Gastroenterology
Volume 128, Issue 7 , Pages 1819-1829 , June 2005

Brain Response to Visceral Aversive Conditioning: A Functional Magnetic Resonance Imaging Study

  • Lidia Yágüez

      Affiliations

    • Department of Psychology, Institute of Psychiatry, King’s College, London, United Kingdom
    • Corresponding Author InformationAddress requests for reprints to: Lidia Yágüez, PhD, Department of Psychology, P077, HWB, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, United Kingdom. fax: (44) 0-20-7848-5006.
  • ,
  • Steven Coen

      Affiliations

    • Centre for Neuroimaging Sciences, Institute of Psychiatry, King’s College, London, United Kingdom
  • ,
  • Lloyd J. Gregory

      Affiliations

    • Section of GI Sciences, University of Manchester, Manchester, United Kingdom
  • ,
  • Edson Amaro Jr

      Affiliations

    • Centre for Neuroimaging Sciences, Institute of Psychiatry, King’s College, London, United Kingdom
  • ,
  • Christian Altman

      Affiliations

    • Department of Psychology, Institute of Psychiatry, King’s College, London, United Kingdom
  • ,
  • Michael J. Brammer

      Affiliations

    • Department of Biostatistics, Institute of Psychiatry, King’s College, London, United Kingdom
  • ,
  • Edward T. Bullmore

      Affiliations

    • Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom
  • ,
  • Steven C.R. Williams

      Affiliations

    • Centre for Neuroimaging Sciences, Institute of Psychiatry, King’s College, London, United Kingdom
  • ,
  • Qasim Aziz

      Affiliations

    • Department of Biostatistics, Institute of Psychiatry, King’s College, London, United Kingdom

Received 1 March 2004 ,Accepted 23 February 2005.

References 

  1. Ploghhaus A , Tracey I , Clare S , Gati JS , Rawlins NP , Matthews PM . Learning about pain (the neural substrate of the prediction error for aversive events) . Proc Natl Acad Sci U S A . 2000;97:9281–9286
  2. Aziz Q, Thompson DG, Ng VWK, Hamdy S, Sarkar S, Brammer MJ, et al. Cortical processing of human somatic and visceral sensation . J Neurosci . 2000;20:2657–2663
  3. Strigo IA , Duncan GH , Boivin M , Bushnell MC . Differentiation of visceral and cutaneous pain in the human brain . J Neurophysiol . 2003;89:3294–3303
  4. Drevets WC , Burton H , Videen TO , Snyder AZ , Simpson JR , Raichle ME . Blood flow changes in human somatosensory cortex during anticipated stimulation . Nature . 1995;373:249–252
  5. Chua P , Kraus M , Toni I , Passingham R , Dolan R . A functional anatomy of anticipatory anxiety . Neuroimage . 1999;9:563–571
  6. Hsieh JC , Stone-Elander S , Ingvar M . Anticipatory coping of pain expressed in the human anterior cingulate cortex (a positron emission tomography study) . Neurosci Lett . 1999;262:61–64
  7. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, et al. Dissociating pain from its anticipation in the human brain . Science . 1999;284:1979–1981
  8. Porro CA, Baraldi P, Pagnoni G, Serafini M, Facchin P, Maieron M, et al. Does anticipation of pain affect cortical nociceptive systems? . J Neurosci . 2002;22:3206–3214
  9. Aziz Q , Anderson JLR , Valin S . Identification of human brain loci processing oesophageal sensation using positron emission tomography . Gastroenterology . 1997;113:50–59
  10. Silverman DHS , Munakata JA , Ennes H , Mandelkern MA , Hoh CK , Mayer EA . Regional cerebral activity in normal and pathological perception of visceral pain . Gastroenterology . 1997;112:64–72
  11. Merz H, Morgan V, Tanner G, Pickens D, Price R, Shyr Y, et al. Regional cerebral activation in irritable bowel syndrome and control subjects with painful and nonpainful rectal distension . Gastroenterology . 2000;118:842–848
  12. Derbyshire SW . A systematic review of neuroimaging data during visceral stimulation . Am J Gastroenterol . 2003;98:12–20
  13. Pavlov IP . Conditioned reflexes . New York: Dover; 1927;
  14. Bykov KM . In:  Gantt WH editors. The cerebral cortex and the internal organs . New York: Chemical Publishing; 1957; trans
  15. Brammer MJ, Bullmore ET, Simmons A, Williams SCR, Grasby PM, Howard RJ, et al. Generic brain activation mapping in fMRI (a nonparametric approach) . Magn Reson Imaging . 1997;15:763–770
  16. Bullmore ET, Brammer MJ, Rabe-Hesketh S, Curtis V, Morris RG, Williams SCR, et al. Methods for diagnosis and treatment of stimulus-correlated motion in generic brain activation studies using fMRI . Hum Brain Mapp . 1999;7:38–48
  17. Friman O , Borga M , Lundberg P , Knutsson H . Adaptive analysis of fMRI data . Neuroimage . 2003;19:837–845
  18. Bullmore E, Long C, Suckling J, Fadili J, Calvert G, Zelaya F, et al. Colored noise and computational inference in neurophysiological (fMRI) time series analysis (resampling methods in time and wavelet domains) . Hum Brain Mapp . 2001;12:61–78
  19. Talairach J , Tournoux P . A coplanar stereotactic atlas of the human brain . New York: Thieme; 1988;
  20. Hobday DI , Aziz Q , Thacker N , Hollander I , Jackson A , Thompson DG . A study of the cortical processing of ano-rectal sensation using functional MRI . Brain . 2001;124:361–368
  21. Casey KL , Minoshima S , Berger KL , Koeppe RA , Morrow TJ , Frey KA . Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli . J Neurophysiol . 1994;71:802–807
  22. Jones AKP , Brown WD , Frison KJ , Qi LY , Frackowiak RSJ . Cortical and subcortical localization of response to pain in man using positron emission tomography . Proc R Soc Lond B . 1991;244:39–44
  23. Talbot JD , Marrett S , Evans AC , Meyer E , Bushnell MC , Duncan GH . Multiple representations of pain in human cerebral cortex . Science . 1991;251:1355–1358
  24. Craig AD , Reiman EM , Evans A , Bunshell MC . Functional imaging of an illusion of pain . Nature . 1996;384:258–260
  25. Peyron R, García-Larrea L, Grégorie MC, Costes N, Convers P, Lavenne F, et al. Haemodynamic brain responses to acute pain in humans (sensory and attentional networks) . Brain . 1999;122:1765–1779
  26. Devinsky O , Morrell MJ , Vogt BA . Contributions of anterior cingulate cortex to behaviour . Brain . 1995;118:279–306
  27. Davis KD , Taylor SJ , Crawley AP , Wood ML , Mikulis DJ . Functional MRI of pain and attention-related activations in the human cingulate cortex . J Neurophysiol . 1997;77:3370–3380
  28. Rainville P , Duncan GH , Price DD , Carrier B , Bushnell MC . Pain affect encoded in human anterior cingulate but not somatosensory cortex . Science . 1997;277:968–971
  29. Derbyshire SWG , Vogt BA , Jones AKP . Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex . Exp Brain Res . 1998;118:52–60
  30. Gregory LJ, Yágüez L, Williams SCR, Altmann C, Coen SJ, Ng V, et al. Cognitive modulation of the cerebral processing of human oesophageal sensation using functional magnetic resonance imaging . Gut . 2003;52:1671–1677
  31. Peyron R , Laurent B , García-Larrea L . Functional imaging of brain responses to pain. A review and meta-analysis . Neurophysiol Clin . 2000;30:263–288
  32. Baron R , Baron Y , Disbrow E , Roberts TPL . Brain processing of capsaicin-induced secondary hyperalgesia. A functional MRI study . Neurology . 1999;53:548–557
  33. Becerra LR, Breiter HC, Stojanovic M, Fishman S, Edwards A, Comite AR, et al. Human brain activation under controlled thermal stimulation and habituation to noxious heat (an fMRI study) . Magn Reson Med . 1999;41:1044–1057
  34. Passingham RE , Toni I , Rushworth MF . Specialisation within the prefrontal cortex (the ventral prefrontal cortex and associative learning) . Exp Brain Res . 2000;133:103–113
  35. Ueda K , Okamoto Y , Okada G , Yamashita H , Hori T , Yamawaki S . Brain activity during expectancy of emotional stimuli (an fMRI study) . Neuroreport . 2003;14:51–55
  36. Steinmetz JE , Lavond DG , Ivkovich D , Logan CG , Thompson RF . Disruption of classical eyelid conditioning after cerebellar lesions (damage to the memory trace system or a simple performance deficit?) . J Neurosci . 1992;12:4403–4426
  37. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, et al. Distributed processing of pain and vibration by the human brain . J Neurosci . 1994;14:4095–4108
  38. Baciu MV, Bonaz BL, Papillon E, Bost R, Le Bas JF, Fournet J, et al. Central processing of rectal pain (a functional MR imaging study) . Am J Neuroradiol . 1999;20:1920–1924
  39. Kornhuber HH , Deecke L , Lang M , Kornhuber A . Will, volitional actions, attention and cerebral potentials in man (Bereitschaftspotential, performance related potentials, directed attention potential and EEG spectrum changes) . In:  Hersberger W editors. Volitional actions. Advances in psychology . 62: Amsterdam: North Holland; 1989;p. 107–168
  40. Deecke L . Bereitschaftspotential as an indicator of movement preparation in supplementary motor area and motor cortex . In:  Bock M ,  O’Connor M ,  Marsh J editor. Motor areas of the cerebral cortex. Ciba Foundation Symposium . Chichester: John Wiley; 1987;p. 231–250
  41. Blair RJR , Morris JS , Frith CD , Perret DI , Dolan RJ . Dissociable neural response to facial expression of sadness and anger . Brain . 1999;122:883–893
  42. Breiter H, Rauch SL, Kwong KK, Baker JR, Weisskoff RM, Kennedy DN, et al. Functional magnetic resonance imaging of symptom provocation in obsessive-compulsive disorder . Arch Gen Psychiatry . 1996;53:595–606
  43. Rauch SL, Savage CR, Alpert NM, Miguel EC, Baer L, Breiter HC, et al. A positron emission tomographic study of simple phobic symptom provocation . Arch Gen Psychiatry . 1995;52:20–28
  44. Rauch SL, Van der Kolk BA, Fisler RE, Alpert NM, Orr SP, Savage CR, et al. A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery . Arch Gen Psychiatry . 1996;53:380–387
  45. Lethem J , Slade PD , Troup JD , Bentley G . Outline of a fear-avoidance model of exaggerated pain perception I . Behav Res Ther . 1983;21:401–408
  46. Buchel C , Morris J , Dolan RJ , Friston KJ . Brain systems mediating aversive conditioning (an event-related fMRI study) . Neuron . 1998;20:947–957
  47. Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, et al. Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula (an event-related functional magnetic resonance imaging study) . J Neurosci . 2000;20:7438–7445
  48. Ploghaus A, Narain C, Beckmann CF, Clare S, Bantick S, Wise R, et al. Exacerbation of pain by anxiety is associated with activity in a hippocampal network . J Neurosci . 2001;21:9896–9903
  49. Porro CA , Cettolo V , Francescato MP , Baraldi P . Functional activity mapping of the mesial hemispheric wall during anticipation of pain . Neuroimage . 2003;19:1738–1747
  50. Kern MK , Jaradeh S , Arndorfer RC , Jesmanowicz A , Hyde J , Shaker R . Gender differences in cortical representation of rectal distension in healthy humans . Am J Physiol Gastrointest Liver Physiol . 2001;281:1512–1523
  51. Hobson AR , Aziz Q . Brain imaging and functional gastrointestinal disorders (has it helped our understanding?) . Gut . 2004;53:1198–1206

 Funded by a grant awarded by the Medical Research Council, UK (to Q.A.).

PII: S0016-5085(05)00629-3

doi: 10.1053/j.gastro.2005.02.068

Gastroenterology
Volume 128, Issue 7 , Pages 1819-1829 , June 2005