Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms

doi:10.1016/j.biopsych.2005.12.015

Biological Psychiatry

Volume 60, Issue 4, 15 August 2006, Pages 352-360

https://doi.org/10.1016/j.biopsych.2005.12.015 Get rights and content

Extinction depends, at least partly, on new learning that is specific to the context in which it is learned. Several behavioral phenomena (renewal, reinstatement, spontaneous recovery, and rapid reacquisition) suggest the importance of context in extinction. The present article reviews research on the behavioral and neurobiological mechanisms of contextual influences on extinction learning and retrieval. Contexts appear to select or retrieve the current relationship of the conditional stimulus (CS) with the unconditional stimulus (US), and they are provided by physical background cues, interoceptive drug cues, emotions, recent trials, and the passage of time. The current article pays particular attention to the effects of recent trials and trial spacing. Control of fear extinction by physical context involves interactions between the dorsal hippocampus and the lateral nucleus of the amygdala. This interaction may be mediated by gamma-aminobutyric acid (GABA)-ergic and adrenergic mechanisms.

Section snippets

Physical Context

At least two behavioral phenomena show that responding to the CS after extinction depends on the current context, typically defined as the apparatus or chamber in which CSs (e.g., a tone) and USs (e.g., a footshock) are presented to rats. In the renewal effect, testing the CS in a context other than the context in which extinction has occurred can cause a recovery of responding (e.g., see Bouton 2002, Bouton 2004 for reviews). The renewal effect takes several different forms. In ABA renewal,

Hippocampus and Amygdala

Across levels of analysis, from systems to cellular to molecular mechanisms of extinction, we have only begun to uncover how the brain mediates the effects of context on extinction. There is considerable evidence that the hippocampus is involved in developing cognitive representations of contexts during Pavlovian fear conditioning (Fanselow 2000, Maren and Holt 2000, Rudy and O’Reilly 1999, Rudy and O’Reilly 2001). Therefore, the hippocampus has naturally been the target of several studies

Conclusions and Implications

A variety of behavioral evidence points to a critical role of context in extinction (e.g., Bouton 2002, Bouton 2004). As illustrated by the renewal effect, behavior after extinction is at least partly under the influence of a context-specific form of inhibitory learning. This article has summarized the behavioral evidence supporting the role of context in extinction, as well as what we know about its neurobiological mechanisms. Activity in the hippocampus seems critical in controlling the

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ReviewContextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms

Section snippets

Physical Context

Hippocampus and Amygdala

Conclusions and Implications

Biol Psychiatry

Learn Motiv

Behav Processes

Learn Motiv

Trends Neurosci

Behav Brain Res

Eur Neuropsychopharmacol

Behav Biol

Brain Res

Behav Brain Res

Behav Brain Res

Behav Ther

Clin Psychol Rev

Cell

Administration of dexamethasone prior to training blocks ACTH-induced recovery of an extinguished avoidance response

Behav Neurosci

Contextual conditioning and reinstatement of extinguished instrumental responding

Q J Exp Psychol B

Fear extinction in rodents basic insight to clinical promise

Curr Opin Neurobiology

Pavlovian conditioning and extinction of context cues and punctate CSs in rats with ibotenate lesions of the hippocampus

Psychobiology (Austin, Tex)

Differential control by context in the inflation and reinstatement paradigms

J Exp Psychol Anim Behav Process

Context, time, and memory retrieval in the interference paradigms of Pavlovian conditioning

Psychol Bull

Context, ambiguity, and classical conditioning

Curr Dir Psychol Sci

Context and behavioral processes in extinction

Learn Mem

Behavior systems and the contextual control of anxiety, fear, and panic

State-dependent fear extinction with two benzodiazepine tranquilizers

Behav Neurosci

Contextual control of the extinction of conditioned fearTests for the associative value of the context

J Exp Psychol Anim Behav Process

Effect of context on performance to conditioned stimuli with mixed histories of reinforcement and nonreinforcement

J Exp Psychol Anim Behav Process

Effects of contextual conditioning and unconditional stimulus presentation on performance in appetitive conditioning

Q J Exp Psychol B

Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination

J Exp Psychol Anim Behav Process

Slow reacquisition following extinctionContext encoding and retrieval mechanisms

J Exp Psychol Anim Behav Process

Mood and memory

Am Psychol

Recent and remote extinction cues reduce spontaneous recovery

Q J Exp Psychol B

A retrieval cue for extinction attenuates spontaneous recovery

J Exp Psychol Anim Behav Process

A retrieval cue for extinction attenuates response recovery (renewal) caused by a return to the conditioning context

J Exp Psychol Anim Behav Process

Temporally massed CS presentations generate more fear extinction than spaced presentations

J Exp Psychol Anim Behav Process

The sequential viewFrom rapidly fading stimulus traces to the organization of memory and the abstract concept of number

Psychon Bull Rev

Regulation of gephyrin and GABAA receptor binding within the amygdala after fear acquisition and extinction

J Neurosci

Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction

J Neurosci

Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction

J Neurosci

Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction

Learn Mem

Alcohol as a cue for extinctionState dependency produced by conditioned inhibition

Anim Learn Behav

Amygdala and bed nucleus of the stria terminalisDifferntial roles in fear and anxiety measured with the acoustic startle reflex

Ann N Y Acad Sci

The hippocampus and behavior

Psychol Bull

Mood as a mediator of place dependent memory

J Exp Psychol Gen

Extinction of fear-potentiated startleBlockade by infusion of an NMDA antagonist into the amygdala

J Neurosci

The effects of neurotoxic hippocampal lesions on two effects of context after extinction

Behav Neurosci

Review
Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms