Cited by 44Anxiety, Depression, Psychometrics, Treatment, Cognitive ProcessesMemory and Neural MechanismsPsychosomatic Disorders and Their Treatments

Interoception, conditioning, and fear: The panic threesome

Open access
Van Diest, Ilse·2019·Psychophysiology

Abstract

The present article aims to illustrate and review evidence on how associative learning involving interoceptive stimuli (interoceptive conditioning) can lead to changes in physiological, emotional, and perceptual outcomes. We first outline a functional perspective on Pavlovian conditioning and provide a general introduction and historical background on interoceptive conditioning as a special instance of Pavlovian conditioning. Next, biological and learning accounts of panic disorder are discussed, followed by an analysis of which stimuli and responses may be most promising to model learning that is relevant to panic disorder. Finally, studies on interoceptive fear conditioning with respiratory stimuli are reviewed and discussed, and future directions are outlined.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/psyp.13421

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 152

  1. Acheson, D. T., Forsyth, J. P., & Moses, E. (2012). Interoceptive fear conditioning and panic disorder: the role of conditioned stimulus-unconditioned stimulus predictability. Behavior therapy, 43(1), 174-189. doi:10.1016/j.beth.2011.06.001 · DOI
  2. Acheson, D. T., Forsyth, J. P., Prenoveau, J. M., & Bouton, M. E. (2007). Interoceptive fear conditioning as a learning model of panic disorder: an experimental evaluation using 20% CO 2 -enriched air in a non-clinical sample. Behaviour research and therapy, 45(10), 2280- 2294. doi:10.1016/j.brat.2007.04.008 · DOI
  3. Alexander-Miller, S., & Davenport, P. W. (2010). Perception of multiple-breath inspiratory resistive loads in males and females. Biological psychology, 84(1), 147-149. doi:10.1016/j.biopsycho.2010.03.004 · DOI
  4. Alius, M. G., Pané-Farré, C. A., Löw, A., & Hamm, A. O. (2015). Modulation of the blink reflex and P3 component of the startle response during an interoceptive challenge. Psychophysiology, 52(1), 140-148. doi:10.1111/psyp.12295 · DOI
  5. Argyropoulos, S. V., Bailey, J. E., Hood, S. D., Kendrick, A. H., Rich, A. S., Laszlo, G., Nash, J. R., Lightman, S., & Nutt, D. J. (2002). Inhalation of 35% CO 2 results in activation of the HPA axis in healthy volunteers. Psychoneuroendocrinology, 27, 715- 729. doi:10.1016/s0306-4530(01)00075-0 · DOI
  6. Bailey, J. E., Argyopoulos, S. V., Kendrick, A. H., & Nutt, D. J. (2005). Behavioral and cardiovascular effects of 7.5% CO 2 in human volunteers. Depression and Anxiety, 21, 18- 25. doi:10.1002/da.20048 · DOI
  7. Barlow, D. H. (1988). Anxiety and its disorders: The nature and treatment of anxiety and panic. New York: Guilford Press.
  8. Battaglia, M. (2017). Sensitivity to carbon dioxide and translational studies of anxiety disorders. Neuroscience, 346, 434-436. doi:10.1016/j.neuroscience.2017.01.053 · DOI
  9. Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A. R. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science, 269(5227), 1115-1118. doi:10.1093/neucas/3.4.267-c · DOI
  10. Benke, C., Alius, M. G., Hamm, A. O., & Pané-Farré, C. A. (2018). Cue and context conditioning to respiratory threat: Effects of suffocation fear and implications for the etiology of panic disorder. International Journal of Psychophysiology, 124, 33-42. doi:10.1016/j.ijpsycho.2018.01.002 · DOI
  11. Benke, C., Hamm, A. O., & Pané-Farré, C. A. (2017). When dyspnea gets worse: Suffocation fear and the dynamics of defensive respiratory responses to increasing interoceptive threat. Psychophysiology, 54(9), 1266-1283. doi:10.1111/psyp.12881 · DOI
  12. Biber, B., & Alkln, T. (1999). Panic disorder subtypes: differential responses to CO2 challenge. American Journal of Psychiatry, 156(5), 739-744.
  13. Blechert, J., Wilhelm, F. H., Meuret, A. E., Wilhelm, E. M., & Roth, W. T. (2013). Experiential, autonomic, and respiratory correlates of CO2 reactivity in individuals with high and low anxiety sensitivity. Psychiatry research, 209(3), 566-573. doi:10.1016/j.psychres.2013.02.010 · DOI
  14. Boettcher, H., & Barlow, D. H. (2018). The unique and conditional effects of interoceptive exposure in the treatment of anxiety: A functional analysis. Behaviour research and therapy. doi:10.1016/j.brat.2018.12.002 · DOI
  15. Bouton, M. E., Mineka, S., & Barlow, D. H. (2001). A modern learning theory perspective on the etiology of panic disorder. Psychological Review, 108(1), 4-32. doi:10.1037/0033- 295x.108.1.4 · DOI · Paper page
  16. Broocks, A., Meyer, T. F., Bandelow, B., George, A., Bartmann, U., Rüther, E., & Hillmer- Vogel, U. (1997). Exercise avoidance and impaired endurance capacity in patients with panic disorder. Neuropsychobiology, 36(4), 182-187. doi:10.1159/000119381 · DOI
  17. Brown, L. A., & Craske, M. G. (2017). Panic Disorder and Agoraphobia. Treatments for Psychological Problems and Syndromes, 34-55. doi:10.1002/9781118877142.ch4 · DOI
  18. Burger, A. M., Verkuil, B., Fenlon, H., Thijs, L., Cools, L., Miller, H. C., ... & Van Diest, I. (2017). Mixed evidence for the potential of non-invasive transcutaneous vagal nerve stimulation to improve the extinction and retention of fear. Behaviour research and therapy, 97, 64-74. doi:10.1016/j.brat.2017.07.005 · DOI
  19. Cameron, O. G. (2001). Interoception: the inside story-a model for psychosomatic processes. Psychosomatic medicine, 63(5), 697-710. doi:10.1097/00006842-200109000- 00001 · DOI · Paper page
  20. Campbell, D., Sanderson, R. E., & Laverty, S. G. (1964). Characteristics of a conditioned response in human subjects during extinction trials following a single traumatic conditioning trial. The Journal of Abnormal and Social Psychology, 68(6), 627-639. doi:10.1037/h0042582 · DOI
  21. Ceunen, E., Vlaeyen, J. W., & Van Diest, I. (2013). Atypical modulation of startle in women in face of aversive bodily sensations. International journal of psychophysiology, 88(2), 157-163. doi:10.1016/j.ijpsycho.2013.03.013 · DOI
  22. Ceunen, E., Zaman, J., Herssens, N., Van Oudenhove, L., Bogaerts, K., Ly, H. G., ... & Van Diest, I. (2015). Startle responding in the context of visceral pain. International journal of psychophysiology, 98(1), 128-134. doi:10.1016/j.ijpsycho.2015.07.009 · DOI
  23. Cook, E. W., Hodes, R. L., & Lang, P. J. (1986). Preparedness and phobia: effects of stimulus content on human visceral conditioning. Journal of abnormal psychology, 95(3), 195. doi:10.1037/0021-843x.95.3.195 · DOI
  24. Coplan, J. D., Moreau, D., Chaput, F., Martinez, J. M., Hoven, C. W., Mandell, D. J., Gorman, J. M., & Pine, D. S. (2002). Salivary cortisol concentrations before and after carbon-dioxide inhalations in children. Biological Psychiatry, 51(4), 326-333. doi:10.1016/s0006-3223(01)01250-1 · DOI
  25. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature reviews neuroscience, 3(8), 655. doi:10.1038/nrn894 · DOI · Paper page
  26. De Cort, K., Griez, E., Büchler, M., & Schruers, K. (2012). The role of "interoceptive" fear conditioning in the development of panic disorder. Behavior therapy, 43(1), 203-215. doi:10.1016/j.beth.2011.06.005 · DOI
  27. Denot-Ledunois, S., Vardon, G., Perruchet, P., & Gallego, J. (1998). The effect of attentional load on the breathing pattern in children. International journal of psychophysiology, 29(1), 13-21. doi:10.1016/s0167-8760(97)00086-x · DOI
  28. De Houwer, J., & Beckers, T. (2002). A review of recent developments in research and theories on human contingency learning. The Quarterly Journal of Experimental Psychology: Section B, 55(4), 289-310. doi:10.1080/02724990244000034 · DOI
  29. Domjan, M. (2005). Pavlovian Conditioning: A Functional Perspective. Annual Review of Psychology, 56(1), 179-206. doi:10.1146/annurev.psych.55.090902.141409 · DOI
  30. Domjan, M., Blesbois, E., & Williams, J. (1998). The adaptive significance of sexual conditioning: Pavlovian control of sperm release. Psychological Science, 9(5), 411-415. doi:10.1111/1467-9280.00077 · DOI
  31. Dworkin, B. R. (1993). Learning and physiological regulation. University of Chicago Press.
  32. Dworkin, B. R., & Dworkin, S. (1995). Learning of physiological responses: II. Classical conditioning of the baroreflex. Behavioral Neuroscience, 109(6), 1119-1136. doi:10.1037/0735-7044.109.6.1119 · DOI
  33. Esquivel, G., Schruers, K., Maddock, R., Colasanti, A., & Griez, E. (2010). Review: Acids in the brain: a factor in panic? Journal of Psychopharmacology, 24(5), 639-647. doi:10.1177/0269881109104847 · DOI
  34. Esser, R. W., Stoeckel, M. C., Kirsten, A., Watz, H., Taube, K., Lehmann, K., ... & von Leupoldt, A. (2017). Brain activation during perception and anticipation of dyspnea in chronic obstructive pulmonary disease. Frontiers in physiology, 8, 617. doi:10.3389/fphys.2017.00617 · DOI
  35. Fanselow, M. S., & Pennington, Z. T. (2018). A return to the psychiatric dark ages with a two-system framework for fear. Behaviour Research and Therapy, 100, 24-29. doi:10.1016/j.brat.2017.10.012 · DOI
  36. Fannes, S., Van Diest, I., Meulders, A., De Peuter, S., Vansteenwegen, D., & Van den Bergh, O. (2008). To inhale or not to inhale: Conditioned avoidance in breathing behavior in an odor-20% CO 2 paradigm. Biological Psychology, 78(1), 87-92. doi:10.1016/j.biopsycho.2008.01.003 · DOI
  37. Fava, G. A., & Sonino, N. (2010). Psychosomatic Medicine. The International Journal of Clinical Practice, 64, 1155-1161. doi:10.1111/j.1742-1241.2009.02266.x · DOI
  38. Ferbinteanu, J. (2019). Memory systems 2018 -Towards a new paradigm. Neurobiology of Learning and Memory, 157, 61-78. doi:10.1016/j.nlm.2018.11.005 · DOI
  39. Finlay, C. G., & Forsyth, J. P. (2009). Context and renewal of conditioned fear: An experimental evaluation using 20% carbon dioxide-enriched air as an unconditioned stimulus. Journal of anxiety disorders, 23(6), 737-745. doi:10.1016/j.janxdis.2009.02.014 · DOI
  40. Flink, I. K., Nicholas, M. K., Boersma, K., & Linton, S. J. (2009). Reducing the threat value of chronic pain: A preliminary replicated single-case study of interoceptive exposure versus distraction in six individuals with chronic back pain. Behaviour research and therapy, 47(8), 721-728. doi:10.1016/j.brat.2009.05.003 · DOI
  41. Fokkema, D. S. (1999). The psychobiology of strained breathing and its cardiovascular implications: A functional system review. Psychophysiology, 36, 164-175. doi:10.1111/1469-8986.3620164 · DOI
  42. Forsyth, J. P., & Eifert, G. H. (1998). Response intensity in content-specific fear conditioning comparing 20% versus 13% CO2-enriched air as unconditioned stimuli. Journal of Abnormal Psychology, 107(2), 291-304. doi:10.1037/0021-843x.107.2.291 · DOI
  43. Forsyth, J. P., Eifert, G. H., & Thompson, R. N. (1996). Systemic alarms in fear conditioning II: An experimental methodology using 20% carbon dioxide inhalation as an unconditioned stimulus. Behavior Therapy, 27(3), 391-415. doi:10.1016/s0005- 7894(96)80024-4 · DOI
  44. Gallego, J., & Perruchet, P. (1991). Classical conditioning of ventilatory responses in humans. Journal of Applied Physiology, 70(2), 676-682. doi:10.1152/jappl.1991.70.2.676 · DOI
  45. Garcia, J., Hankins, W.G., & Rusiniak, K.W. (1974). Behavioral regulation of the milieu interne in man and rat. Science 185, 824-831. doi:10.1126/science.185.4154.824 · DOI
  46. Garcia, J., & Koelling, R. A. (1966). Relation of cue to consequence in avoidance learning. Psychonomic science, 4(1), 123-124. doi:10.3758/bf03342209 · DOI
  47. Gardner, W. N. (1996). The pathophysiology of hyperventilation disorders. Chest, 109(2), 516-534. doi:10.1378/chest.109.2.516 · DOI · Paper page
  48. Giannese, F., Luchetti, A., Barbiera, G., Lampis, V., Zanettini, C., Knudsen, G. P., ... & Battaglia, M. (2018). Conserved DNA Methylation Signatures in Early Maternal Separation and in Twins Discordant for CO 2 Sensitivity. Scientific reports, 8(1), 2258. doi:10.1038/s41598-018-20457-3 · DOI
  49. Goddard, M. J. (1999). The role of US signal value in contingency, drug conditioning, and learned helplessness. Psychonomic bulletin & review, 6(3), 412-423. doi:10.3758/bf03210829 · DOI
  50. Hamm, A. O., & Vaitl, D. (1996). Affective learning: Awareness and aversion. Psychophysiology, 33(6), 698-710. doi:10.1111/j.1469-8986.1996.tb02366.x · DOI · Paper page
  51. Han, J. N., Stegen, K., De Valck, C., Clement, J., & Van de Woestijne, K. P. (1996). Influence of breathing therapy on complaints, anxiety and breathing pattern in patients with hyperventilation syndrome and anxiety disorders. Journal of psychosomatic research, 41(5), 481-493. doi:10.1016/s0022-3999(96)00220-6 · DOI · Paper page
  52. Haroutunian, V., & Campbell, B. A. (1979). Emergence of interoceptive and exteroceptive control of behavior in rats. Science, 205(4409), 927-929. doi:10.1126/science.472715 · DOI
  53. Hegel, M. T., & Ferguson, R. J. (1997). Psychophysiological assessment of respiratory function in panic disorder: Evidence for a hyperventilation subtype. Psychosomatic Medicine, 59, 224-230. doi:10.1097/00006842-199705000-00003 · DOI · Paper page
  54. Hodes, R. L., Cook, E. W., & Lang, P. J. (1985). Individual differences in autonomic response: conditioned association or conditioned fear? Psychophysiology, 22(5), 545-560. doi:10.1111/j.1469-8986.1985.tb01649.x · DOI
  55. Hofer, M. A., & Hinkle Jr., L. E. (1964). Conditioned diuresis in man: Effects of altered environment, subjective state, and conditioning Experience. Psychosomatic medicine, 26(2), 108-124. doi:10.1097/00006842-196403000-0000 · DOI
  56. Hugdahl, K. (1981). The three-systems-model of fear and emotion-a critical examination. Behaviour Research and Therapy, 19(1), 75-83. doi:10.1016/0005-7967(81)90114-5 · DOI
  57. Kessler, R. C., Chiu, W. T., Jin, R., Ruscio, A. M., Shear, K., & Walters, E. E. (2006). The epidemiology of panic attacks, panic disorder, and agoraphobia in the National Comorbidity Survey Replication. Archives of general psychiatry, 63(4), 415-424. doi:10.1001/archpsyc.63.4.415 · DOI · Paper page
  58. Krause, E., Benke, C., Koenig, J., Thayer, J. F., Hamm, A. O., & Pané-Farré, C. A. (2018). Dynamics of Defensive Response Mobilization to Approaching External Versus Interoceptive Threat. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(6), 525-538. doi:10.1016/j.bpsc.2017.12.002 · DOI
  59. Krause, M. A., & Domjan, M. (2017). Ethological and evolutionary perspectives on Pavlovian conditioning. APA Handbook of Comparative Psychology. Vol 2. Perception, Learning, and Cognition, 247-266. doi:10.1037/0000012-012 · DOI
  60. Lang, P. J., & Bradley, M. M. (2013). Appetitive and defensive motivation: Goal-directed or goal-determined?. Emotion Review, 5(3), 230-234. doi:10.1177/1754073913477511 · DOI
  61. Lang, P. J., Wangelin, B. C., Bradley, M. M., Versace, F., Davenport, P. W., & Costa, V. D. (2011). Threat of suffocation and defensive reflex activation. Psychophysiology, 48(3), 393-396. doi:10.1111/j.1469-8986.2010.01076.x · DOI
  62. Lavietes, M. H., Sanchez, C. W., Tiersky, L. A., Cherniack, N. S., & Natelson, B. H. (2000). Psychological profile and ventilatory response to inspiratory resistive loading. American journal of respiratory and critical care medicine, 161(3), 737-744. doi:10.1164/ajrccm.161.3.9810075 · DOI
  63. Lee, K., Noda, Y., Nakano, Y., Ogawa, S., Kinoshita, Y., Funayama, T., & Furukawa, T. A. (2006). Interoceptive hypersensitivity and interoceptive exposure in patients with panic disorder: specificity and effectiveness. BMC psychiatry, 6(1), 32. doi:10.1186/1471-244x- 6-32 · DOI
  64. Leibold, N. K., van den Hove, D. L. A., Esquivel, G., De Cort, K., Goossens, L., Strackx, E., ... & Schruers, K. R. J. (2015). The brain acid-base homeostasis and serotonin: A perspective on the use of carbon dioxide as human and rodent experimental model of panic. Progress in neurobiology, 129, 58-78. doi:10.1016/j.pneurobio.2015.04.001 · DOI
  65. Leibold, N. K., van den Hove, D. L., Viechtbauer, W., Kenis, G., Goossens, L., Lange, I., ... & Schruers, K. R. (2017). Amiloride-sensitive cation channel 2 genotype affects the response to a carbon dioxide panic challenge. Journal of Psychopharmacology, 31(10), 1294-1301. doi:10.1177/0269881116686880 · DOI
  66. Leibold, N. K., Viechtbauer, W., Goossens, L., De Cort, K., Griez, E. J., Myin-Germeys, I., ... & Schruers, K. R. (2013). Carbon dioxide inhalation as a human experimental model of panic: the relationship between emotions and cardiovascular physiology. Biological psychology, 94(2), 331-340. doi:10.1016/j.biopsycho.2013.06.004 · DOI
  67. Limebeer, C. L., Krohn, J. P., Cross-Mellor, S., Litt, D. E., Ossenkopp, K. P., & Parker, L. A. (2008). Exposure to a context previously associated with nausea elicits conditioned gaping in rats: a model of anticipatory nausea. Behavioural brain research, 187(1), 33-40. doi:10.1016/j.bbr.2007.08.024 · DOI
  68. Lovibond, P. F., & Shanks, D. R. (2002). The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. Journal of Experimental Psychology: Animal Behavior Processes, 28(1), 3. doi:10.1037/0097-7403.28.1.3 · DOI
  69. Löw, A., Weymar, M., & Hamm, A. O. (2015). When threat is near, get out of here: Dynamics of defensive behavior during freezing and active avoidance. Psychological science, 26(11), 1706-1716. doi:10.1177/0956797615597332 · DOI
  70. Masaoka, Y., & Homma, I. (1999). Expiratory time determined by individual anxiety levels in humans. Journal of Applied Physiology, 86(4), 1329-1336. doi:10.1152/jappl.1999.86.4.1329 · DOI
  71. McNally, R. J., & Eke, M. (1996). Anxiety sensitivity, suffocation fear, and breath-holding duration as predictors of response to carbon dioxide challenge. Journal of Abnormal Psychology, 105(1), 146-149. doi:10.1037/0021-843x.105.1.146 · DOI
  72. Melzig, C. A., Holtz, K., Michalowski, J. M., & Hamm, A. O. (2011). Interoceptive threat leads to defensive mobilization in highly anxiety sensitive persons. Psychophysiology, 48(6), 745-754. doi:10.1111/j.1469-8986.2010.01150. · DOI
  73. Meuret, A. E., Ritz, T., Wilhelm, F. H., Roth, W. T., & Rosenfield, D. (2018). Hypoventilation therapy alleviates panic by repeated induction of dyspnea. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 3(6), 539-545. doi:10.1016/j.bpsc.2018.01.010 · DOI
  74. Meuret, A. E., Rosenfield, D., Wilhelm, F. H., Zhou, E., Conrad, A., Ritz, T., & Roth, W. T. (2011). Do unexpected panic attacks occur spontaneously? Biological psychiatry, 70(10), 985-991. doi:10.1016/j.biopsych.2011.05.027 · DOI
  75. Miskovic, V., & Keil, A. (2012). Acquired fears reflected in cortical sensory processing: a review of electrophysiological studies of human classical conditioning. Psychophysiology, 49(9), 1230-1241. doi:10.1111/j.1469-8986.2012.01398. · DOI
  76. Mitte, K. (2005). A meta-analysis of the efficacy of psycho-and pharmacotherapy in panic disorder with and without agoraphobia. Journal of affective disorders, 88(1), 27-45. doi:10.1016/j.jad.2005.05.003 · DOI
  77. Moessnang, C., Pauly, K., Kellermann, T., Krämer, J., Finkelmeyer, A., Hummel, T., ... & Habel, U. (2013). The scent of salience-Is there olfactory-trigeminal conditioning in humans?. Neuroimage, 77, 93-104. doi:10.1016/j.neuroimage.2013.03.049 · DOI
  78. Mongeluzi, D. L., Rosellini, R. A., Ley, R., Caldarone, B. J., & Stock, H. S. (2003). The conditioning of dyspneic suffocation fear: effects of carbon dioxide concentration on behavioral freezing and analgesia. Behavior modification, 27(5), 620-636. doi:10.1177/0145445503256316 · DOI
  79. Moratti, S., Keil, A., & Miller, G. A. (2006). Fear but not awareness predicts enhanced sensory processing in fear conditioning. Psychophysiology, 43(2), 216-226. doi:10.1111/j.1464-8986.2006.00386 · DOI
  80. Pain, M. C. F., Biddle, N., & Tiller, J. W. G. (1988). Panic disorder, the ventilatory response to carbon dioxide and respiratory variables. Psychosomatic Medicine, 50, 541- 548. doi:10.1097/00006842-198809000-00010 · DOI
  81. Pappens, M., De Peuter, S., Vansteenwegen, D., Van den Bergh, O., & Van Diest, I. (2012a). Psychophysiological responses to CO2 inhalation. International journal of psychophysiology, 84(1), 45-50. doi:10.1016/j.ijpsycho.2012.01.008 · DOI
  82. Pappens, M., Schroijen, M., Van den Bergh, O., & Van Diest, I. (2015a). Retention of perceptual generalization of fear extinction. International Journal of Psychophysiology, 98(3), 520-528. doi:10.1016/j.ijpsycho.2015.01.007 · DOI
  83. Pappens, M., Smets, E., Bergh, O., & Van Diest, I. (2012b). Fear of suffocation alters respiration during obstructed breathing. Psychophysiology, 49(6), 829-832. doi:10.1111/j.1469-8986.2012.01355. · DOI
  84. Pappens, M., Smets, E., Vansteenwegen, D., Van den Bergh, O., & Van Diest, I. (2012c). Learning to fear suffocation: a new paradigm for interoceptive fear conditioning. Psychophysiology, 49(6), 821-828. doi:10.1111/j.1469-8986.2012.01357 · DOI
  85. Pappens, M., Van den Bergh, O., De Peuter, S., Bresseleers, J., Vansteenwegen, D., & Van Diest, I. (2010). Defense reactions to interoceptive threats: a comparison between loaded breathing and aversive picture viewing. Biological psychology, 84(1), 98-103. doi:10.1016/j.biopsycho.2010.02.006 · DOI
  86. Pappens, M., Van den Bergh, O., Vansteenwegen, D., Ceunen, E., De Peuter, S., & Van Diest, I. (2013). Learning to fear obstructed breathing: comparing interoceptive and exteroceptive cues. Biological psychology, 92(1), 36-42. doi:10.1016/j.biopsycho.2011.05.004 · DOI
  87. Pappens, M., Van den Bergh, O., Vansteenwegen, D., & Van Diest, I. (2011). Psychophysiological responses to inspiratory resistive loads. International Journal of Psychophysiology, 80(2), 161-165. doi:10.1016/j.ijpsycho.2011.02.015 · DOI
  88. Pappens, M., Vandenbossche, E., Van den Bergh, O., & Van Diest, I. (2015b). Interoceptive fear learning to mild breathlessness as a laboratory model for unexpected panic attacks. Frontiers in psychology, 6, 1150. doi: 10.3389/fpsyg.2015.01150 · DOI
  89. Perna G, Cocchi S, Bertani A, Arancio C, Bellodi L. Sensitivity to 35% CO 2 in healthy first- degree relatives of patients with panic disorder (1995). The American Journal of Psychiatry, 152, 623-625. doi:10.1176/ajp.152.4.623 · DOI
  90. Petzschner, F. H., Weber, L. A., Gard, T., & Stephan, K. E. (2017). Computational psychosomatics and computational psychiatry: Toward a joint framework for differential diagnosis. Biological psychiatry, 82(6), 421-430. doi:10.1016/j.biopsych.2017.05.012 · DOI · Paper page
  91. Pinkney, V., Wickens, R., Bamford, S., Baldwin, D. S., & Garner, M. (2014). Defensive eye-blink startle responses in a human experimental model of anxiety. Journal of Psychopharmacology, 28(9), 874-880. doi:10.1177/0269881114532858 · DOI
  92. Poon, C. S., Tin, C., & Yu, Y. (2007). Homeostasis of exercise hyperpnea and optimal sensorimotor integration: the internal model paradigm. Respiratory physiology & neurobiology, 159(1), 1-13. doi:10.1016/j.resp.2007.02.020 · DOI
  93. Radomsky, A. S., Rachman, S., Thordarson, D. S., McIsaac, H. K., & Teachman, B. A. (2001). The claustrophobia questionnaire. Journal of anxiety disorders, 15(4), 287-297. doi:10.1016/s0887-6185(01)00064-0 · DOI
  94. Rafferty, G. F., & Gardner, W. N. (1996). Control of the respiratory cycle in conscious humans. Journal of Applied Physiology, 81(4), 1744-1753. doi:10.1152/jappl.1996.81.4.1744 · DOI
  95. Rapee, R. M., Brown, T. A., Antony, M. M., & Barlow, D. H. (1992). Response to hyperventilation and inhalation of 5.5% carbon dioxide-enriched air across the DSM- III-R anxiety disorders. Journal of Abnormal Psychology, 101(3), 538 -552. doi:10.1037/0021-843x.101.3.538. · DOI · Paper page
  96. Rappaport, L. M., Sheerin, C., Savage, J. E., Hettema, J. M., & Roberson-Nay, R. (2017). Clinical characteristics of latent classes of CO 2 hypersensitivity in adolescents and young adults. Behaviour research and therapy, 93, 95-103. doi:10.1016/j.brat.2017.03.015 · DOI
  97. Rassovsky, Y., & Kushner, M. G. (2003). Carbon dioxide in the study of panic disorder: issues of definition, methodology and outcome. Anxiety Disorders, 17(1), 1-32. doi:10.1016/s0887-6185(02)00181-0 · DOI
  98. Rassovsky, Y., Kushner, M. G., Schwarze, N. J., & Wangensteen, D. O. (2000). Psychological and Physiological predictors of response to carbon dioxide challenge in individuals with panic disorder. Journal of Abnormal Psychology, 109(4), 616-623. doi:10.1037/0021-843x.109.4.616 · DOI
  99. Rau, H., Elbert, T., Lutzenberger, W., Eves, F., et al. (1988). Pavlovian conditioning of peripheral and central components of the baroreceptor reflex. Journal of Psychophysiology, 2(2), 119-127.
  100. Read, D. J. C. (1967). A clinical method for assessing the ventilatory response to carbon dioxide. Australasian annals of medicine, 16(1), 20-32. doi:10.1111/imj.1967.16.1.20 · DOI
  101. Resnik, J., Sobel, N., & Paz, R. (2011). Auditory aversive learning increases discrimination thresholds. Nature neuroscience, 14(6), 791. doi:10.1038/nn.2802 · DOI
  102. Rossi, V., Vanlessen, N., Bayer, M., Grass, A., Pourtois, G., & Schacht, A. (2017). Motivational salience modulates early visual cortex responses across task sets. Journal of Cognitive Neuroscience, 29(6), 968-979. doi:10.1162/jocn_a_01093 · DOI
  103. Sapienza, C. M., Davenport, P. W., & Martin, A. D. (2002). Expiratory muscle training increases pressure support in high school band students. Journal of Voice, 16(4), 495-501. doi:10.1016/s0892-1997(02)00125-x · DOI
  104. Sclafani, A., & Ackroff, K. (2012). Role of gut nutrient sensing in stimulating appetite and conditioning food preferences. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 302(10), R1119-R1133. doi:10.1152/ajpregu.00038.2012 · DOI
  105. Schmitz, A., & Grillon, C. (2012). Assessing fear and anxiety in humans using the threat of predictable and unpredictable aversive events (the NPU-threat test). Nature Protocols, 7(3), 527-532. doi:10.1038/nprot.2012.001 · DOI · Paper page
  106. Schroijen, M., Davenport, P., Van den Bergh, O., & Van Diest, I. (in press). Respiratory perception: From sensation to symptom. In J. E. Cotes, J. E., R. Maynard, B. Nemery, P. Wagnor, B. Cooper (Eds.), Lung function: physiology, measurement and application in medicine, 7th edition. Oxford: John Wiley & Sons.
  107. Schroijen, M., Fantoni, S., Rivera, C., Vervliet, B., Schruers, K., Van den Bergh, O., & Van Diest, I. (2016). Defensive activation to (un) predictable interoceptive threat: The NPU respiratory threat test (NPUr). Psychophysiology, 53(6), 905-913. doi:10.1111/psyp.12621 · DOI
  108. Schroijen, M., Pappens, M., Schruers, K., Van den Bergh, O., Vervliet, B., & Van Diest, I. (2015). Generalization of fear to respiratory sensations. Behavior therapy, 46(5), 611- 626. doi:10.1016/j.beth.2015.05.004 · DOI
  109. Schruers, K., Esquivel, G., van Duinen, M., Wichers, M., Kenis, G., Colasanti, A., ... & Smeets, H. (2011). Genetic moderation of CO2-induced fear by 5-HTTLPR genotype. Journal of psychopharmacology, 25(1), 37-42. doi:10.1177/0269881110372543 · DOI
  110. Seligman, M. E. (1971). Phobias and preparedness. Behavior therapy, 2(3), 307-320. doi:10.1016/s0005-7894(71)80064-3 · DOI
  111. Sevenster, D., Beckers, T., & Kindt, M. (2014). Fear conditioning of SCR but not the startle reflex requires conscious discrimination of threat and safety. Frontiers in behavioral neuroscience, 8, 32. doi:10.3389/fnbeh.2014.00032 · DOI · Paper page
  112. Siegel, S. (1989). Pharmacological conditioning and drug effects. In A. J. Goudie, & M. W. Emmett-Oglesby, Psychoactive drugs: Tolerance and sensitization . Clifton, NJ: Humana Press.
  113. Skinner, M. D., & Aubin, H. J. (2010). Craving's place in addiction theory: contributions of the major models. Neuroscience & Biobehavioral Reviews, 34(4), 606-623. https://doi.org/10.1016/j.neubiorev.2009.11.024 · DOI · Paper page
  114. Sinha, S., Papp, L. A., & Gorman, J. M. (2000). How study of respiratory physiology aided our understanding of abnormal brain function in panic disorder. Journal of Affective Disorders, 61, 191-200. doi:10.1016/s0165-0327(00)00337-2 · DOI
  115. Soeter, M., & Kindt, M. (2011). Noradrenergic enhancement of associative fear memory in humans. Neurobiology of learning and memory, 96(2), 263-271. doi:10.1016/j.nlm.2011.05.003 · DOI
  116. Somjen, G. G. (1992). The missing error signal-regulation beyond negative feedback. Physiology, 7(4), 184-185. doi:10.1152/physiologyonline.1992.7.4.184 · DOI
  117. Stegen, K., De Bruyne, K., Rasschaert, W., Van de Woestijne, K. P., & Van den Bergh, O. (1999). Fear-relevant images as conditioned stimuli for somatic complaints, respiratory behavior, and reduced end-tidal pCO₂. Journal of Abnormal Psychology, 108(1), 143- 152. doi:10.1037/0021-843x.108.1.143 · DOI
  118. Stekelenburg, J. J., & Van Boxtel, A. (2002). Pericranial muscular, respiratory, and heart rate components of the orienting response. Psychophysiology, 39(6), 707-722. doi:10.1111/1469-8986.3960707 · DOI
  119. Stockhorst, U., Steingrüber, H. J., & Scherbaum, W. A. (2000). Classically conditioned responses following repeated insulin and glucose administration in humans. Behavioural brain research, 110(1), 143-159. doi:10.1016/s0166-4328(99)00192-8 · DOI · Paper page
  120. Tansey, E. M. (2006). Pavlov at home and abroad: His role in international physiology. Autonomic Neuroscience, 125(1), 1-11. doi:10.1016/j.autneu.2006.01.013 · DOI
  121. Taugher, R. J., Lu, Y., Wang, Y., Kreple, C. J., Ghobbeh, A., Fan, R., ... & Wemmie, J. A. (2014). The bed nucleus of the stria terminalis is critical for anxiety-related behavior evoked by CO 2 and acidosis. Journal of Neuroscience, 34(31), 10247-10255. doi:10.1523/jneurosci.1680-14.2014 · DOI
  122. Telch, M. J., Jacquin, K., Smits, J. A. J., & Powers, M. B. (2003). Emotional responding to hyperventilation as a predictor of agoraphobia status among individuals suffering from panic disorder. Journal of Behavior Therapy, 34, 161-170. doi:10.1016/s0005- 7916(03)00037-5 · DOI
  123. Tipton, M. J., Harper, A., Paton, J. F., & Costello, J. T. (2017). The human ventilatory response to stress: rate or depth?. The Journal of physiology, 595(17), 5729-5752. doi:10.1113/jp274596 · DOI
  124. Uematsu, A., Tsurugizawa, T., Uneyama, H., & Torii, K. (2010). Brain-gut communication via vagus nerve modulates conditioned flavor preference. European Journal of Neuroscience, 31(6), 1136-1143. doi:10.1111/j.1460-9568.2010.07136.x · DOI
  125. Valdivia-Salas, S., Forsyth, J. P., Berghoff, C. R., & Ritzert, T. R. (2014). Using panicogenic inhalations of carbon dioxide enriched air to induce attentional bias for threat: Implications for the development of anxiety disorders. Cognition and Emotion, 28(8), 1474-1482. doi:10.1080/02699931.2014.883964 · DOI
  126. van Beek, N., & Griez, E. (2000). Reactivity to a 35% CO2 challenge in healthy first-degree relatives of patients with panic disorder. Biological Psychiatry, 47(9), 830-835. doi:10.1016/s0006-3223(99)00265-6 · DOI
  127. Van den Bergh, O., Kempynck, P. J., Van De Woestijne, K. P., Baeyens, F., & Eelen, P. (1995). Respiratory learning and somatic complaints: a conditioning approach using CO2-enriched air inhalation. Behaviour research and therapy, 33(5), 517-527. doi:10.1016/0005-7967(94)00080-4 · DOI
  128. Van den Hout, M. A., van der Molen, G. M., Griez, E., & Lousberg, H. (1987). Specificity of interoceptive fear to panic disorders. Journal of Psychopathology and Behavioral Assessment, 9(1), 99-106. doi:10.1007/bf00961635 · DOI
  129. Van der Molen, G. M., & van den Hout, M. A. (1988). Expectancy effects on respiration during lactate infusion. Psychosomatic Medicine, 50(4), 439-443. doi:10.1097/00006842- 198807000-00011 · DOI
  130. Van Diest, I. (2017). Interoceptive fear conditioning and generalization in panic disorder. Oral presentation at the Anxiety and Depression conference of the Anxiety & Depression Association of America (ADAA), San Francisco, April 2017.
  131. Van Diest, I., Bradley, M. M., Guerra, P., Van den Bergh, O., & Lang, P. J. (2009). Fear- conditioned respiration and its association to cardiac reactivity. Biological psychology, 80(2), 212-217. doi:10.1016/j.biopsycho.2008.09.006 · DOI
  132. Van Diest, I., De Peuter, S., Piedfort, K., Bresseleers, J., Devriese, S., Van de Woestijne, K. P., & Van den Bergh, O. (2006). Acquired lightheadedness in response to odors after hyperventilation. Psychosomatic medicine, 68(2), 340-347. doi:10.1097/01.psy.0000204782.49159. · DOI
  133. Van Diest, I., Proot, P., Van de Woestijne, K. P., Han, J. N., Devriese, S., Winters, W., & Van den Bergh, O. (2001a). Critical conditions for hyperventilation responses: The role of autonomic response propositions during emotional imagery. Behavior Modification, 25(4), 621-639. doi:10.1177/0145445501254008 · DOI
  134. Van Diest, I., Winters, W., Devriese, S., Vercamst, E., Han, J. N., Van de Woestijne, K. P., & Van den Bergh, O. (2001b). Hyperventilation beyond fight/flight: Respiratory responses during emotional imagery. Psychophysiology, 38, 961-968. doi:10.1111/1469- 8986.3860961 · DOI
  135. Vlemincx, E., Sprenger, C., & Büchel, C. (2017). A breath of air: Nocebo-effects in dyspnea. Biological Psychology, 129, 376. doi:10.1016/j.biopsycho.2017.08.023 · DOI
  136. Vollmer, L. L., Strawn, J. R., & Sah, R. (2015). Acid-base dysregulation and chemosensory mechanisms in panic disorder: a translational update. Translational psychiatry, 5(5), e572. doi:10.1038/tp.2015. · DOI
  137. von Leupoldt, A., Sommer, T., Kegat, S., Baumann, H. J., Klose, H., Dahme, B., & Büchel, C. (2008). The unpleasantness of perceived dyspnea is processed in the anterior insula and amygdala. American Journal of Respiratory and Critical Care Medicine, 177(9), 1026-1032. doi:10.1164/rccm.200712-1821oc · DOI · Paper page
  138. Wan, L., Van Diest, I., De Peuter, S., Bogaerts, K., Oyen, N., Hombroux, N., ... & Van den Bergh, O. (2008). Repeated experiences of air hunger and ventilatory behavior in response to hypercapnia in the standardized rebreathing test: effects of anxiety. Biological psychology, 77(2), 223-232. doi:10.1016/j.biopsycho.2007.10.013 · DOI
  139. Wendt, J., Neubert, J., Koenig, J., Thayer, J. F., & Hamm, A. O. (2015). Resting heart rate variability is associated with inhibition of conditioned fear. Psychophysiology, 52(9), 1161-1166. doi:10.1111/psyp.12456 · DOI · Paper page
  140. Wicrtelak, E. P., Smith, K. P., Furness, L., Mooney-Heiberger, K., Mayr, T., Maier, S. F., & Watkins, L. R. (1994). Acute and conditioned hyperalgesic responses to illness. Pain, 56(2), 227-234. doi:10.1016/0304-3959(94)90098-1 · DOI
  141. Wirth, T., Ober, K., Prager, G., Vogelsang, M., Benson, S., Witzke, O., ... & Schedlowski, M. (2011). Repeated recall of learned immunosuppression: evidence from rats and men. Brain, behavior, and immunity, 25(7), 1444-1451. doi:10.1016/j.bbi.2011.05.011 · DOI
  142. Wolpe, J., & Rowan, V. C. (1988). Panic disorder: A product of classical conditioning. Behaviour research and therapy, 26(6), 441-450. doi:10.1016/0005-7967(88)90138-6 · DOI
  143. Woods, S. W., Charney, D. S., Loke, J., Goodman, W., Redmond, D. E., & Heninger, G. R. (1986). Carbon dioxide sensitivity in panic anxiety. Archives of General Psychiatry, 43(9), 900. doi:10.1001/archpsyc.1986.01800090090013 · DOI
  144. Woods, S. C., & Ramsay, D. S. (2000). Pavlovian influences over food and drug intake. Behavioural brain research, 110(1), 175-182. doi:10.1016/s0166-4328(99)00194-1 · DOI
  145. Zaman, J., Van den Bergh, O., Fannes, S., & Van Diest, I. (2014). Learning to breathe? Feedforward regulation of the inspiratory motor drive. Respiratory physiology & neurobiology, 201, 1-6. doi:10.1016/j.resp.2014.05.009 · DOI
  146. Zaman, J., Vlaeyen, J. W., Van Oudenhove, L., Wiech, K., & Van Diest, I. (2015). Associative fear learning and perceptual discrimination: a perceptual pathway in the development of chronic pain. Neuroscience & Biobehavioral Reviews, 51, 118-125. doi:10.1016/j.neubiorev.2015.01.009 · DOI
  147. Zaman, J., Weltens, N., Ly, H. G., Struyf, D., Vlaeyen, J. W., Van den Bergh, O., ... & Van Diest, I. (2016). Influence of interoceptive fear learning on visceral perception. Psychosomatic medicine, 78(2), 248-258. doi:10.1097/psy.0000000000000257 · DOI
  148. Zandbergen, J., & Bright, M. (1991). Higher lifetime prevalence of respiratory diseases in panic disorder?. The American journal of psychiatry, 148(11), 1583-1585. doi:10.1176/ajp.148.11.1583 · DOI
  149. Ziemann, A. E., Allen, J. E., Dahdaleh, N. S., Drebot, I. I., Coryell, M. W., Wunsch, A. M., ... & Wemmie, J. A. (2009). The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell, 139(5), 1012-1021. doi:10.1016/j.cell.2009.10.029 · DOI
  150. Zinbarg, R., Brown, T., Barlow, D., & Rapee, R. (2001). Fear responses to hyperventilation and 5.5% carbon dioxide enriched air and anxiety sensitivity: A reanalysis of Rapee, Brown, Antony, & Barlow (1992). Journal of Abnormal Psychology, 10, 372-377.
  151. Zucker, N., Mauro, C., Craske, M., Wagner, H. R., Datta, N., Hopkins, H., ... & Mayer, E. (2017). Acceptance-based interoceptive exposure for young children with functional abdominal pain. Behaviour research and therapy, 97, 200-212. doi:10.1016/j.brat.2017.07.009 · DOI · Paper page
  152. Zvolensky, M. J. (2001). Evaluating differential predictions of emotional reactivity during repeated 20% carbon dioxide-enriched air challenge. Cognition and Emotion, 15( 6), 767- 786. doi:10.1080/02699930143000284 · DOI

Cited by

Sorted by citations

Authors
Van Diest, I.
Affiliations
Health, Behavior & Psychopathology, Faculty of Psychology & Educational Sciences University of Leuven Leuven Belgium
Venue
Psychophysiology
Publisher
Wiley
Published
2019-06-22
Volume
56
Issue
8
Pages
e13421-e13421
ISSN
  • 0048-5772 (ISSN-L)
  • 1469-8986
OpenAlex
W2951324233
Cited by
44
References
24
Citations by year
2026: 10 · 2025: 2 · 2024: 8 · 2023: 6 · 2022: 6 · 2021: 5 · 2020: 6 · 2019: 1
FWCI
0.67
Type
journal article
Language
en
Open access
Locations
  • Psychophysiology (publishedVersion)
  • PubMed (publishedVersion)
  • Lirias (KU Leuven) (submittedVersion, other-oa)
Funders
  • Research Foundation - Flanders, Belgium (G071918N, K802117N)
  • Flemish Government, Belgium (Meth/15/011)
Topics
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Health Sciences › Medicine › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
Keywords
interoception, interoceptive conditioning, panic disorder, fear conditioning, classical conditioning, physiological responses, emotional learning, perceptual learning
MeSH terms
Animals, Anxiety, Association Learning, Conditioning, Classical, Fear, Humans, Panic Disorder, Interoception

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review