Fast-forwarding disgust conditioning: US pre-exposure facilitates the acquisition of oculomotor avoidance

Abstract

During human development, disgust is acquired to a broad range of stimuli, from rotting food to moral transgressions. Disgust’s expansion surely involves associative learning, yet little is known about Pavlovian disgust conditioning. The present study examined conditioned disgust responding as revealed by oculomotor avoidance, the tendency to look away from offensive stimuli. In two experiments, oculomotor avoidance was acquired to a neutral image associated with a disgusting image. However, to our surprise, participants initially dwelled on disgusting images, avoiding them only after multiple exposures. In Experiment 1, this “rubbernecking” response delayed oculomotor avoidance of the associated neutral image. In Experiment 2, we exhausted rubbernecking prior to conditioning by repeatedly exposing participants to the disgusting images. This procedure elicited earlier oculomotor avoidance of the associated neutral stimulus, essentially fast-forwarding conditioning. These findings reveal competing motivational tendencies elicited by disgust stimuli that complicate associative disgust learning.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Notes

  1. 1.

    At the end of each stage, participants also rated the CSs in terms of how afraid, how pleasant/unpleasant, and how aroused the stimuli made them feel. These ratings were included to allow us to compare these results with a fear conditioning version of this experiment, if we were to run one in the future (we instead decided to pursue the rubbernecking finding in Experiment 2). Also, as an experimental measure of conditioning, participants rated how attractive the faces were at the end of each stage. We have omitted these measures for the sake of brevity, but we include them in the data file shared on the OSF.

  2. 2.

    We used 100% reinforcement of the CS because our main concern was documenting the oculomotor CR, not probing extinction resistance. Also, prior disgust conditioning research has generally used this contingency (e.g., Mason and Richardson 2010).

  3. 3.

    The 16 trials of acquisition and extinction were presented in two blocks to allow for potential re-calibration of the eye tracker, to allow for additional assessment of contingency awareness, and to break up the monotonous task.

  4. 4.

    Although interest is often viewed as an aesthetic emotion involving the contemplation of an object for the sake of contemplation (see Armstrong and Detweiler-Bedell 2008a, b), one can also view interest as a highly motivated state. For example, one might seek information about an unpleasant stimulus (and thus view it from a safe vantage point) to prepare for future encounters with the stimulus.

References

  1. Angyal, A. (1941). Disgust and related aversions. The Journal of Abnormal and Social Psychology, 36, 393–412.

    Article  Google Scholar 

  2. Armstrong, T. (2014). Normative and pathological effects of aversive learning on spatial attention. Unpublished doctoral dissertation. Nashville, TN: Vanderbilt University.

  3. Armstrong, T., & Detweiler-Bedell, B. (2008a). Beauty as an emotion: The exhilarating prospect of mastering a challenging world. Review of General Psychology, 12, 305–329.

    Article  Google Scholar 

  4. Armstrong, T., & Detweiler-Bedell, B. (2008b). Beauty as an emotion: The exhilarating prospect of mastering a challenging world. Review of General Psychology, 12(4), 305–329.

    Article  Google Scholar 

  5. Armstrong, T., McClenahan, L., Kittle, J., & Olatunji, B. O. (2014). Don’t look now! Oculomotor avoidance as a conditioned disgust response. Emotion, 14, 95–104.

    Article  PubMed  Google Scholar 

  6. Armstrong, T., & Olatunji, B. O. (2012). Eye tracking of attention in the affective disorders: A meta-analytic review and synthesis. Clinical Psychology Review, 32, 704–723.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Armstrong, T., & Olatunji, B. O. (2017). Pavlovian disgust conditioning as a model for contamination-based OCD: Evidence from an analogue study. Behaviour Research and Therapy, 93, 78–87.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Armstrong, T., Sarawgi, S., & Olatunji, B. O. (2012). Attentional bias toward threat in contamination fear: Overt components and behavioral correlates. Journal of Abnormal Psychology, 121, 232–237.

    Article  PubMed  Google Scholar 

  9. Boddez, Y., Baeyens, F., Luyten, L., Vansteenwegen, D., Hermans, D., & Beckers, T. (2013). Rating data are underrated: Validity of US expectancy in human fear conditioning. Journal of Behavior Therapy and Experimental Psychiatry, 44, 201–206.

    Article  PubMed  Google Scholar 

  10. Borg, C., Bosman, R. C., Engelhard, I., Olatunji, B. O., & de Jong, P. J. (2016). Is disgust sensitive to classical conditioning as indexed by facial electromyography and behavioural responses? Cognition and Emotion, 30, 669–686.

    Article  PubMed  Google Scholar 

  11. Bosman, R. C., Borg, C., & de Jong, P. J. (2016). Optimising extinction of conditioned disgust. PLoS One, 11, e0148626.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bouton, M. E. (2007). Learning and behavior: A contemporary synthesis. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  13. Bradley, M. M., Costa, V. D., & Lang, P. J. (2015). Selective looking at natural scenes: Hedonic content and gender. International Journal of Psychophysiology, 98, 54–58.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bradley, M. M., Lang, P. J., & Cuthbert, B. N. (1993). Emotion, novelty, and the startle reflex: Habituation in humans. Behavioral Neuroscience, 107, 970–980.

    Article  PubMed  Google Scholar 

  15. Calvo, M. G., & Lang, P. J. (2004). Gaze patterns when looking at emotional pictures: Motivationally biased attention. Motivation and Emotion, 28, 221–243.

    Article  Google Scholar 

  16. Cisler, J. M., & Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30, 203–216.

    Article  PubMed  Google Scholar 

  17. Davey, G. C. (2011). Disgust: The disease-avoidance emotion and its dysfunctions. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1583), 3453–3465.

    Article  Google Scholar 

  18. David, B., & Olatunji, B. O. (2011). The effect of disgust conditioning and disgust sensitivity on appraisals of moral transgressions. Personality and Individual Differences, 50, 1142–1146.

    Article  Google Scholar 

  19. De Houwer, J., Thomas, S., & Baeyens, F. (2001). Association learning of likes and dislikes: A review of 25 years of research on human evaluative conditioning. Psychological Bulletin, 127, 853–869.

    Article  PubMed  Google Scholar 

  20. Duits, P., Cath, D. C., Lissek, S., Hox, J. J., Hamm, A. O., & Engelhard, I. M. (2015). Updated meta-analysis of classical fear conditioning in the anxiety disorders. Depression and Anxiety, 32, 239–253.

    Article  PubMed  Google Scholar 

  21. Engelhard, I. M., Leer, A., Lange, E., & Olatunji, B. O. (2014). Shaking that icky feeling: Effects of extinction and counterconditioning on disgust-related evaluative conditioning. Behavior Therapy, 45, 708–719.

    Article  PubMed  Google Scholar 

  22. Hess, U., Arslan, R., Mauersberger, H., Blaison, C., Dufner, M., Denissen, J. J., et al. (2017). Reliability of surface facial electromyography. Psychophysiology, 54(1), 12–23.

    Article  PubMed  Google Scholar 

  23. Hildebrandt, T., Grotzinger, A., Reddan, M., Greif, R., Levy, I., Goodman, W., et al. (2015). Testing the disgust conditioning theory of food-avoidance in adolescents with recent onset anorexia nervosa. Behaviour Research and Therapy, 71, 131–138.

    Article  PubMed  Google Scholar 

  24. Hofmann, W., De Houwer, J., Perugini, M., Baeyens, F., & Crombez, G. (2010). Evaluative conditioning in humans: A meta-analysis. Psychological Bulletin, 136, 390–421.

    Article  PubMed  Google Scholar 

  25. Inbar, Y., Pizarro, D. A., Knobe, J., & Bloom, P. (2009). Disgust sensitivity predicts intuitive disapproval of gays. Emotion, 9, 435–439.

    Article  PubMed  Google Scholar 

  26. Kelly, M. M., & Forsyth, J. P. (2007). Observational fear conditioning in the acquisition and extinction of attentional bias for threat: An experimental evaluation. Emotion, 7, 324–335.

    Article  PubMed  Google Scholar 

  27. Kron, A., Pilkiw, M., Goldstein, A., Lee, D. H., Gardhouse, K., & Anderson, A. K. (2014). Spending one’s time: The hedonic principle in ad libitum viewing of pictures. Emotion, 146, 1087–1101.

    Article  Google Scholar 

  28. Krypotos, A. M., Effting, M., Kindt, M., & Beckers, T. (2015). Avoidance learning: A review of theoretical models and recent developments. Frontiers in Behavioral Neuroscience, 9, 189.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical report A-8. University of Florida, Gainesville, FL.

  30. Lazarus, R. S. (1982). Thoughts on the relations between emotion and cognition. American Psychologist, 37(9), 1019–1024.

    Article  Google Scholar 

  31. Lishner, D. A., Cooter, A. B., & Zald, D. H. (2008). Addressing measurement limitations in affective rating scales: Development of an empirical valence scale. Cognition and Emotion, 22, 180–192.

    Article  Google Scholar 

  32. Lissek, S., Biggs, A. L., Rabin, S. J., Cornwell, B. R., Alvarez, R. P., Pine, D. S., et al. (2008). Generalization of conditioned fear potentiated startle in humans: Experimental validation and clinical relevance. Behaviour Research and Therapy, 46, 678–687.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Loewenstein, G. (1994). The psychology of curiosity: A review and reinterpretation. Psychological Bulletin, 116(1), 75–98.

    Article  Google Scholar 

  34. Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska directed emotional faces (KDEF) (p. 1998). Solna: CD ROM from Department of Clinical Neuroscience, Psychology section, Karolinska Institutet.

    Google Scholar 

  35. Malson, L. (1972). Wolf children. New York, NY: Monthly Review Press. Originally Les Enfants Sauvages. (Original work published 1964).

    Google Scholar 

  36. Mason, E. C., & Richardson, R. (2010). Looking beyond fear: The extinction of other emotions implicated in anxiety disorders. Journal of Anxiety Disorders, 24, 63–70.

    Article  PubMed  Google Scholar 

  37. Mason, E. C., & Richardson, R. (2012). Treating disgust in anxiety disorders. Clinical Psychology: Science and Practice, 19, 180–194.

    Google Scholar 

  38. Mulckhuyse, M., & Dalmaijer, E. S. (2016). Distracted by danger: Temporal and spatial dynamics of visual selection in the presence of threat. Cognitive, Affective, & Behavioral Neuroscience, 16, 315–324.

    Article  Google Scholar 

  39. Nosek, B. A. (2007). Implicit–explicit relations. Current Directions in Psychological Science, 16(2), 65–69.

    Article  Google Scholar 

  40. Nussbaum, M. C. (2001). Upheavals of thought: The intelligence of emotions. New York: Cambridge University Press.

    Google Scholar 

  41. Oaten, M., Stevenson, R. J., & Case, T. I. (2009). Disgust as a disease—avoidance mechanism. Psychological Bulletin, 135, 303–321.

    Article  PubMed  Google Scholar 

  42. Olatunji, B. O., Forsyth, J. P., & Cherian, A. (2007). Evaluative conditioning of disgust: Sticky form of relational learning that is resistant to extinction. Journal of Anxiety Disorders, 21, 820–834.

    Article  PubMed  Google Scholar 

  43. Olatunji, B. O., Lohr, J. M., Smits, J. A., Sawchuk, C. N., & Patten, K. (2009). Evaluative conditioning of fear and disgust in blood-injection-injury phobia: Specificity and impact of individual differences in disgust sensitivity. Journal of Anxiety Disorders, 23, 153–159.

    Article  PubMed  Google Scholar 

  44. Olatunji, B. O., Tomarken, A., & Puncochar, B. D. (2013). Disgust propensity potentiates evaluative learning of aversion. Emotion, 13, 881–890.

    Article  PubMed  Google Scholar 

  45. Oosterwijk, S. (2017). Choosing the negative: A behavioral demonstration of morbid curiosity. PLoS One, 12, e0178399.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Oosterwijk, S., Lindquist, K. A., Adebayo, M., & Barrett, L. F. (2015). The neural representation of typical and atypical experiences of negative images: Comparing fear, disgust and morbid fascination. Social Cognitive and Affective Neuroscience, 11, 11–22.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Pischek-Simpson, L. K., Boschen, M. J., Neumann, D. L., & Waters, A. M. (2009). The development of an attentional bias for angry faces following Pavlovian fear conditioning. Behaviour Research and Therapy, 47, 322–330.

    Article  PubMed  Google Scholar 

  48. Pittig, A., Treanor, M., LeBeau, R. T., & Craske, M. G. (2018). The role of associative fear and avoidance learning in anxiety disorders: Gaps and directions for future research. Neuroscience and Biobehavioral Reviews, 88, 117–140.

    Article  PubMed  Google Scholar 

  49. Rodebaugh, T. L., Scullin, R. B., Langer, J. K., Dixon, D. J., Huppert, J. D., Bernstein, A., et al. (2016). Unreliability as a threat to understanding psychopathology: The cautionary tale of attentional bias. Journal of Abnormal Psychology, 125, 840–851.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Royzman, E. B., & Sabini, J. (2001). Something it takes to be an emotion: The interesting case of disgust. Journal for the Theory of Social Behaviour, 31, 29–59.

    Article  Google Scholar 

  51. Rozin, P., & Fallon, A. E. (1987). A perspective on disgust. Psychological Review, 94, 23–41.

    Article  PubMed  Google Scholar 

  52. Rozin, P., Millman, L., & Nemeroff, C. (1986). Operation of the laws of sympathetic magic in disgust and other domains. Journal of Personality and Social Psychology, 50, 703–712.

    Article  Google Scholar 

  53. Schaller, M., & Park, J. H. (2011). The behavioral immune system (and why it matters). Current Directions in Psychological Science, 20, 99–103.

    Article  Google Scholar 

  54. Schienle, A., Stark, R., & Vaitl, D. (2001). Evaluative conditioning: A possible explanation for the acquisition of disgust responses? Learning and Motivation, 32, 65–83.

    Article  Google Scholar 

  55. Schupp, H. T., Stockburger, J., Codispoti, M., Junghöfer, M., Weike, A. I., & Hamm, A. O. (2006). Stimulus novelty and emotion perception: the near absence of habituation in the visual cortex. NeuroReport, 17, 365–369.

    Article  PubMed  Google Scholar 

  56. Silvia, P. J. (2006). Exploring the psychology of interest. Oxford: Oxford University Press.

    Google Scholar 

  57. Stevenson, R. J., Oaten, M. J., Case, T. I., Repacholi, B. M., & Wagland, P. (2010). Children’s response to adult disgust elicitors: Development and acquisition. Developmental Psychology, 46, 165–177.

    Article  PubMed  Google Scholar 

  58. Turner, S. A., & Silvia, P. J. (2006). Must interesting things be pleasant? A test of competing appraisal structures. Emotion, 6, 670–674.

    Article  PubMed  Google Scholar 

  59. Tybur, J. M., Lieberman, D., Kurzban, R., & DeScioli, P. (2013). Disgust: Evolved function and structure. Psychological Review, 120, 65–84.

    Article  PubMed  Google Scholar 

  60. Vrana, S. R. (1994). Startle reflex response during sensory modality specific disgust, anger and neutral imagery. Journal of Psychophysiology, 8, 211.

    Google Scholar 

  61. Waechter, S., Nelson, A. L., Wright, C., Hyatt, A., & Oakman, J. (2014). Measuring attentional bias to threat: Reliability of dot probe and eye movement indices. Cognitive Therapy and Research, 38(3), 313–333.

    Article  Google Scholar 

  62. Waters, A. M., Theresiana, C., Neumann, D. L., & Craske, M. G. (2017). Developmental differences in aversive conditioning, extinction, and reinstatement: A study with children, adolescents, and adults. Journal of Experimental Child Psychology, 159, 263–278.

    Article  PubMed  Google Scholar 

  63. Zuckerman, M., & Litle, P. (1986). Personality and curiosity about morbid and sexual events. Personality and Individual Differences, 7(1), 49–56.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Thomas Armstrong.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Armstrong, T., Engel, M., Press, T. et al. Fast-forwarding disgust conditioning: US pre-exposure facilitates the acquisition of oculomotor avoidance. Motiv Emot 43, 681–695 (2019). https://doi.org/10.1007/s11031-019-09770-0

Download citation

Keywords

  • Disgust
  • Conditioning
  • Eye movements
  • Morbid curiosity
  • Interest