ReviewBehavioral and neurobiological mechanisms of extinction in Pavlovian and instrumental learning
Introduction
Behavioral research over the last few decades has made significant progress in uncovering the mechanisms that underlie extinction, the behavioral phenomenon in which learned behavior decreases in strength or frequency when the event that reinforced it is removed (e.g., Delamater & Westbrook, 2014). Extinction is important, in part because it is one of the most basic of all behavioral change effects, and in part because it is thought to be involved in many clinical treatments that are designed to get rid of unwanted learned behaviors, thoughts, and emotions (e.g., Craske et al., 2008, Craske et al., 2012). Since the 1970s, extinction has been extensively studied in Pavlovian conditioning, where responding to a conditioned stimulus (CS) that has been associated with an unconditioned stimulus (US) decreases when the CS is then presented repeatedly alone. The results of this literature, along with the larger behavioral research literature of which it is a part, support a set of principles of extinction that are summarized in Table 1. These principles have gone onto shape further research on extinction at both the behavioral and neurobiological levels of analysis. The purpose of the present article is to discuss these principles and explore how they have facilitated progress in behavioral and neurobiological research on Pavlovian extinction and a “newer” frontier concerning the extinction of instrumental learning, where the focus is on voluntary behaviors that are controlled by their consequences (reinforcers). We also suggest that continued success at elucidating the neurobiological mechanisms of Pavlovian and instrumental extinction will require continued research at the behavioral level.
Section snippets
Summary extinction principles
The first extinction principle supported by behavioral research is perhaps the most widely recognized today: Although behavior goes away in extinction, Extinction is not the same as erasure. Learning theorists have long recognized that there is a difference between behavior on the one hand and the organism’s knowledge on the other. Extinction is a good example of the so-called “learning-performance distinction:” Although performance is at a zero level at the end of extinction, the original
Neurobiological mechanisms of Pavlovian extinction
Advances in our understanding of extinction from a behavioral point of view contributed directly to a new interest in the underlying neurobiological mechanisms that began to crystallize and mature in the 2000s (e.g., Delamater, 2004, Myers and Davis, 2002). In general, the neuroscience literature can be divided into several areas that emphasize one of the major principles just described. Perhaps the largest area is one investigating the neural circuits and synaptic changes that support new
Behavioral mechanisms of instrumental extinction
Other advances are being made in understanding the behavioral and neurobiological mechanisms of instrumental extinction. In instrumental (or operant) learning, organisms learn to perform certain behaviors (e.g., pressing a lever or pulling a chain) when a reinforcing event like a food pellet is presented as a consequence of it. In extinction, the behavior declines when the reinforcer is no longer presented. Instrumental extinction is as important to understand as Pavlovian extinction if we want
Neurobiological mechanisms of instrumental extinction
Instrumental learning and extinction procedures have recently become important tools for investigating the neurobiology of drug-taking and relapse (e.g., Marchant, Li, & Shaham, 2013). The approach has been stimulated and enriched by behavioral work. For example, many studies have examined the contextual control of extinguished operant behavior reinforced by drugs of abuse (see Bouton, Winterbauer, & Vurbic, 2012; Millan, Marchant, & McNally, 2011 for reviews). The area has the potential to
Conclusion
Our review has illustrated a tight coupling between behavior theory and research on the neural mechanisms of extinction. Indeed, it can be said that the study of neurobiological mechanisms of extinction has stood on the shoulders of research that has investigated its behavioral underpinnings. However, we will close by noting that, in all likelihood, the linkage between these levels of analysis will need to be ongoing. As our review indicates, extinction and the many behavioral effects that
Acknowledgment
Preparation of the manuscript was supported by National of Institute on Drug Abuse Grant RO1 DA033123 to M.E.B.
References (202)
Partial reinforcement effects on vigor and persistence
- et al.
d-Cycloserine facilitates extinction of a cocaine-induced conditioned place preference
Behavioral Brain Research
(2006) Context and ambiguity in the extinction of emotional learning: Implications for exposure therapy
Behaviour Research and Therapy
(1988)Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction
Biological Psychiatry
(2002)- et al.
Contextual control of the extinction of conditioned fear
Learning and Motivation
(1979) - et al.
Sources of relapse after extinction in Pavlovian and instrumental learning
Clinical Psychology Review
(1991) - et al.
d-Cycloserine facilitates context specific fear extinction learning
Neurobiology of Learning and Memory
(2008) - et al.
Occasional reinforced trials during extinction can slow the rate of rapid reacquisition
Learning and Motivation
(2004) - et al.
Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex
Neuron
(2007) - et al.
ABA and ABC renewal of conditioned magazine approach are not impaired by dorsal hippocampus inactivation or lesions
Behavioral Brain Research
(2013)
A sequential hypothesis of instrumental learning
Psychology of Learning and Motivation
Optimizing inhibitory learning during exposure therapy
Behaviour Research and Therapy
Issues in the extinction of specific stimulus–outcome associations in Pavlovian conditioning
Behavioural Processes
Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction
Neuropsychopharmacology
Extinction after aversive conditioning: An associative or nonassociative process?
Learning and Motivation
Renewal of extinguished cocaine-seeking
Neuroscience
The neural correlates and role of D1 dopamine receptors in renewal of extinguished alcohol-seeking
Neuroscience
Occasion setting in Pavlovian conditioning
Transfer of inhibitory stimulus control in operant feature-negative discrimination
Learning and Motivation
No erasure effect of retrieval–extinction trial on fear memory in the hippocampus-independent and dependent paradigms
Neuroscience Letters
Deepened extinction of cocaine cues
Drug and Alcohol Dependence
Reconsolidation in a human fear conditioning study: A test of extinction as updating mechanism
Biological Psychology
Facilitation of extinction and re-extinction of operant behavior in mice by chlordiazepoxide and d-cycloserine
Neurobiology of Learning and Memory
A randomized placebo-controlled trial of d-cycloserine and exposure therapy for posttraumatic stress disorder
Journal of Psychiatric Research
Recent developments in animal models of drug relapse
Current Opinion in Neurobiology
Post-retrieval extinction as reconsolidation interference: Methodological issues or boundary conditions?
Psychopharmacology
Contextual conditioning during free-operant extinction: Unsignaled, signaled, and backward-signaled noncontingent food
Animal Learning & Behavior
Contextual conditioning and reinstatement of extinguished instrumental responding
The Quarterly Journal of Experimental Psychology
Still at the choice point: Action selection and initiation in instrumental conditioning
Annals of the New York Academy of Sciences
Effects of ambient temperature on the relative reinforcing strength of MDMA using a choice procedure in monkeys
Psychopharmacology
A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking
The Journal of Neuroscience
Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin
Nature Neuroscience
Characterization of methylphenidate self-administration and reinstatement in the rat
Psychopharmacology
Differential control by context in the inflation and reinstatement paradigms
Journal of Experimental Psychology: Animal Behavior Processes
Context, time, and memory retrieval in the interference paradigm of Pavlovian learning
Psychological Bulletin
Signals for whether versus when an event will occur
A learning theory perspective on lapse and relapse and the maintenance of behavior change
Health Psychology
Context and behavioral processes in extinction
Learning & Memory
Role of conditioned contextual stimuli in reinstatement of extinguished fear
Journal of Experimental Psychology: Animal Behavioral Processes
Intertrial interval as a contextual stimulus: Further analysis of a novel asymmetry in temporal discrimination learning
Journal of Experimental Psychology: Animal Behavior Processes
State-dependent fear extinction with two benzodiazepine tranquilizers
Behavioral Neuroscience
Contextual control of the extinction of conditioned fear: Tests for the associative value of the context
Journal of Experimental Psychology: Animal Behavior Processes
Context effects on conditioning, extinction, and reinstatement in an appetitive conditioning preparation
Animal Learning & Behavior
Renewal of extinguished responding in a second context
Animal Learning & Behavior
Effects of contextual conditioning and unconditional stimulus presentation on performance in appetitive conditioning
The Quarterly Journal of Experimental Psychology
Renewal after the extinction of free operant behavior
Learning & Behavior
Relapse processes after the extinction of instrumental behavior: Renewal, resurgence, and reacquisition
Behavioral Processes
Context and extinction: Mechanisms of relapse in drug self-administration
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