of the habit system. We therefore provide direct behavioural evidence that compulsive alcohol seeking emerges alongside compulsive drinking in individuals that have preferentially engaged the habit system.