Fear Conditioning in an Abdominal Pain Model: Neural Responses during Associative Learning and Extinction in Healthy Subjects

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Kattoor, Joswin ^a   Gizewski, Elke R ^b   Kotsis, Vassilios ^a   Benson, Sven ^a   Gramsch, Carolin ^a   Theysohn, Nina ^a   Maderwald, Stefan ^c   Forsting, Michael ^a   Schedlowski, Manfred ^a   Elsenbruch, Sigrid ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABDOMINAL PAIN; ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; AWARENESS; BRAIN FUNCTION; CLINICAL ARTICLE; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INSULA; MALE; MEMORY; NERVE POTENTIAL; PATHOPHYSIOLOGY; PRECUNEUS; PREFRONTAL CORTEX; RECTUM DISEASE; REINFORCEMENT; SOMATOSENSORY CORTEX; STATE DEPENDENT LEARNING; UNCONDITIONED STIMULI; VISUAL CONDITIONED STIMULI; VISUAL STIMULATION;

ABDOMINAL PAIN; ADULT; AMYGDALA; BRAIN; BRAIN MAPPING; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; YOUNG ADULT;

EID: 84874503646     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051149     Document Type: Article

References (56)

1. Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, et al. (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4: e5865.
2. Milad MR, Quirk GJ, (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63: 129-151.
3. Klosterhalfen S, Rüttgers A, Krumrey E, Otto B, Stockhorst U, et al. (2000) Pavlovian conditioning of taste aversion using a motion sickness paradigm. Psychosom Med 62: 671-677.
4. Stockhorst U, Enck P, Klosterhalfen S, (2007) Role of classical conditioning in learning gastrointestinal symptoms. World J Gastroenterol 13: 3430-3437.
5. De Peuter S, Van Diest I, Vansteenwegen D, Van den Bergh O, Vlaeyen JW, (2011) Understanding fear of pain in chronic pain: interoceptive fear conditioning as a novel approach. Eur J Pain 15: 889-894.
6. Yágüez L, Coen S, Gregory LJ, Amaro E, Altman C, et al. (2005) Brain response to visceral aversive conditioning: a functional magnetic resonance imaging study. Gastroenterology 128: 1819-1829.
7. Tyler K, Moriceau S, Sullivan RM, Greenwood-van Meerveld B, (2007) Long-term colonic hypersensitivity in adult rats induced by neonatal unpredictable vs predictable shock. Neurogastroenterol Motil 19: 761-768.
8. Wang Z, Bradesi S, Charles JR, Pang RD, Maarek JM, et al. (2011) Functional brain activation during retrieval of visceral pain-conditioned passive avoidance in the rat. Pain 152: 2746-2756.
9. Nozu T, Kudaira M, Kitamori S, Uehara A, (2006) Repetitive rectal painful distention induces rectal hypersensitivity in patients with irritable bowel syndrome. J Gastroenterol 41: 217-222.
10. Lembo T, Naliboff B, Munakata J, Fullerton S, Saba L, et al. (1999) Symptoms and visceral perception in patients with pain-predominant irritable bowel syndrome. Am J Gastroenterol 94: 1320-1326.
11. Nees F, Rüddel H, Mussgay L, Kuehl LK, Römer S, et al. (2010) Alteration of delay and trace eyeblink conditioning in fibromyalgia patients. Psychosom Med 72: 412-418.
12. Klinger R, Matter N, Kothe R, Dahme B, Hofmann UG, et al. (2010) Unconditioned and conditioned muscular responses in patients with chronic back pain and chronic tension-type headaches and in healthy controls. Pain 150: 66-74.
13. Bishop SJ, (2007) Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn Sci 11: 307-316.
14. Lissek S, Rabin SJ, McDowell DJ, Dvir S, Bradford DE, et al. (2009) Impaired discriminative fear-conditioning resulting from elevated fear responding to learned safety cues among individuals with panic disorder. Behav Res Ther 47: 111-118.
15. Lissek S, Rabin S, Heller RE, Lukenbaugh D, Geraci M, et al. (2010) Overgeneralization of conditioned fear as a pathogenic marker of panic disorder. Am J Psychiatry 167: 47-55.
16. Hermans D, Craske MG, Mineka S, Lovibond PF, (2006) Extinction in human fear conditioning. Biol Psychiatry 60: 361-368.
17. North CS, Hong BA, Alpers DH, (2007) Relationship of functional gastrointestinal disorders and psychiatric disorders: implications for treatment. World J Gastroenterol 13: 2020-2027.
18. Elsenbruch S, (2011) Abdominal pain in Irritable Bowel Syndrome: a review of putative psychological, neural and neuro-immune mechanisms. Brain Behav Immun 25: 386-394.
19. Quirk GJ, Paré D, Richardson R, Herry C, Monfils MH, et al. (2010) Erasing fear memories with extinction training. J Neurosci 30: 14993-14997.
20. LaBar KS, Phelps EA, (2005) Reinstatement of conditioned fear in humans is context dependent and impaired in amnesia. Behav Neurosci 119: 677-686.
21. Giovanello KS, Schnyer D, Verfaellie M, (2009) Distinct hippocampal regions make unique contributions to relational memory. Hippocampus 19: 111-117.
22. Hermans D, Dirikx T, Vansteenwegen D, Vansteenwegenin D, Baeyens F, et al. (2005) Reinstatement of fear responses in human aversive conditioning. Behav Res Ther 43: 533-551.
23. Schmajuk NA, Larrauri JA, Labar KS, (2007) Reinstatement of conditioned fear and the hippocampus: an attentional-associative model. Behav Brain Res 177: 242-253.
24. Vouimba RM, Maroun M, (2011) Learning-induced changes in mPFC-BLA connections after fear conditioning, extinction, and reinstatement of fear. Neuropsychopharmacology 36: 2276-2285.
25. Herrmann-Lingen C, Buss U, Snaith RP (2005) Hospital Anxiety and Depression Scale (HADS)- Deutsche Version (2. Auflage). Bern: Hans Huber.
26. Amaro E, Barker GJ, (2006) Study design in fMRI: basic principles. Brain Cogn 60: 220-232.
27. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH, (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239.
28. Benson S, Kotsis V, Rosenberger C, Bingel U, Forsting M, et al. (2012) Behavioural and neural correlates of visceral pain sensitivity in healthy men and women: Does sex matter? Eur J Pain 16: 349-358.
29. Elsenbruch S, Kotsis V, Benson S, Rosenberger C, Reidick D, et al. (2012) Neural mechanisms mediating the effects of expectation in visceral placebo analgesia: an fMRI study in healthy placebo responders and nonresponders. Pain 153: 382-390.
30. Elsenbruch S, Rosenberger C, Bingel U, Forsting M, Schedlowski M, et al. (2010) Patients with irritable bowel syndrome have altered emotional modulation of neural responses to visceral stimuli. Gastroenterology 139: 1310-1319.
31. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, et al. (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62: 757-771.
32. Büchel C, Morris J, Dolan RJ, Friston KJ, (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20: 947-957.
33. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA, (1998) Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20: 937-945.
34. Straube T, Weiss T, Mentzel HJ, Miltner WH, (2007) Time course of amygdala activation during aversive conditioning depends on attention. Neuroimage 34: 462-469.
35. Tabbert K, Stark R, Kirsch P, Vaitl D, (2005) Hemodynamic responses of the amygdala, the orbitofrontal cortex and the visual cortex during a fear conditioning paradigm. Int J Psychophysiol 57: 15-23.
36. Dunsmoor JE, Bandettini PA, Knight DC, (2007) Impact of continuous versus intermittent CS-UCS pairing on human brain activation during Pavlovian fear conditioning. Behav Neurosci 121: 635-642.
37. Dunsmoor JE, Bandettini PA, Knight DC, (2008) Neural correlates of unconditioned response diminution during Pavlovian conditioning. Neuroimage 40: 811-817.
38. Phelps EA, Delgado MR, Nearing KI, LeDoux JE, (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43: 897-905.
39. Fiddick L, (2011) There is more than the amygdala: potential threat assessment in the cingulate cortex. Neurosci Biobehav Rev 35: 1007-1018.
40. Rosenberger C, Elsenbruch S, Scholle A, de Greiff A, Schedlowski M, et al. (2009) Effects of psychological stress on the cerebral processing of visceral stimuli in healthy women. Neurogastroenterol Motil 21: 740-e745.
41. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, et al. (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12: 154-167.
42. Price DD, (2000) Psychological and neural mechanisms of the affective dimension of pain. Science 288: 1769-1772.
43. Davis KD, Taylor KS, Hutchison WD, Dostrovsky JO, McAndrews MP, et al. (2005) Human anterior cingulate cortex neurons encode cognitive and emotional demands. J Neurosci 25: 8402-8406.
44. Vogt BA, (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6: 533-544.
45. Labus JS, Naliboff BD, Berman SM, Suyenobu B, Vianna EP, et al. (2009) Brain networks underlying perceptual habituation to repeated aversive visceral stimuli in patients with irritable bowel syndrome. Neuroimage 47: 952-960.
46. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, et al. (2008) Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. J Neurosci 28: 349-359.
47. Worthen SF, Hobson AR, Hall SD, Aziz Q, Furlong PL, (2011) Primary and secondary somatosensory cortex responses to anticipation and pain: a magnetoencephalography study. Eur J Neurosci 33: 946-959.
48. Coen SJ, Kano M, Farmer AD, Kumari V, Giampietro V, et al. (2011) Neuroticism influences brain activity during the experience of visceral pain. Gastroenterology 141: 909-917.e901.
49. Hubbard CS, Labus JS, Bueller J, Stains J, Suyenobu B, et al. (2011) Corticotropin-releasing factor receptor 1 antagonist alters regional activation and effective connectivity in an emotional-arousal circuit during expectation of abdominal pain. J Neurosci 31: 12491-12500.
50. Schneider C, Palomba D, Flor H, (2004) Pavlovian conditioning of muscular responses in chronic pain patients: central and peripheral correlates. Pain 112: 239-247.
51. Flor H, Knost B, Birbaumer N, (2002) The role of operant conditioning in chronic pain: an experimental investigation. Pain 95: 111-118.
52. Van Damme S, Crombez G, Eccleston C, Koster EH, (2006) Hypervigilance to learned pain signals: a componential analysis. J Pain 7: 346-357.
53. Ljótsson B, Andersson G, Andersson E, Hedman E, Lindfors P, et al. (2011) Acceptability, effectiveness, and cost-effectiveness of internet-based exposure treatment for irritable bowel syndrome in a clinical sample: a randomized controlled trial. BMC Gastroenterol 11: 110.
54. Bouton ME, (2004) Context and behavioral processes in extinction. Learn Mem 11: 485-494.
55. Norberg MM, Krystal JH, Tolin DF, (2008) A meta-analysis of D-cycloserine and the facilitation of fear extinction and exposure therapy. Biol Psychiatry 63: 1118-1126.
56. Craske MG, Wolitzky-Taylor KB, Labus J, Wu S, Frese M, et al. (2011) A cognitive-behavioral treatment for irritable bowel syndrome using interoceptive exposure to visceral sensations. Behav Res Ther 49: 413-421.