PAIN
Volume 145, Issue 1 , Pages 120-128 , September 2009

Sex differences in functional brain activation during noxious visceral stimulation in rats

  • Zhuo Wang

      Affiliations

    • Center for Neurobiology of Stress, UCLA, Los Angeles, CA, USA
    • VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA
    • Department of Psychiatry & the Behavioral Sciences, USC, Los Angeles, CA, USA
    • These authors contributed equally to this work.
    • ,
  • Yumei Guo

      Affiliations

    • Department of Psychiatry & the Behavioral Sciences, USC, Los Angeles, CA, USA
    • These authors contributed equally to this work.
    • ,
  • Sylvie Bradesi

      Affiliations

    • Center for Neurobiology of Stress, UCLA, Los Angeles, CA, USA
    • Department of Medicine, UCLA, Los Angeles, CA, USA
    • VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA
    • ,
  • Jennifer S. Labus

      Affiliations

    • Center for Neurobiology of Stress, UCLA, Los Angeles, CA, USA
    • Department of Psychiatry & Biobehavioral Sciences, UCLA, Los Angeles, CA, USA
    • Brain Research Institute, UCLA, Los Angeles, CA, USA
    • ,
  • Jean-Michel I. Maarek

      Affiliations

    • Department of Biomedical Engineering, USC, Los Angeles, CA, USA
    • ,
  • Kevin Lee

      Affiliations

    • Neurology & GI Center of Excellence for Drug Discovery, GlaxoSmithKline, Harlow, UK
    • ,
  • Wendy J. Winchester

      Affiliations

    • Neurology & GI Center of Excellence for Drug Discovery, GlaxoSmithKline, Harlow, UK
    • ,
  • Emeran A. Mayer

      Affiliations

    • Center for Neurobiology of Stress, UCLA, Los Angeles, CA, USA
    • Department of Medicine, UCLA, Los Angeles, CA, USA
    • Department of Physiology, UCLA, Los Angeles, CA, USA
    • Department of Psychiatry & Biobehavioral Sciences, UCLA, Los Angeles, CA, USA
    • Brain Research Institute, UCLA, Los Angeles, CA, USA
    • VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA
    • ,
  • Daniel P. Holschneider

      Affiliations

    • VA Greater Los Angeles Healthcare System, Los Angeles, CA, USA
    • Department of Biomedical Engineering, USC, Los Angeles, CA, USA
    • Department of Psychiatry & the Behavioral Sciences, USC, Los Angeles, CA, USA
    • Departments of Neurology, Cell & Neurobiology, USC, Los Angeles, CA, USA
    • Corresponding Author InformationCorresponding author. Address: Dept. of Psychiatry and the Behavioral Sciences, Keck School of Medicine, University of Southern California, 1333 San Pablo St., BMT 403, Los Angeles, CA 90089-9112, USA. Tel.: +1 323 442 1536; fax: +1 323 442 1587.

Received 19 December 2008 ,Revised 3 May 2009 ,Accepted 27 May 2009.

References 

  1. Berman S, Munakata J, Naliboff BD, Chang L, Mandelkern M, Silverman D, et al. Gender differences in regional brain response to visceral pressure in IBS patients. Eur J Pain. 2000;4:157–172
  2. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, Bueller JA, et al. Sex differences in regional brain response to aversive pelvic visceral stimuli. Am J Physiol Regul Integr Comp Physiol. 2006;291:R268–R276
  3. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, Ohning G, et al. 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. 2008;28:349–359
  4. Bonaz B, Baciu M, Papillon E, Bost R, Gueddah N, Le Bas JF, et al. Central processing of rectal pain in patients with irritable bowel syndrome: an fMRI study. Am J Gastroenterol. 2002;97:654–661
  5. Castro-Alamancos MA. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol. 2004;74:213–247
  6. Cordero ME, Rodriguez A, Torres R, Valenzuela CY. Human raphe magnus nucleus: a morphometric Golgi-Cox study with emphasis on sex differences. Brain Res Dev Brain Res. 2001;131:85–92
  7. Cordero ME, Valenzuela CY, Torres R, Rodriguez A. Sexual dimorphism in number and proportion of neurons in the human median raphe nucleus. Brain Res Dev Brain Res. 2000;124:43–52
  8. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Rev. 2002;3:655–666
  9. Curtis AL, Bethea T, Valentino RJ. Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology. 2006;31:544–554
  10. Dominguez R, Cruz-Morales SE, Carvalho MC, Xavier M, Brandao ML. Sex differences in serotonergic activity in dorsal and median raphe nucleus. Physiol Behav. 2003;80:203–210
  11. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Comparing functional (PET) images: the assessment of significant change. J Cereb Blood Flow Metab. 1991;11:690–699
  12. Goodman RL. A quantitative analysis of the physiological role of estradiol and progesterone in the control of tonic and surge secretion of luteinizing hormone in the rat. Endocrinology. 1978;102:142–150
  13. Heinsbroek RP, van Haaren F, Feenstra MG, van Galen H, Boer G, van de Poll NE. Sex differences in the effects of inescapable footshock on central catecholaminergic and serotonergic activity. Pharmacol Biochem Behav. 1990;37:539–550
  14. Holdcroft A, Sapsed-Byrne S, Ma D, Hammal D, Forsling ML. Sex and oestrous cycle differences in visceromotor responses and vasopressin release in response to colonic distension in male and female rats anaesthetized with halothane. Br J Anaesth. 2000;85:907–910
  15. Holschneider DP, Maarek JM. Brain maps on the go: functional imaging during motor challenge in animals. Methods (San Diego, CA) 2008;45:255–61.
  16. Jenkins WJ, Becker JB, Sex . In:  Whishaw IQ,  Kolb B editor. The behavior of the laboratory rat: a handbook with tests. New York: Oxford University Press; 2004;p. 307–320
  17. Ji Y, Murphy AZ, Traub RJ. Sex differences in morphine-induced analgesia of visceral pain are supraspinally and peripherally mediated. Am J Physiol Regul Integr Comp Physiol. 2006;291:R307–R314
  18. Ji Y, Tang B, Traub RJ. The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats. Neuroscience. 2008;154:1562–1567
  19. Jovanovic H, Lundberg J, Karlsson P, Cerin A, Saijo T, Varrone A, et al. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. Neuroimage. 2008;39:1408–1419
  20. 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:G1512–G1523
  21. Kim D, Park D, Choi S, Lee S, Sun M, Kim C, et al. Thalamic control of visceral nociception mediated by T-type Ca2+ channels. Science. 2003;302:117–119
  22. Labus JS, Naliboff BN, Fallon J, Berman SM, Suyenobu B, Bueller JA, et al. Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: a network analysis. Neuroimage. 2008;41:1032–1043
  23. Lu CL, Wu YT, Yeh TC, Chen LF, Chang FY, Lee SD, et al. Neuronal correlates of gastric pain induced by fundus distension: a 3T-fMRI study. Neurogastroenterol Motil. 2004;16:575–587
  24. Luque JM, de Blas MR, Segovia S, Guillamon A. Sexual dimorphism of the dopamine-beta-hydroxylase-immunoreactive neurons in the rat locus ceruleus. Brain Res Dev Brain Res. 1992;67:211–215
  25. Mayer EA, Berman S, Chang L, Naliboff BD. Sex-based differences in gastrointestinal pain. Eur J Pain (London, UK). 2004;8:451–463
  26. Mayer EA, Berman S, Suyenobu B, Labus J, Mandelkern MA, Naliboff BD, et al. Differences in brain responses to visceral pain between patients with irritable bowel syndrome and ulcerative colitis. Pain. 2005;115:398–409
  27. Mayer EA, Naliboff BD, Craig AD. Neuroimaging of the brain–gut axis: from basic understanding to treatment of functional GI disorders. Gastroenterology. 2006;131:1925–1942
  28. Murphy AZ, Suckow SK, Johns M, Traub RJ. Sex differences in the activation of the spinoparabrachial circuit by visceral pain. Physiol Behav. 2009;97:205–212
  29. Naliboff BD, Berman S, Chang L, Derbyshire SW, Suyenobu B, Vogt BA, et al. Sex-related differences in IBS patients: central processing of visceral stimuli. Gastroenterology. 2003;124:1738–1747
  30. Naliboff BD, Berman S, Suyenobu B, Labus JS, Chang L, Stains J, et al. Longitudinal change in perceptual and brain activation response to visceral stimuli in irritable bowel syndrome patients. Gastroenterology. 2006;131:352–365
  31. Ness TJ, Gebhart GF. Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res. 1988;450:153–169
  32. Nguyen PT, Holschneider DP, Maarek JM, Yang J, Mandelkern MA. Statistical parametric mapping applied to an autoradiographic study of cerebral activation during treadmill walking in rats. Neuroimage. 2004;23:252–259
  33. Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. Cardiovascular effects of human insular cortex stimulation. Neurology. 1992;42:1727–1732
  34. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Elsevier Academic Press; 2005;
  35. Petrovic P, Carlsson K, Petersson KM, Hansson P, Ingvar M. Context-dependent deactivation of the amygdala during pain. J Cogn Neurosci. 2004;16:1289–1301
  36. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol Psychiatry. 2003;54:504–514
  37. Pinos H, Collado P, Rodriguez-Zafra M, Rodriguez C, Segovia S, Guillamon A. The development of sex differences in the locus coeruleus of the rat. Brain Res Bull. 2001;56:73–78
  38. Preuss TM. Do rats have prefrontal cortex – The Rose–Woolsey–Akert Program reconsidered. J Cogn Neurosci. 1995;7:1–24
  39. Stam R, van Laar TJ, Wiegant VM. Physiological and behavioural responses to duodenal pain in freely moving rats. Physiol Behav. 2004;81:163–169
  40. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS, et al. A validated network of effective amygdala connectivity. NeuroImage. 2007;36:736–745
  41. Tache Y, Bonaz B. Corticotropin-releasing factor receptors and stress-related alterations of gut motor function. J Clin Invest. 2007;117:33–40
  42. Thevenaz P, Ruttimann UE, Unser M. A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process. 1998;7:27–41
  43. Tomasi D, Chang L, Caparelli EC, Ernst T. Sex differences in sensory gating of the thalamus during auditory interference of visual attention tasks. Neuroscience. 2008;151:1006–1015
  44. Unruh AM. Gender variations in clinical pain experience. Pain. 1996;65:123–167
  45. Uylings HB, Groenewegen HJ, Kolb B. Do rats have a prefrontal cortex?. Behav Brain Res. 2003;146:3–17
  46. Valentino RJ, Miselis RR, Pavcovich LA. Pontine regulation of pelvic viscera: pharmacological target for pelvic visceral dysfunctions. Trends Pharmacol Sci. 1999;20:253–260
  47. Vertes RP. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience. 2006;142:1–20
  48. Vertes RP. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol. 1991;313:643–668
  49. Vogt BA, Peters A. Form and distribution of neurons in rat cingulate cortex: areas 32, 24, and 29. J Comp Neurol. 1981;195:603–625
  50. Wang Z, Bradesi S, Maarek JM, Lee K, Winchester WJ, Mayer EA, et al. Regional brain activation in conscious, nonrestrained rats in response to noxious visceral stimulation. Pain. 2008;138:233–243
  51. Wilder-Smith CH, Schindler D, Lovblad K, Redmond SM, Nirkko A. Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls. Gut. 2004;53:1595–1601
  52. Wong SW, Kimmerly DS, Masse N, Menon RS, Cechetto DF, Shoemaker JK. Sex differences in forebrain and cardiovagal responses at the onset of isometric handgrip exercise: a retrospective fMRI study. J Appl Physiol. 2007;103:1402–1411
  53. Yang SW, Follett KA, Piper JG, Ness TJ. The effect of morphine on responses of mediodorsal thalamic nuclei and nucleus submedius neurons to colorectal distension in the rat. Brain Res. 1998;779:41–52
  54. Yang SW, Follett KA, Piper JG, Ness TJ. The effect of morphine on responses of nucleus ventroposterolateralis neurons to colorectal distension in the rat. Brain Res Bull. 1999;48:609–614
  55. Yasui Y, Breder CD, Saper CB, Cechetto DF. Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol. 1991;303:355–374

PII: S0304-3959(09)00318-2

doi: 10.1016/j.pain.2009.05.025

PAIN
Volume 145, Issue 1 , Pages 120-128 , September 2009

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