Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat

Brain Research

Volumn 1153, Issue 1, 2007, Pages 68-77

  Chung, Elaine K Y ^a   Zhang, XiaoJun ^a   Li, Zhi ^a   Zhang, Hongqi ^a   Xu, HongXi ^b   Bian, ZhaoXiang ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Colorectal distention (CRD); Irritable bowel syndrome (IBS); Neonatal maternal separation (NMS); Visceral hyperalgesia

Indexed keywords

PROTEIN C FOS;

ANIMAL EXPERIMENT; ARTICLE; CINGULATE GYRUS; COLON DILATATION; CONTROLLED STUDY; FEMALE; IRRITABLE COLON; MATERNAL DEPRIVATION; MENTAL STRESS; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; COLON; DILATATION, PATHOLOGIC; ELECTROMYOGRAPHY; MATERNAL DEPRIVATION; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PROTO-ONCOGENE PROTEINS C-FOS; RATS; REFLEX;

RATTUS; RATTUS NORVEGICUS;

EID: 34249074047     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.03.047     Document Type: Article

References (50)

1. Al-Chaer E.D., and Traub R.J. Biological basis of visceral pain: recent developments. Pain 96 (2002) 221-225
2. Al-Chaer E.D., Kawasaki M., and Pasricha P.J. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 119 (2000) 1276-1285
3. Almeida T.F., Roizenblatt S., and Tufik S. Afferent pain pathways: a neuroanatomical review. Brain Res. 1000 (2004) 40-56
4. Barreau F., Ferrier L., Fioramonti J., and Bueno L. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53 (2004) 501-506
5. Benarroch E.E. Pain-autonomic interactions: a selective review. Clin. Auton. Res. 11 (2001) 343-349
6. Bercik P., Wang L., Verdu E.F., Mao Y.K., Blennerhassett P., Khan W.I., Kean I., Tougas G., and Collins S.M. Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 127 (2004) 179-187
7. Boatman J.A., and Kim J.J. A thalamo-cortico-amygdala pathway mediates auditory fear conditioning in the intact brain. Eur. J. Neurosci. 24 (2006) 894-900
8. Bonaz B., Baciu M., Papillon E., Bost R., Gueddah N., Le Bas J.F., Fournet J., and Segebarth C. Central processing of rectal pain in patients with irritable bowel syndrome: an fMRI study. Am. J. Gastroenterol. 97 (2002) 654-661
9. Buchel C., Bornhovd K., Quante M., Glauche V., Bromm B., and Weiller C. Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: a parametric single-trial laser functional magnetic resonance imaging study. J. Neurosci. 22 (2002) 970-976
10. Burdin T.A., Graeff F.G., and Pela I.R. Opioid mediation of the antiaversive and hyperalgesic actions of bradykinin injected into the dorsal periaqueductal gray of the rat. Physiol. Behav. 52 (1992) 405-410
11. Caldji C., Diorio J., and Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry 48 (2000) 1164-1174
12. Clark M.R., and Treisman G.J. Neurobiology of pain. Adv. Psychosom. Med. 25 (2004) 78-88
13. Coghill R.C., Sang C.N., Maisog J.M., and Iadarola M.J. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J. Neurophysiol. 82 (1999) 934-943
14. Cohen R.A., Grieve S., Hoth K.F., Paul R.H., Sweet L., Tate D., Gunstad J., Stroud L., McCaffery J., Hitsman B., Niaura R., Clark C.R., McFarlane A., Bryant R., Gordon E., and Williams L.M. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatry 59 (2006) 975-982
15. Coutinho S.V., Plotsky P.M., Sablad M., Miller J.C., Zhou H., Bayati A.I., McRoberts J.A., and Mayer E.A. Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am. J. Physiol., Gastrointest. Liver Physiol. 282 (2002) G307-G316
16. Dafny N., Dong W.Q., Prieto-Gomez C., Reyes-Vazquez C., Stanford J., and Qiao J.T. Lateral hypothalamus: site involved in pain modulation. Neuroscience 70 (1996) 449-460
17. Delvaux M.M. Stress and visceral perception. Can. J. Gastroenterol. 13 Suppl A (1999) 32A-36A
18. Dickhaus B., Mayer E.A., Firooz N., Stains J., Conde F., Olivas T.I., Fass R., Chang L., Mayer M., and Naliboff B.D. Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress. Am. J. Gastroenterol. 98 (2003) 135-143
19. Fitzgerald M. The development of nociceptive circuits. Nat. Rev., Neurosci. 6 (2005) 507-520
20. Gareau M.G., Jury J., Yang P.C., MacQueen G., and Perdue M.H. Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr. Res. 59 (2006) 83-88
21. Han J.S., and Neugebauer V. Synaptic plasticity in the amygdala in a visceral pain model in rats. Neurosci. Lett. 361 (2004) 254-257
22. Hosobuchi Y., Adams J.E., and Linchitz R. Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone. Science 197 (1977) 183-186
23. Hutchison W.D., Davis K.D., Lozano A.M., Tasker R.R., and Dostrovsky J.O. Pain-related neurons in the human cingulate cortex. Nat. Neurosci. 2 (1999) 403-405
24. Jones M.P., Dilley J.B., Drossman D., and Crowell M.D. Brain-gut connections in functional GI disorders: anatomic and physiologic relationships. Neurogastroenterol. Motil. 18 (2006) 91-103
25. Kobelt P., Tebbe J.J., Tjandra I., Bae H.G., Ruter J., Klapp B.F., Wiedenmann B., and Monnikes H. Two immunocytochemical protocols for immunofluorescent detection of c-Fos positive neurons in the rat brain. Brain Res. Brain Res. Protoc. 13 (2004) 45-52
26. Mayer E.A. Spinal and supraspinal modulation of visceral sensation. Gut 47 Suppl 4 (2000) iv69-iv72
27. Mayer E.A. The neurobiology of stress and gastrointestinal disease. Gut 47 (2000) 861-869
28. Mayer E.A., Naliboff B.D., Chang L., and Coutinho S.V. V. Stress and irritable bowel syndrome. Am. J. Physiol., Gastrointest. Liver Physiol. 280 (2001) G519-G524
29. McEwen B.S., and Stellar E. Stress and the individual. Mechanisms leading to disease. Arch. Intern. Med. 153 (1993) 2093-2101
30. Menetrey D., Gannon A., Levine J.D., and Basbaum A.I. Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation. J. Comp. Neurol. 285 (1989) 177-195
31. Millan M.J. Descending control of pain. Prog. Neurobiol. 66 (2002) 355-474
32. Monnikes H., Ruter J., Konig M., Grote C., Kobelt P., Klapp B.F., Arnold R., Wiedenmann B., and Tebbe J.J. Differential induction of c-fos expression in brain nuclei by noxious and non-noxious colonic distension: role of afferent C-fibers and 5-HT3 receptors. Brain Res. 966 (2003) 253-264
33. Morgan V., Pickens D., Gautam S., Kessler R., and Mertz H. Amitriptyline reduces rectal pain related activation of the anterior cingulate cortex in patients with irritable bowel syndrome. Gut 54 (2005) 601-607
34. Murray C.D., Flynn J., Ratcliffe L., Jacyna M.R., Kamm M.A., and Emmanuel A.V. Effect of acute physical and psychological stress on gut autonomic innervation in irritable bowel syndrome. Gastroenterology 127 (2004) 1695-1703
35. Neugebauer V., and Li W. Differential sensitization of amygdala neurons to afferent inputs in a model of arthritic pain. J. Neurophysiol. 89 (2003) 716-727
36. Pacak K., and Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr. Rev. 22 (2001) 502-548
37. Palecek J. The role of dorsal columns pathway in visceral pain. Physiol. Res. 53 Suppl 1 (2004) S125-S130
38. Pihoker C., Owens M.J., Kuhn C.M., Schanberg S.M., and Nemeroff C.B. Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis: a putative role for corticotropin-releasing factor. Psychoneuroendocrinology 18 (1993) 485-493
39. Posserud I., Agerforz P., Ekman R., Bjornsson E.S., Abrahamsson H., and Simren M. Altered visceral perceptual and neuroendocrine response in patients with irritable bowel syndrome during mental stress. Gut 53 (2004) 1102-1108
40. Rainville P., Duncan G.H., Price D.D., Carrier B., and Bushnell M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277 (1997) 968-971
41. Rosztoczy A., Fioramonti J., Jarmay K., Barreau F., Wittmann T., and Bueno L. Influence of sex and experimental protocol on the effect of maternal deprivation on rectal sensitivity to distension in the adult rat. Neurogastroenterol. Motil. 15 (2003) 679-686
42. Sagar S.M., Sharp F.R., and Curran T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240 (1988) 1328-1331
43. Stam R., Ekkelenkamp K., Frankhuijzen A.C., Bruijnzeel A.W., Akkermans L.M., and Wiegant V.M. Long-lasting changes in central nervous system responsivity to colonic distention after stress in rats. Gastroenterology 123 (2002) 1216-1225
44. Tammpere A., Brusberg M., Axenborg J., Hirsch I., Larsson H., and Lindstrom E. Evaluation of pseudo-affective responses to noxious colorectal distension in rats by manometric recordings. Pain 116 (2005) 220-226
45. Traub R.J., Sengupta J.N., and Gebhart G.F. Differential c-fos expression in the nucleus of the solitary tract and spinal cord following noxious gastric distention in the rat. Neuroscience 74 (1996) 873-884
46. Urban M.O., and Gebhart G.F. Supraspinal contributions to hyperalgesia. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 7687-7692
47. Welting O., Van Den Wijngaard R.M., De Jonge W.J., Holman R., and Boeckxstaens G.E. Assessment of visceral sensitivity using radio telemetry in a rat model of maternal separation. Neurogastroenterol. Motil. 17 (2005) 838-845
48. Willis W.D., Al-Chaer E.D., Quast M.J., and Westlund K.N. A visceral pain pathway in the dorsal column of the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 7675-7679
49. Yuan Y.Z., Tao R.J., Xu B., Sun J., Chen K.M., Miao F., Zhang Z.W., and Xu J.Y. Functional brain imaging in irritable bowel syndrome with rectal balloon-distention by using fMRI. World J. Gastroenterol. 9 (2003) 1356-1360
50. Zhang L., Zhang Y., and Zhao Z.Q. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur. J. Neurosci. 22 (2005) 1141-1148