Behavioral and neural processes in counterconditioning: Past and future directions

https://doi.org/10.1016/j.brat.2019.103532Get rights and content

Highlights

  • Counterconditioning is a technique and process of behavior modification.

  • Whether counterconditioning is more or less effective than extinction is unclear.

  • We review behavioral and neural findings of counterconditioning across species.

  • We hope this review motivates further research on this underexplored topic.

Abstract

Counterconditioning refers both to the technique and putative process by which behavior is modified through a new association with a stimulus of an opposite valence. Similar to extinction, counterconditioning is considered a form of inhibition that interferes with the expression of the originally learned response without erasing it. But whereas interest in extinction continues to rise, counterconditioning has received far less attention. Here, we provide an in-depth review of counterconditioning research and detail whether counterconditioning is any more effective than extinction at preventing relapse of the originally learned behavior. We consider the clinical implications of counterconditioning, describe recent neurobiological and neuroimaging research in this area, and consider future avenues in need of further investigation.

Section snippets

A short history of counterconditioning

As the term implies, counterconditioning is derived from research in Pavlovian and operant conditioning. In a typical Pavlovian counterconditioning design, a neutral conditioned stimulus (CS, e.g., a tone) is first paired with a biologically salient US of a particular valence (e.g., shock or food) and then paired with a US of the opposite valence (e.g., food or shock, respectively). In rodents, performance at test is oftentimes measured as the amount of time either freezing to the CS, the

Counterconditioning versus standard extinction

Extinction refers both to the technique of omitting a US or reinforcement following conditioning, as well as to the process by which omission leads to a reduction in learned behavior. It is considered a form of retroactive inhibition that interferes with expression of the originally learned response. It is also widely appreciated that extinction tends to be a fairly weak and impermanent form of inhibition, and that the originally learned response often reemerges under a variety of circumstances

Non-human animal research on counterconditioning

While the focus of counterconditioning has predominately been on modulating responses to the CS, early work showed that counterconditioning alters the value of a US (US1) when it is paired with another US of the opposite valence (US2). Pearce and Dickinson (1975) showed that pairing shock with food (US1-US2 pairing) reduced the effectiveness of the shock in subsequent conditioned suppression training. Another fairly robust finding in the counterconditioning literature is that of proactive

Neurobiology of counterconditioning

Whether the neural mechanism by which counterconditioning achieves its effects are distinct from the well-delineated neural circuitry of extinction is unclear. The switch from appetitive-to-aversive conditioning has been linked to reduced levels of activity in midbrain periaqueductal grey, as compared to aversive conditioning without prior appetitive conditioning (Nasser & McNally, 2012). Appetitive-to-aversive counterconditioning is also linked to increased activity in regions associated with

Human research on counterconditioning

Human research focused on counterconditioning has been sparse, but the topic has maintained some interest in the area of pain, fear, and changing learned preferences. The use of counterconditioning as a strategy to reduce fear of pain shows mixed results. Meulders, Karsdorp, Claes, and Vlaeyen (2015) first fear-conditioned a movement (CS) using a painful shock (US), and then paired the movement with either monetary reward (counterconditioning group) or simply omitted the US (extinction group).

Derivatives of counterconditioning

Another approach to augment extinction training involves replacing a valenced US (e.g., shock) with a neutral stimulus. Raes and De Raedt (2012) found that replacing the aversive US with a neutral outcome (a simple tone) was equivalent to replacing the aversive US with an appetitive outcome (the sound of baby laughter), in reducing evaluative responses of fear. In a cross-species behavioral experiment, Dunsmoor, Campese, et al. (2015) tested the effect of augmenting extinction by replacing

Negative valence system disorders

The principles of counterconditioning have been effectively utilized through systematic desensitization therapy to treat disorders characterized by negative valence, such as Specific Phobias and Obsessive Compulsive Disorder (Tryon, 2005). Paunovic (2011) developed an exposure counterconditioning method to treat PTSD by asking patients to undergo imaginal reliving of a pleasurable emotional experience incompatible to the trauma. Approaches that integrate exposure treatment with appetitive

Optimizing counterconditioning

The ultimate goal of seeking alternative approaches to standard extinction is to innovate clinical treatment to more effectively prevent the relapse of unwanted thoughts and behavior. Counterconditioning is procedurally distinct from standard extinction because it involves the presentation of a new outcome, rather than omission of the expected outcome. Mechanistically, counterconditioning might operate by increasing the prediction error, thereby enhancing the recruitment of dopaminergic

Counterconditioning via real-time fMRI neurofeedback

An inherit drawback of exposure-based treatments is the distress and anxiety caused by stimulus exposure during treatment. In the worst case, the anxiety produced during exposure leads to patient attrition (Loerinc et al., 2015). Real-time fMRI neurofeedback (rt-fMRI) combined with multivariate pattern analysis (MVPA) may offer one path of treatment without the need for patient exposure to the stimulus (Norman, Polyn, Detre, & Haxby, 2006; Sitaram et al., 2017). The general goal of combining

Conclusion

Historically, research on counterconditioning has been largely situated in learning theory accounts of animal behavior. But research on affective value coding in the brain has borrowed from the theoretical tradition of aversive-appetitive interactions in Pavlovian conditioning, and exciting avenues of neuroimaging research in humans is using counterconditioning in an attempt to change the neural representations of feared stimuli. As research on counterconditioning moves forward, an important

Acknowledgments

The authors acknowledge funding from National Institutes of Health R00MH106719 and a National Science Foundation CAREER award (#1844792) to JED and National Institutes of Health R00MH106719-04S to NEK.

References (138)

  • A. Brunet et al.

    Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder

    Journal of Psychiatric Research

    (2008)
  • N. Claes et al.

    Competing goals attenuate avoidance behavior in the context of pain

    The Journal of Pain

    (2014)
  • A.C. Courville et al.

    Bayesian theories of conditioning in a changing world

    Trends in Cognitive Sciences

    (2006)
  • M.G. Craske et al.

    Maximizing exposure therapy: An inhibitory learning approach

    Behaviour Research and Therapy

    (2014)
  • N.D. Daw et al.

    Opponent interactions between serotonin and dopamine

    Neural Networks

    (2002)
  • D.J. Delprato et al.

    Counterconditioning and exposure-only in the treatment of specific (conditioned suppression) and generalized fear in rats

    Behaviour Research and Therapy

    (1973)
  • H.J. Dour et al.

    Positive valence reduces susceptibility to return of fear and enhances approach behavior

    Journal of Behavior Therapy and Experimental Psychiatry

    (2016)
  • J.E. Dunsmoor et al.

    Novelty-facilitated extinction: Providing a novel outcome in place of an expected threat diminishes recovery of defensive responses

    Biological Psychiatry

    (2015)
  • J.E. Dunsmoor et al.

    Episodic memory and Pavlovian conditioning: Ships passing in the night

    Current opinion in behavioral sciences

    (2019)
  • J.E. Dunsmoor et al.

    Role of conceptual knowledge in learning and retention of conditioned fear

    Biological Psychology

    (2012)
  • J.E. Dunsmoor et al.

    Rethinking extinction

    Neuron

    (2015)
  • G.H. Eifert et al.

    Affect modification through evaluative conditioning with music

    Behaviour Research and Therapy

    (1988)
  • I.M. Engelhard et al.

    Shaking that icky feeling: Effects of extinction and counterconditioning on disgust-related evaluative learning

    Behavior Therapy

    (2014)
  • T.F. Giustino et al.

    Revisiting propranolol and PTSD: Memory erasure or extinction enhancement?

    Neurobiology of Learning and Memory

    (2016)
  • S. Grossberg

    The imbalanced brain: From normal behavior to schizophrenia

    Biological Psychiatry

    (2000)
  • L.M. Gunther et al.

    Conducting exposure treatment in multiple contexts can prevent relapse

    Behaviour Research and Therapy

    (1998)
  • D. Hermans et al.

    Expectancy-learning and evaluative learning in human classical conditioning: Affective priming as an indirect and unobtrusive measure of conditioned stimulus valence

    Behaviour Research and Therapy

    (2002)
  • P.J. de Jong et al.

    Counterconditioning in the treatment of spider phobia: Effects on disgust, fear and valence

    Behaviour Research and Therapy

    (2000)
  • R. Kalisch et al.

    A dopaminergic basis for fear extinction

    Trends in Cognitive Sciences

    (2019)
  • S. Kang et al.

    Reduced return of threat expectancy after counterconditioning versus extinction

    Behaviour Research and Therapy

    (2018)
  • V.L. Kelly et al.

    Can Rachman's indirect pathways be used to un-learn fear? A prospective paradigm to test whether children's fears can be reduced using positive information and modelling a non-anxious response

    Behaviour Research and Therapy

    (2010)
  • A.-M. Krypotos et al.

    Testing a novelty-based extinction procedure for the reduction of conditioned avoidance

    Journal of Behavior Therapy and Experimental Psychiatry

    (2018)
  • J.L. Lee

    Reconsolidation: Maintaining memory relevance

    Trends in Neurosciences

    (2009)
  • A.G. Loerinc et al.

    Response rates for CBT for anxiety disorders: Need for standardized criteria

    Clinical Psychology Review

    (2015)
  • J.F. Lomont

    Reciprocal inhibition or extinction?

    Behaviour Research and Therapy

    (1965)
  • K. Lucas et al.

    Novelty-facilitated extinction and the reinstatement of conditional human fear

    Behaviour Research and Therapy

    (2018)
  • D. Ludvik et al.

    Effective behavioural strategies for reducing disgust in contamination-related OCD: A review

    Clinical Psychology Review

    (2015)
  • L. Luyten et al.

    A preregistered, direct replication attempt of the retrieval-extinction effect in cued fear conditioning in rats

    Neurobiology of Learning and Memory

    (2017)
  • A. Meulders et al.

    Comparing counterconditioning and extinction as methods to reduce fear of movement-related pain

    The Journal of Pain

    (2015)
  • P. Muris et al.

    Reduction of verbally learned fear in children: A comparison between positive information, imagery, and a control condition

    Journal of Behavior Therapy and Experimental Psychiatry

    (2011)
  • C. Newall et al.

    The relative effectiveness of extinction and counter-conditioning in diminishing children's fear

    Behaviour Research and Therapy

    (2017)
  • K.A. Norman et al.

    Beyond mind-reading: Multi-voxel pattern analysis of fMRI data

    Trends in Cognitive Sciences

    (2006)
  • C.A. Peck et al.

    Context and performance in aversive-to-appetitive and appetitive-to-aversive transfer

    Learning and Motivation

    (1990)
  • M.B. Powers et al.

    Virtual reality exposure therapy for anxiety disorders: A meta-analysis

    Journal of Anxiety Disorders

    (2008)
  • A.K. Raes et al.

    The effect of counterconditioning on evaluative responses and harm expectancy in a fear conditioning paradigm

    Behavior Therapy

    (2012)
  • M.J. Anderson et al.

    Exposure to novelty weakens conditioned fear in long-Evans rats

    Psicológica: International Journal of Methodology and Experimental Psychology

    (2013)
  • F. Baeyens et al.

    Pavlovian associations are forever: On classical conditioning and extinction

    Journal of Psychophysiology

    (1995)
  • K.C. Berridge

    Affective valence in the brain: Modules or modes?

    Nature Reviews Neuroscience

    (2019)
  • M.E. Bouton

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

    Psychological Bulletin

    (1993)
  • M.E. Bouton

    Context and behavioral processes in extinction

    Learning & Memory

    (2004)
  • Cited by (50)

    View all citing articles on Scopus
    View full text