Extinction, generalization, and return of fear: A critical review of renewal research in humans
Highlights
► There are many demonstrations of contextual renewal in human fear conditioning, but the underlying theory is not systematically tested in this sample. ► We outline the different renewal theories and summarize the critical tests. ► We review and evaluate the current set of empirical studies. ► We identify beacons for future research and propose an optimized renewal procedure.
Introduction
Human conditioning research is strongly inspired by animal conditioning findings and theories. One of the central aims is to bridge the translational gap between pre-clinical animal research and patient studies, by testing the animal-based empirical findings and theoretical models in a human (healthy and/or patient) sample using comparable experimental methodology. Validating animal-based theories in human experimental protocols provides the necessary ground for generalizing innovative applications from animals to patients.
Fear extinction is a major research focus in animal conditioning, and has culminated in a widely used theory of extinction (Bouton, 1994). It is obviously also very important in the clinical domain. Fears constitute an important part of anxiety disorders; the extinction of fears contributes importantly to treatment success (Craske et al., 2008). Currently, Bouton's theory of extinction is also widely applied in human clinical and pre-clinical research. It serves as an important guideline for investigating fear extinction on different levels (e.g., emotion, cognition, brain imaging) and for developing and screening extinction-enhancing techniques (see Vervliet, 2008). Most of these studies index the effects of extinction training by assessing contextual renewal, which is also the central phenomenon on which Bouton's theory of extinction is based. In this paper, we (1) describe the renewal phenomenon and outline Bouton's theory of extinction, (2) summarize the critical tests that have validated this extinction theory in animal conditioning research, and (3) evaluate its empirical basis in human fear conditioning. It will become clear throughout the paper that, theoretically, different mechanisms of extinction may (co-)exist and lead up to renewal, but that critical tests are currently lacking in the human domain. Hence, detailed behavioral analysis of extinction in the human fear conditioning paradigm is necessary to further develop human theories of fear extinction, to guide interpretations of brain activity patterns underlying extinction, and to design and screen new behavioral and/or pharmacological enhancers of extinction.
In general, the term ‘fear conditioning’ refers to an experimental procedure in which (1) a neutral stimulus is arranged as a reliable predictor of an aversive stimulus (mostly an electrical stimulation), and (2) the predicting stimulus starts eliciting cognitive, emotional and/or behavioral reactions in anticipation of the aversive shock. In contemporary research, psychophysiological recordings and subjective ratings are often combined in order to get a clear picture of the conditioned fear response. These recordings frequently include skin conductance responses and/or fear-potentiated startle reflexes. Ratings often ask for the expectancy of the shock, the level of fear, or the acquired valence of the predicting stimulus (see Lipp, 2006).
The conditioning process is usually conceptualized as follows. Paired presentations of a neutral stimulus (the conditional stimulus, CS) and an aversive stimulus (the unconditional stimulus, US) result in the formation of an association between the memory representations of the neutral CS and the aversive US. Future confrontations with the CS will activate its own representation and, by virtue of the association, the memory of the US as well. This ‘thinking of the aversive US’ elicits anticipatory fear. Hence, the basic associative learning framework is a sort of ‘spreading of activation’ framework.
Fear extinction occurs when repeated presentations of the CS, in the absence of the US, lead to a gradual decay of anticipatory fear reactions. This apparently simple phenomenon has proven difficult to explain. Since Pavlov's original observations (Pavlov, 1927), the crucial question has been whether behavioral extinction reflects unlearning of the original CS–US association (e.g., Rescorla and Wagner, 1972), or whether it reflects an inhibition of the original CS–US association (e.g., Pavlov, 1927, Konorski, 1967). In the former case, extinction is considered a passive process by which the CS returns to a neutral state (as if no conditioning has occurred). However, numerous studies demonstrate that fear reactions can easily return to a conditioned-and-extinguished CS (Bouton, 2002). This strongly suggests that an extinguished CS is not at all neutral: The fear reactions can only recover if the original CS–US association somehow survives extinction. Arguably, new learning occurs during extinction that inhibits, but not erases, the CS–US association (Pavlov, 1927, Konorski, 1967). This new learning is often conceptualized as the formation of an inhibitory CS–US association. Henceforth, the CS both activates and deactivates the representation of the US, so that the CS will sometimes elicit fear and sometimes not. The circumstances at test largely determine which association will determine the behavioral outcome of the CS (fear/no fear). This is convincingly demonstrated by the renewal effect.
Section snippets
Contextual renewal: extinction, generalization, and return of fear
Contextual renewal refers to a situation where changes in the background context evoke a recovery of fear to a conditioned-and-extinguished stimulus (see Bouton, 2002). For example, if CS–US pairings have occurred in context A, and CS-only extinction presentations have occurred in context B, renewal tests can consist of presenting the CS in context A again or in a novel context C (ABA-renewal and ABC-renewal, respectively; Bouton and Bolles, 1979). The typical renewal observation is an increase
The theory of extinction: critical tests
The extinction theory of Bouton (1994) has been validated in animal conditioning research by systematically rejecting a set of alternative hypotheses that are simpler in nature (and hence, more parsimonious). We briefly introduce these alternative hypotheses and present the critical tests.
Contextual renewal studies in human fear conditioning
In human fear conditioning research, it is conventional to include a control stimulus throughout the experiment. This control stimulus (CS−) is equally often presented as the CS+ during the acquisition phase, but never paired with the aversive US. Hence, the only difference between the CS+ and the CS− is their contingency with shock. Comparing the response to the CS+ with the response to the CS− reflects the actual conditioning effect, controlling for non-associative processes. This is
Recommendations for future research
We propose that studies on contextual renewal should routinely include analyses of the generalization of acquisition (by comparing the end of acquisition and the beginning of extinction) and the recovery of fear (by comparing the end of extinction with the beginning of test). These analyses should also include the responses to the CS−, in order to distinguish fear recovery from a general increase of fear. Possibly, an extinction retention index can be used that includes the end levels of
Acknowledgement
This research was supported by University of Leuven grants GOA/2007/03 and PF/10/005.
References (46)
- et al.
Effects of multiple contexts and context similarity on the renewal of extinguished conditioned behaviour in an ABA design with humans
Learning and Motivation
(2011) 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.
Optimizing inhibition learning during exposure therapy
Behaviour Research and Therapy
(2008) - et al.
All we need is a cue to remember: the effect of an extinction cue on renewal
Behaviour Research and Therapy
(2008) - et al.
The effect of an extinction cue on ABA-renewal: does valence matter?
Learning and Motivation
(2011) - et al.
Non-differential return of fear in humans after a reinstatement procedure
Acta Psychologica
(2009) - et al.
Contextual renewal of human fear associations in a renewal paradigm
Behaviour Research and Therapy
(2007) - et al.
Reducing chronic anxiety by making the threatening event predictable: an experimental approach
Behaviour Research and Therapy
(2009) Generalization of conditioned fear-potentiated startle in humans: experimental validation and clinical relevance
Behaviour Research and Therapy
(2008)
Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert
Biological Psychiatry
Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study
Journal of Psychiatry Research
Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder
Biological Psychiatry
The influence of gonadal hormones on conditioned fear extinction in healthy humans
Neuroscience
Behavioral and neural analysis of extinction
Neuron
Exposure to a novel context after extinction causes a renewal of extinguished conditioned responses: implications for the treatment of fear
Behaviour Research and Therapy
Conducting extinction in multiple contexts does not necessarity attenuate the renewal of shock expectancy in a fear-conditioning procedure with humans
Behaviour Research and Therapy
The renewal of extinguished conditioned fear with fear-relevant and fear-irrelevant stimuli by a context change after extinction
Behaviour Research and Therapy
Return of fear in a human differential conditioning paradigm caused by a return to the original acquisition context
Behaviour Research and Therapy
Stronger renewal in human fear conditioning when tested with an acquisition retrieval cue than with an extinction retrieval cue
Behaviour Research and Therapy
Learning and memory in conditioned fear extinction: effects of d-cycloserine
Acta Psychologica
Unpaired shocks during extinction weaken the contextual renewal of a conditioned discrimination
Learning and Motivation
Contextual-specificity of short-delay extinction in humans: renewal of fear-potentiated startle in a virtual environment
Learning and Memory
Cited by (132)
Gaze and avoidant patterns of visual attention to aversive stimuli during fear habituation trial: A pilot eye tracking study
2023, Journal of Behavioral and Cognitive TherapyThe role of consciousness in threat extinction learning
2023, Consciousness and CognitionInactivation of medial or lateral orbitofrontal cortex during fear extinction did not interfere with fear renewal
2023, Neurobiology of Learning and MemoryFear Reduced Through Unconditional Stimulus Deflation Is Behaviorally Distinct From Extinction and Differentially Engages the Amygdala
2023, Biological Psychiatry Global Open ScienceBrief Imaginal Exposure for PTSD: Trajectories of Change in Distress
2023, Cognitive and Behavioral PracticeSystematically investigating the role of context on effect replicability in reinstatement of fear in humans
2023, Behaviour Research and Therapy