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Neurobiology of Stress-Induced Hyperalgesia

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Book cover Behavioral Neurobiology of Chronic Pain

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 20))

Abstract

The intensity and severity of perceived pain does not correlate consistently with the degree of peripheral or central nervous system tissue damage or with the intensity of primary afferent or spinal nociceptive neurone activity. In this respect, the modulation of pain by emotion and context is now widely recognized. In particular, stress, fear and anxiety exert potent, but complex, modulatory influences on pain. Stress can either suppress pain (stress-induced analgesia) or exacerbate it (stress-induced hyperalgesia; SIH) depending on the nature, duration and intensity of the stressor. Herein, we review the methods and models used to study the phenomenon of SIH in rodents and humans and then present a detailed discussion of our current understanding of neural substrates and neurobiological mechanisms. The review provides perspectives and challenges for the current and future treatment of pain and the co-morbidity of pain with stress-related psychiatric disorders including anxiety and depression.

Parts of this text have previously been published in Olango and Finn (2013) and are reproduced by permission of the Royal Society of Chemistry.

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References

  • Abdelhamid RE, Kovacs KJ, Pasley JD, Nunez MG, Larson AA (2013) Forced swim-induced musculoskeletal hyperalgesia is mediated by CRF2 receptors but not by TRPV1 receptors. Neuropharmacology 72:29–37. doi:10.1016/j.neuropharm.2013.04.016S0028-3908(13)00162-7 [pii]

  • Adell A, Casanovas JM, Artigas F (1997) Comparative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas. Neuropharmacology 36(4–5):735–741

    CAS  PubMed  Google Scholar 

  • Adler G, Gattaz WF (1993) Pain perception threshold in major depression. Biol Psychiatry 34(10):687–689

    CAS  PubMed  Google Scholar 

  • Ait-Belgnaoui A, Bradesi S, Fioramonti J, Theodorou V, Bueno L (2005) Acute stress-induced hypersensitivity to colonic distension depends upon increase in paracellular permeability: role of myosin light chain kinase. Pain 113(1–2):141–147

    CAS  PubMed  Google Scholar 

  • Al Absi M, Rokke PD (1991) Can anxiety help us tolerate pain? Pain 46(1):43–51

    CAS  PubMed  Google Scholar 

  • Alfven G, Östberg V, Hjern A (2008) Stressor, perceived stress and recurrent pain in Swedish schoolchildren. J Psychosom Res 65(4):381–387

    PubMed  Google Scholar 

  • Andre J, Zeau B, Pohl M, Cesselin, Francois, Benoliel, Jean-Jacques, Becker C (2005) Involvement of cholecystokininergic systems in anxiety-induced hyperalgesia in male rats: behavioral and biochemical studies. J Neurosci 25(35):7896–7904. doi:10.1523/jneurosci.0743-05.2005

  • Angst MS, Koppert W, Pahl I, Clark DJ, Schmelz M (2003) Short-term infusion of the [mu]-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 106(1–2):49–57

    CAS  PubMed  Google Scholar 

  • Arnow BA, Hunkeler EM, Blasey CM, Lee J, Constantino MJ, Fireman B, Kraemer HC, Dea R, Robinson R, Hayward C (2006) Comorbid depression, chronic pain, and disability in primary care. Psychosom Med 68(2):262–268. doi:10.1097/01.psy.0000204851.15499.fc

    PubMed  Google Scholar 

  • Arntz A (1991) Attention, not anxiety, influences pain. Behav Res Ther 29(1):41–50

    CAS  PubMed  Google Scholar 

  • Arntz A, Dreessen L, De Jong P (1994) The influence of anxiety on pain: attentional and attributional mediators. Pain 56(3):307–314

    CAS  PubMed  Google Scholar 

  • Asmundson GJ, Katz J (2009) Understanding the co-occurrence of anxiety disorders and chronic pain: state-of-the-art. Depress Anxiety 26(10):888–901. doi:10.1002/da.20600

    PubMed  Google Scholar 

  • Asmundson GJG, Katz J (2008) Understanding pain and posttraumatic stress disorder comorbidity: do pathological responses to trauma alter the perception of pain? Pain 138(2):247–249

    PubMed  Google Scholar 

  • Atkinson JH, Slater MA, Patterson TL, Grant I, Garfin SR (1991) Prevalence, onset, and risk of psychiatric disorders in men with chronic low back pain: a controlled study. Pain 45(2):111–121

    CAS  PubMed  Google Scholar 

  • Bair MJ, Robinson RL, Katon W, Kroenke K (2003) Depression and pain comorbidity: a literature review. Arch Intern Med 163(20):2433–2445. doi:10.1001/archinte.163.20.2433

    PubMed  Google Scholar 

  • Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44(1):525–557. doi:10.1146/annurev.pharmtox.44.101802.121410

    CAS  PubMed  Google Scholar 

  • Bannon MJ, Elliott PJ, Alpert JE, Goedert M, Iversen SD, Iversen LL (1983) Role of endogenous substance P in stress-induced activation of mesocortical dopamine neurones. Nature 306(5945):791–792

    CAS  PubMed  Google Scholar 

  • Bardin L, Malfetes N, Newman-Tancredi A, Depoortère R (2009) Chronic restraint stress induces mechanical and cold allodynia, and enhances inflammatory pain in rat: relevance to human stress-associated painful pathologies. Behav Brain Res 205(2):360–366

    CAS  PubMed  Google Scholar 

  • Beecher H (1969) Anxiety and pain. JAMA 209(7):1080

    CAS  PubMed  Google Scholar 

  • Belozertseva IV, Bespalov AY (1998) Effects of NMDA receptor channel blockers, dizocilpine and memantine, on the development of opiate analgesic tolerance induced by repeated morphine exposures or social defeats in mice. Naunyn-Schmiedeberg’s Archives Pharmacol 358(2):270–274. doi:10.1007/pl00005252

    CAS  Google Scholar 

  • Benedetti F, Amanzio M, Casadio C, Oliaro A, Maggi G (1997) Blockade of nocebo hyperalgesia by the cholecystokinin antagonist proglumide. Pain 71(2):135–140

    CAS  PubMed  Google Scholar 

  • Benedetti F, Amanzio M, Vighetti S, Asteggiano G (2006) The Biochemical and Neuroendocrine Bases of the Hyperalgesic Nocebo Effect. J Neurosci 26(46):12014–12022. doi:10.1523/jneurosci.2947-06.2006

    CAS  PubMed  Google Scholar 

  • Bennett EJ, Tennant CC, Piesse C, Badcock C-A, Kellow JE (1998) Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 43(2):256–261. doi:10.1136/gut.43.2.256

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bertolucci-D’Angio M, Serrano A, Scatton B (1990) Mesocorticolimbic dopaminergic systems and emotional states. J Neurosci Methods 34(1–3):135–142

    PubMed  Google Scholar 

  • Biggio G, Concas A, Corda MG, Giorgi O, Sanna E, Serra M (1990) Gabaergic and dopaminergic transmission in the rat cerebral cortex: Effect of stress, anxiolytic and anxiogenic drugs. Pharmacol Ther 48(2):121–142

    CAS  PubMed  Google Scholar 

  • Boccalon S, Scaggiante B, Perissin L (2006) Anxiety stress and nociceptive responses in mice. Life Sci 78(11):1225–1230

    CAS  PubMed  Google Scholar 

  • Boey CC-M, Goh K-L (2002) Psychosocial factors and childhood recurrent abdominal pain. J Gastroenterol Hepatol 17(12):1250–1253. doi:10.1046/j.1440-1746.2002.02884.x

    PubMed  Google Scholar 

  • Bradesi S, Eutamene H, Garcia-Villar R, Fioramonti J, BuÉNo L (2002) Acute and chronic stress differently affect visceral sensitivity to rectal distension in female rats. Neurogastroenterol Motil 14(1):75–82. doi:10.1046/j.1365-2982.2002.00305.x

    CAS  PubMed  Google Scholar 

  • Bradesi S, Golovatscka V, Ennes HS, McRoberts JA, Karagiannides I, Bakirtzi K, Pothoulakis C, Mayer EA (2011) Role of astrocytes and altered regulation of spinal glutamatergic neurotransmission in stress-induced visceral hyperalgesia in rats. Am J Physiol Gastrointest Liver Physiol 301(3):G580–589. doi:10.1152/ajpgi.00182.2011 [pii]

  • Bradesi S, Schwetz I, Ennes HS, Lamy CMR, Ohning G, Fanselow M, Pothoulakis C, McRoberts JA, Mayer EA (2005) Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol 289(1):G42–G53. doi:10.1152/ajpgi.00500.2004

    CAS  PubMed  Google Scholar 

  • Burke NN, Hayes E, Calpin P, Kerr DM, Moriarty O, Finn DP, Roche M (2010) Enhanced nociceptive responding in two rat models of depression is associated with alterations in monoamine levels in discrete brain regions. Neuroscience 171(4):1300–1313

    CAS  PubMed  Google Scholar 

  • Burke NN, Llorente R, Marco EM, Tong K, Finn DP, Viveros MP, Roche M (2013) Maternal deprivation is associated with sex-dependent alterations in nociceptive behavior and neuroinflammatory mediators in the rat following peripheral nerve injury. J Pain 14(10):1173–1184. doi:10.1016/j.jpain.2013.05.003 [pii] S1526-5900(13)01028-6

    Google Scholar 

  • Butkevich IP, Barr GA, Mikhailenko VA, Otellin VA (2006) Increased formalin-induced pain and expression of fos neurons in the lumbar spinal cord of prenatally stressed infant rats. Neurosci Lett 403(3):222–226

    CAS  PubMed  Google Scholar 

  • Butkevich IP, Barr GA, Vershinina EA (2007) Sex differences in formalin-induced pain in prenatally stressed infant rats. Eur J Pain 11(8):888–894

    PubMed  Google Scholar 

  • Butkevich IP, Vershinina EA (2001) Prenatal stress alters time characteristics and intensity of formalin-induced pain responses in juvenile rats. Brain Res 915(1):88–93

    CAS  PubMed  Google Scholar 

  • Butler RK, Finn DP (2009) Stress-induced analgesia. Prog Neurobiol 88(3):184–202

    CAS  PubMed  Google Scholar 

  • Carter LE, McNeil DW, Vowles KE, Sorrell JT, Turk CL, Ries BJ, Hopko DR (2002) Effects of emotion on pain reports, tolerance and physiology. Pain Res Manag 7(1):21–30

    PubMed  Google Scholar 

  • Chen X, Green PG, Levine JD (2011) Stress enhances muscle nociceptor activity in the rat. Neuroscience 185:166–173. doi:10.1016/j.neuroscience.2011.04.020 [pii] S0306-4522(11)00400-3

    Google Scholar 

  • Christie MJ, Connor M, Vaughan CW, Ingram SL, Bagley EE (2000) Cellular actions of opioids and other analgesics: implications for synergism in pain relief. Clin Exp Pharmacol Physiol 27(7):520–523. doi:10.1046/j.1440-1681.2000.03291.x

    CAS  PubMed  Google Scholar 

  • Chung EK, Zhang X, Li Z, Zhang H, Xu H, Bian Z (2007a) Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat. Brain Res 1153:68-77. doi:S0006-8993(07)00726-3 [pii] 10.1016/j.brainres.2007.03.047

    Google Scholar 

  • Chung EK, Zhang XJ, Xu HX, Sung JJ, Bian ZX (2007b) Visceral hyperalgesia induced by neonatal maternal separation is associated with nerve growth factor-mediated central neuronal plasticity in rat spinal cord. Neuroscience 149(3):685–695. doi:S0306-4522(07)00892-5 [pii] 10.1016/j.neuroscience.2007.07.055

    Google Scholar 

  • Conrad R, Schilling G, Bausch C, Nadstawek J, Wartenberg HC, Wegener I, Geiser F, Imbierowicz K, Liedtke R (2007) Temperament and character personality profiles and personality disorders in chronic pain patients. Pain 133(1–3):197–209

    PubMed  Google Scholar 

  • Cornwall A, Donderi DC (1988) The effect of experimentally induced anxiety on the experience of pressure pain. Pain 35(1):105–113

    CAS  PubMed  Google Scholar 

  • Costa A, Smeraldi A, Tassorelli C, Greco R, Nappi G (2005) Effects of acute and chronic restraint stress on nitroglycerin-induced hyperalgesia in rats. Neurosci Lett 383(1–2):7–11. doi:S0304-3940(05)00318-6 [pii] 10.1016/j.neulet.2005.03.026

    Google Scholar 

  • Crettaz B, Marziniak M, Willeke P, Young P, Hellhammer D, Stumpf A, Burgmer M (2013) Stress-induced allodynia–evidence of increased pain sensitivity in healthy humans and patients with chronic pain after experimentally induced psychosocial stress. PLoS ONE 8(8):e69460. doi:10.1371/journal.pone.0069460 [pii] PONE-D-12-38646

    Google Scholar 

  • Curtis AL, Bello NT, Valentino RJ (2001) Evidence for functional release of endogenous opioids in the locus ceruleus during stress termination. J Neurosci 21(13):RC152

    Google Scholar 

  • da Silva Torres IL, Bonan CD, Crema L, De Leon Nunes M, Battastini AMO, Sarkis JJF, Dalmaz C, Ferreira MBC (2003a) Effect of drugs active at adenosine receptors upon chronic stress-induced hyperalgesia in rats. Eur j pharmacol 481(2–3):197–201

    Google Scholar 

  • da Silva Torres IL, Cucco SNS, Bassani M, Duarte MS, Silveira PP, Vasconcellos AP, Tabajara AS, Dantas G, Fontella FU, Dalmaz C, Ferreira MBC (2003b) Long-lasting delayed hyperalgesia after chronic restraint stress in rats–effect of morphine administration. Neurosci Res 45(3):277–283

    PubMed  Google Scholar 

  • Dantas G, Torres ILDS, Crema LM, Lara DR, Dalmaz C (2005) Repeated restraint stress reduces opioid receptor binding in different rat CNS structures. Neurochem Res 30(1):1–7. doi:10.1007/s11064-004-9679-2

    CAS  PubMed  Google Scholar 

  • de Wied M, Verbaten MN (2001) Affective pictures processing, attention, and pain tolerance. Pain 90(1–2):163–172

    PubMed  Google Scholar 

  • Delvaux MM (1999) Stress and visceral perception. Can J Gastroenterol 13(Suppl A):32A–36A

    Google Scholar 

  • Devall AJ, Liu Z-W, Lovick TA (2009) Hyperalgesia in the setting of anxiety: sex differences and effects of the oestrous cycle in Wistar rats. Psychoneuroendocrinology 34(4):587–596

    CAS  PubMed  Google Scholar 

  • Dhir A, Kulkarni SK (2008) Venlafaxine reverses chronic fatigue-induced behavioral, biochemical and neurochemical alterations in mice. Pharmacol Biochem Behav 89(4):563–571. doi:10.1016/j.pbb.2008.02.011 [pii] S0091-3057(08)00058-0

    Google Scholar 

  • Dhir A, Padi SSV, Naidu PS, Kulkarni SK (2006) Protective effect of naproxen (non-selective COX-inhibitor) or rofecoxib (selective COX-2 inhibitor) on immobilization stress-induced behavioral and biochemical alterations in mice. Eur J Pharmacol 535(1–3):192–198

    CAS  PubMed  Google Scholar 

  • Dominick CH, Blyth FM, Nicholas MK (2012) Unpacking the burden: understanding the relationships between chronic pain and comorbidity in the general population. Pain 153(2):293–3040. doi:S0304-3959(11)00560-4 [pii] 10.1016/j.pain.2011.09.018

    Google Scholar 

  • Dougher MJ (1979) Sensory decision theory analysis of the effects of anxiety and experimental instructions on pain. J Abnorm Psychol 88(2):137–144

    CAS  PubMed  Google Scholar 

  • Drolet G, Dumont ÉC, Gosselin I, Kinkead R, Laforest S, Trottier J-F (2001) Role of endogenous opioid system in the regulation of the stress response. Prog Neuropsychopharmacol Biol Psychiatry 25(4):729–741

    CAS  PubMed  Google Scholar 

  • Dufton LM, Konik B, Colletti R, Stanger C, Boyer M, Morrow S, Compas BE (2008) Effects of stress on pain threshold and tolerance in children with recurrent abdominal pain. Pain 136(1–2):38–43

    PubMed  Google Scholar 

  • Dworkin RH, Clark WC, Lipsitz JD (1995) Pain responsivity in major depression and bipolar disorder. Psychiatry Res 56(2):173–181

    CAS  PubMed  Google Scholar 

  • Engelmann M, Wolf G, Horn TFW (2002) Release patterns of excitatory and inhibitory amino acids within the hypothalamic supraoptic nucleus in response to direct nitric oxide administration during forced swimming in rats. Neurosci Lett 324(3):252–254

    CAS  PubMed  Google Scholar 

  • Fecho K, Nackley AG, Wu Y, Maixner W (2005) Basal and carrageenan-induced pain behavior in Sprague-Dawley, Lewis and Fischer rats. Physiol Behav 85(2):177–186

    CAS  PubMed  Google Scholar 

  • Fereidoni M, Javan M, Semnanian S, Ahmadiani A (2007) Chronic forced swim stress inhibits ultra-low dose morphine-induced hyperalgesia in rats. Behav Pharmacol 18(7):667–672. doi:10.1097/FBP.0b013e3282f007cb [pii] 00008877-200711000-00010

    Google Scholar 

  • Finn DP (2010) Endocannabinoid-mediated modulation of stress responses: Physiological and pathophysiological significance. Immunobiology 215(8):629–646

    CAS  PubMed  Google Scholar 

  • Fishbain DA, Cole B, Cutler RB, Lewis J, Rosomoff HL, Rosomoff RS (2006) Chronic pain and the measurement of personality: do states influence traits? Pain Med 7(6):509–529. doi:10.1111/j.1526-4637.2006.00239.x

    PubMed  Google Scholar 

  • Fishbain DA, Goldberg M, Meagher BR, Steele R, Rosomoff H (1986) Male and female chronic pain patients categorized by DSM-III psychiatric diagnostic criteria. Pain 26(2):181–197

    CAS  PubMed  Google Scholar 

  • Fontella FU, Vendite DA, Tabajara AS, Porciúncula LO, Torres ILdS, Jardim FM, Martini L, Souza DO, Netto CA, Dalmaz C (2004) Repeated restraint stress alters hippocampal glutamate uptake and release in the rat. Neurochem Res 29(9):1703–1709. doi:10.1023/B:NERE.0000035805.46592.6c

  • Ford GK, Finn DP (2008) Clinical correlates of stress-induced analgesia: evidence from pharmacological studies. Pain 140(1):3–7

    PubMed  Google Scholar 

  • Fujisawa H, Ohtani-Kaneko R, Naiki M, Okada T, Masuko K, Yudoh K, Suematsu N, Okamoto K, Nishioka K, Kato T (2008) Involvement of post-translational modification of neuronal plasticity-related proteins in hyperalgesia revealed by a proteomic analysis. Proteomics 8(8):1706–1719. doi:10.1002/pmic.200700928

    CAS  PubMed  Google Scholar 

  • Gamaro GD, Xavier MH, Denardin JD, Pilger JA, Ely DR, Ferreira MBC, Dalmaz C (1998) The Effects of acute and repeated restraint stress on the nociceptive response in rats. Physiol Behav 63(4):693–697

    CAS  PubMed  Google Scholar 

  • Gambarana C, Masi F, Tagliamonte A, Scheggi S, Ghiglieri O, Graziella De Montis M (1999) A chronic stress that impairs reactivity in rats also decreases dopaminergic transmission in the nucleus accumbens: a microdialysis study. J Neurochem 72(5):2039–2046. doi:10.1046/j.1471-4159.1999.0722039.x

  • Gambassi G (2009) Pain and depression: the egg and the chicken story revisited. Arch Gerontol Geriatr 49(Suppl 1):103–112. doi:S0167-4943(09)00218-0 [pii] 10.1016/j.archger.2009.09.018

    Google Scholar 

  • Gameiro GH, da Silva Andrade A, de Castro M, Pereira LF, Tambeli CH, Ferraz de Arruda Veiga MC (2005) The effects of restraint stress on nociceptive responses induced by formalin injected in rat’s TMJ. Pharmacol Biochem Behav 82(2):338–344

    Google Scholar 

  • Gameiro GH, Gameiro PH, da Silva Andrade A, Pereira LF, Arthuri MT, Marcondes FK, de Arruda Veiga MCF (2006) Nociception- and anxiety-like behavior in rats submitted to different periods of restraint stress. Physiol Behav 87(4):643–649

    Google Scholar 

  • Gatchel R, Garofalo J, Ellis E, Holt C (1996) Major psychological disorders in acute and chronic TMD: an initial examination. J Am Dent Assoc 127(9):1365–1370

    CAS  PubMed  Google Scholar 

  • Geerse G-J, van Gurp LCA, Wiegant VM, Stam R (2006) Individual reactivity to the open-field predicts the expression of cardiovascular and behavioural sensitisation to novel stress. Behav Brain Res 175(1):9–17

    PubMed  Google Scholar 

  • Gentsch C, Lichtsteiner M, Feer H (1987) Open field and elevated plus-maze: A behavioural comparison between spontaneously hypertensive (SHR) and Wistar-Kyoto (WKY) rats and the effects of chlordiazepoxide. Behav Brain Res 25(2):101–107

    CAS  PubMed  Google Scholar 

  • Gibbons CH, Adler GK, Bonyhay I, Freeman R (2012) Experimental hypoglycemia is a human model of stress-induced hyperalgesia. Pain 153(11):2204–2209. doi:10.1016/j.pain.2012.06.030 [pii] S0304-3959(12)00406-X

    Google Scholar 

  • Gibney SM, Gosselin RD, Dinan TG, Cryan JF (2010) Colorectal distension-induced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience 165(3):675–683

    CAS  PubMed  Google Scholar 

  • Glowa JR, Hansen CT (1994) Differences in response to an acoustic startle stimulus among forty-six rat strains. Behav Genet 24(1):79–84

    CAS  PubMed  Google Scholar 

  • Grande LA, Loeser JD, Ozuna J, Ashleigh A, Samii A (2004) Complex regional pain syndrome as a stress response. Pain 110(1–2):495–498

    PubMed  Google Scholar 

  • Green PG, Alvarez P, Gear RW, Mendoza D, Levine JD (2011) Further validation of a model of fibromyalgia syndrome in the rat. J Pain 12(7):811–818. doi:10.1016/j.jpain.2011.01.006 S1526-5900(11)00032-0 [pii]

    Google Scholar 

  • Greenwood-Van Meerveld B, Johnson AC, Foreman RD, Linderoth B (2005) Spinal cord stimulation attenuates visceromotor reflexes in a rat model of post-inflammatory colonic hypersensitivity. Auton Neurosci 122(1–2):69–76

    PubMed  Google Scholar 

  • Gue M, Bonbonne C, Fioramonti J, More J, Del Rio-Lacheze C, Comera C, Bueno L (1997a) Stress-induced enhancement of colitis in rats: CRF and arginine vasopressin are not involved. Am J Physiol Gastrointest Liver Physiol 272(1):G84–G91

    CAS  Google Scholar 

  • Gue M, Del Rio-Lacheze C, Eutamene H, Theodorou V, Fioramonti J, Bueno L (1997b) Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol Motil 9(4):271–279

    CAS  PubMed  Google Scholar 

  • Gunter WD, Shepard JD, Foreman RD, Myers DA, Beverley (2000) Evidence for visceral hypersensitivity in high-anxiety rats. Physiol Behav 69(3):379–382

    Google Scholar 

  • Hata T, Itoh E, Kawabata A (1991) Changes in CNS levels of serotonin and its metabolite in SART-stressed (repeatedly cold-stressed) rats. Jpn J Pharmacol 56(1):101–104

    CAS  PubMed  Google Scholar 

  • Hata T, Kita T, Itoh E, Kawabata A (1988) The relationship of hyperalgesia in SART (repeated cold)-stressed animals to the autonomic nervous system. J Auton Pharmacol 8(1):45–52

    CAS  PubMed  Google Scholar 

  • Hellhammer D, Hingtgen J, Wade S, Shea P, Aprison M (1983) Serotonergic changes in specific areas of rat brain associated with activity–stress gastric lesions. Psychosom Med 45(2):115–122

    CAS  PubMed  Google Scholar 

  • Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20(2):78–84

    CAS  PubMed  Google Scholar 

  • Hong S, Fan J, Kemmerer ES, Evans S, Li Y, Wiley JW (2009) Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. Gut 58(2):202–210. doi:10.1136/gut.2008.157594

    CAS  PubMed  Google Scholar 

  • Hong S, Zheng G, Wu X, Snider NT, Owyang C, Wiley JW (2011) Corticosterone mediates reciprocal changes in CB 1 and TRPV1 receptors in primary sensory neurons in the chronically stressed rat. Gastroenterology 140(2):627–637 e624. doi:10.1053/j.gastro.2010.11.003 [pii] S0016-5085(10)01600-8

    Google Scholar 

  • Ikeda M, Nagatsu T (1985) Effect of short-term swimming stress and diazepam on 3,4-dihydroxyphenylacetic acid (DOPAC) and 5-hydroxyindoleacetic acid (5-HIAA) levels in the caudate nucleus: an in vivo voltammetric study. Naunyn Schmiedebergs Arch Pharmacol 331(1):23–26

    CAS  PubMed  Google Scholar 

  • Imbe H, Iwai-Liao Y, Senba E (2006) Stress-induced hyperalgesia: animal models and putative mechanisms. Front Biosci 11:2179–2192. doi:1960 [pii]

    Google Scholar 

  • Imbe H, Kimura A, Donishi T, Kaneoke Y (2012) Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter. Neuroscience 223:209–218. doi:10.1016/j.neuroscience.2012.08.007 [pii] S0306-4522(12)00827-5

    Google Scholar 

  • Imbe H, Murakami S, Okamoto K, Iwai-Liao Y, Senba E (2004) The effects of acute and chronic restraint stress on activation of ERK in the rostral ventromedial medulla and locus coeruleus. Pain 112(3):361–371

    PubMed  Google Scholar 

  • Imbe H, Okamoto K, Donishi T, Senba E, Kimura A (2010) Involvement of descending facilitation from the rostral ventromedial medulla in the enhancement of formalin-evoked nocifensive behavior following repeated forced swim stress. Brain Res 1329:103–112

    CAS  PubMed  Google Scholar 

  • Ip HYV, Abrishami A, Peng PWH, Wong J, Chung F (2009) Predictors of postoperative pain and analgesic consumption: a qualitative systematic review. Anesthesiology 111(3):657–677 610.1097/ALN.1090b1013e3181aae1087a

    Google Scholar 

  • James JE, Hardardottir D (2002) Influence of attention focus and trait anxiety on tolerance of acute pain. Br J Health Psychol 7(Pt 2):149–162. doi:10.1348/135910702169411

    PubMed  Google Scholar 

  • Janssen SA, Arntz A (1996) Anxiety and pain: attentional and endorphinergic influences. Pain 66(2–3):145–150

    CAS  PubMed  Google Scholar 

  • Jones DA, Rollman GB, Brooke RI (1997) The cortisol response to psychological stress in temporomandibular dysfunction. Pain 72(1–2):171–182

    CAS  PubMed  Google Scholar 

  • Jorum E (1988) Noradrenergic mechanisms in mediation of stress-induced hyperalgesia in rats. Pain 32(3):349–355

    CAS  PubMed  Google Scholar 

  • Kain ZN, Sevarino F, Alexander GM, Pincus S, Mayes LC (2000) Preoperative anxiety and postoperative pain in women undergoing hysterectomy: a repeated-measures design. J Psychosom Res 49(6):417–422

    CAS  PubMed  Google Scholar 

  • Kalivas PW, Abhold R (1987) Enkephalin release into the ventral tegmental area in response to stress: modulation of mesocorticolimbic dopamine. Brain Res 414(2):339–348

    CAS  PubMed  Google Scholar 

  • Kawanishi C, Fukuda M, Tamura R, Nishijo H, Ono T (1997) Effects of repeated cold stress on feeding, avoidance behavior, and pain-related nerve fiber activity. Physiol Behav 62(4):849–855

    CAS  PubMed  Google Scholar 

  • Keltner JR, Furst A, Fan C, Redfern R, Inglis B, Fields HL (2006) Isolating the modulatory effect of expectation on pain transmission: a functional magnetic resonance imaging study. J Neurosci 26(16):4437–4443. doi:10.1523/jneurosci.4463-05.2006

    CAS  PubMed  Google Scholar 

  • Khasar SG, Burkham J, Dina OA, Brown AS, Bogen O, Alessandri-Haber N, Green PG, Reichling DB, Levine JD (2008) Stress induces a switch of intracellular signaling in sensory neurons in a model of generalized pain. J Neurosci 28(22):5721–5730. doi:10.1523/jneurosci.0256-08.2008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Khasar SG, Dina OA, Green PG, Levine JD (2009) Sound stress-induced long-term enhancement of mechanical hyperalgesia in rats is maintained by sympathoadrenal catecholamines. The Journal of Pain 10(10):1073–1077

    PubMed Central  PubMed  Google Scholar 

  • Khasar SG, Green PG, Levine JD (2005) Repeated sound stress enhances inflammatory pain in the rat. Pain 116(1–2):79–86. doi:S0304-3959(05)00160-0 [pii] 10.1016/j.pain.2005.03.040

    Google Scholar 

  • King CD, Devine DP, Vierck CJ, Mauderli A, Yezierski RP (2007) Opioid modulation of reflex versus operant responses following stress in the rat. Neuroscience 147(1):174–182

    CAS  PubMed  Google Scholar 

  • King CD, Devine DP, Vierck CJ, Rodgers J, Yezierski RP (2003) Differential effects of stress on escape and reflex responses to nociceptive thermal stimuli in the rat. Brain Res 987(2):214–222

    CAS  PubMed  Google Scholar 

  • King TE, Crown ED, Sieve AN, Joynes RL, Grau JW, Meagher MW (1999) Shock-induced hyperalgesia: evidence forebrain systems play an essential role. Behav Brain Res 100(1–2):33–42

    CAS  PubMed  Google Scholar 

  • Kirby LG, Allen AR, Lucki I (1995) Regional differences in the effects of forced swimming on extracellular levels of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 682(1–2):189–196

    CAS  PubMed  Google Scholar 

  • Koyama T, McHaffie JG, Laurienti PJ, Coghill RC (2005) The subjective experience of pain: where expectations become reality. Proc Natl Acad Sci USA 102(36):12950–12955. doi:10.1073/pnas.0408576102

    CAS  PubMed Central  PubMed  Google Scholar 

  • Langford DJ, Tuttle AH, Briscoe C, Harvey-Lewis C, Baran I, Gleeson P, Fischer DB, Buonora M, Sternberg WF, Mogil JS (2011) Varying perceived social threat modulates pain behavior in male mice. J Pain 12(1):125–132

    PubMed  Google Scholar 

  • Larauche M, Bradesi S, Million M, McLean P, Tache Y, Mayer EA, McRoberts JA (2008) Corticotropin-releasing factor type 1 receptors mediate the visceral hyperalgesia induced by repeated psychological stress in rats. Am J Physiol Gastrointest Liver Physiol 294(4):G1033–1040. doi:10.1152/ajpgi.00507.2007 [pii] 00507.2007

    Google Scholar 

  • Laulin J-P, Larcher A, Célèrier E, Moal ML, Simonnet G (1998) Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time. Eur J Neurosci 10(2):782–785. doi:10.1046/j.1460-9568.1998.00083.x

    CAS  PubMed  Google Scholar 

  • Laulin J-P, Maurette P, Corcuff J-B, Rivat C, Chauvin M, Simonnet G (2002) The role of ketamine in preventing fentanyl-induced hyperalgesia and subsequent acute morphine tolerance. Anesth Analg 94(5):1263–1269

    CAS  PubMed  Google Scholar 

  • Lautenbacher S, Spernal J, Schreiber W, Krieg J-C (1999) Relationship between clinical pain complaints and pain sensitivity in patients with depression and panic disorder. Psychosom Med 61(6):822–827

    CAS  PubMed  Google Scholar 

  • Legangneux E, Mora JJ, Spreux-Varoquaux O, Thorin I, Herrou M, Alvado G, Gomeni C (2001) Cerebrospinal fluid biogenic amine metabolites, plasma-rich platelet serotonin and [3H]imipramine reuptake in the primary fibromyalgia syndrome. Rheumatology 40(3):290–296. doi:10.1093/rheumatology/40.3.290

    CAS  PubMed  Google Scholar 

  • Lembo T, Plourde V, Shui Z, Fullerton S, Mertz H, Tache Y, Sytnik B, Munakata J, Mayer E (1996) Effects of the corticotropin-releasing factor (CRF) on rectal afferent nerves in humans. Neurogastroenterol Motil 8(1):9–18

    CAS  PubMed  Google Scholar 

  • Lieb R, Meinlschmidt G, Araya R (2007) Epidemiology of the association between somatoform disorders and anxiety and depressive disorders: an update. Psychosom Med 69(9):860–863. doi:69/9/860 [pii] 10.1097/PSY.0b013e31815b0103

    Google Scholar 

  • Maier SF, Drugan RC, Grau JW (1982) Controllability, coping behavior, and stress-induced analgesia in the rat. Pain 12(1):47–56

    CAS  PubMed  Google Scholar 

  • Malow RM, West JA, Sutker PB (1987) A sensory decision theory analysis of anxiety and pain responses in chronic drug abusers. J Abnorm Psychol 96(3):184–189

    CAS  PubMed  Google Scholar 

  • Mao J, Price DD, Lu J, Mayer DJ (1998) Antinociceptive tolerance to the mu-opioid agonist DAMGO is dose-dependently reduced by MK-801 in rats. Neurosci Lett 250(3):193–196

    CAS  PubMed  Google Scholar 

  • Marcinkiewcz CA, Green MK, Devine DP, Duarte P, Vierck CJ, Yezierski RP (2009) Social defeat stress potentiates thermal sensitivity in operant models of pain processing. Brain Res 1251:112–120. doi:10.1016/j.brainres.2008.11.042 [pii] S0006-8993(08)02811-4

    Google Scholar 

  • Martenson ME, Cetas JS, Heinricher MM (2009) A possible neural basis for stress-induced hyperalgesia. Pain 142(3):236–244. doi:10.1016/j.pain.2009.01.011 [pii] S0304-3959(09)00040-2

    Google Scholar 

  • Martinez-Urrutia A (1975) Anxiety and pain in surgical patients. J Consult Clin Psychol 43(4):437–442

    CAS  PubMed  Google Scholar 

  • Max M, Wu T, Atlas S, Edwards R, Haythornthwaite J, Bollettino A, Hipp H, McKnight C, Osman I, Crawford E, Pao M, Nejim J, Kingman A, Aisen D, Scully M, Keller R, Goldman D, Belfer I (2006) A clinical genetic method to identify mechanisms by which pain causes depression and anxiety. Molecular Pain 2(1):14

    PubMed Central  PubMed  Google Scholar 

  • Mayer DJ, Mao J, Holt J, Price DD (1999) Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions. Proc Natl Acad Sci 96(14):7731–7736. doi:10.1073/pnas.96.14.7731

    CAS  PubMed Central  PubMed  Google Scholar 

  • McNally GP, Johnston IN, Westbrook RF (2000) A peripheral, intracerebral, or intrathecal administration of an opioid receptor antagonist blocks illness-induced hyperalgesia in the rat. Behav Neurosci 114(6):1183–1190

    CAS  PubMed  Google Scholar 

  • McWilliams LA, Cox BJ, Enns MW (2003) Mood and anxiety disorders associated with chronic pain: an examination in a nationally representative sample. Pain 106(1–2):127–133. doi:S0304395903003014 [pii]

    Google Scholar 

  • Meagher MW, Arnau RC, Rhudy JL (2001) Pain and emotion: effects of affective picture modulation. Psychosom Med 63(1):79–90

    CAS  PubMed  Google Scholar 

  • Metz GAS, Schwab ME, Welzl H (2001) The effects of acute and chronic stress on motor and sensory performance in male Lewis rats. Physiol Behav 72(1–2):29–35

    Google Scholar 

  • Million M, Grigoriadis DE, Sullivan S, Crowe PD, McRoberts JA, Zhou H, Saunders PR, Maillot C, Mayer EA, Taché Y (2003) A novel water-soluble selective CRF1 receptor antagonist, NBI 35965, blunts stress-induced visceral hyperalgesia and colonic motor function in rats. Brain Res 985(1):32–42

    CAS  PubMed  Google Scholar 

  • Nasu T, Taguchi T, Mizumura K (2010) Persistent deep mechanical hyperalgesia induced by repeated cold stress in rats. Eur J Pain 14 (3):236–244. doi:10.1016/j.ejpain.2009.05.009 [pii] S1090-3801(09)00097-4

    Google Scholar 

  • Nilsen KB, Sand T, Westgaard RH, Stovner LJ, White LR, Bang Leistad R, Helde G, Rø M (2007) Autonomic activation and pain in response to low-grade mental stress in fibromyalgia and shoulder/neck pain patients. Eur J Pain 11(7):743–755

    Google Scholar 

  • O’Mahony SM, Bulmer DC, Coelho Am, Fitzgerald P, Bongiovanni C, Lee K, Winchester W, Dinan TG, Cryan JF (2010) 5-HT2B receptors modulate visceral hypersensitivity in a stress-sensitive animal model of brain-gut axis dysfunction. Neurogastroenterol Motil 22(5):573–e124. doi:10.1111/j.1365-2982.2009.01432.x

  • Ohara H, Kawamura M, Namimatsu A, Miura T, Yoneda R, Hata T (1991) Mechanism of hyperalgesia in SART stressed (repeated cold stress) mice: antinociceptive effect of neurotropin. Jpn J Pharmacol 57(2):243–250

    CAS  PubMed  Google Scholar 

  • Ohashi-Doi K, Himaki D, Nagao K, Kawai M, Gale JD, Furness JB, Kurebayashi Y (2010) A selective, high affinity 5-HT 2B receptor antagonist inhibits visceral hypersensitivity in rats. Neurogastroenterol Motil 22(2):e69–e76. doi:10.1111/j.1365-2982.2009.01395.x NMO1395 [pii]

    Google Scholar 

  • Okano K, Ueda M, Kuraishi Y, Satoh M (1997) Effect of repeated cold stress on capsaicin-evoked release of glutamate from rat spinal dorsal horn slices. Neurosci Res 29(4):319–324

    CAS  PubMed  Google Scholar 

  • Olango WM, Finn DP (2013) Affective and cognitive modulation of pain. In: Allerton C (ed) Pain therapeutics: current and future treatment paradigms, RSC Drug Discovery Series vol 35. Royal Society of Chemistry, pp 270–309

    Google Scholar 

  • Omiya Y, Goto K, Ishige A, Komatsu Y (2000) Changes in analgesia-producing mechanism of repeated cold stress loading in mice. Pharmacol Biochem Behav 65(2):261–266

    CAS  PubMed  Google Scholar 

  • Otis JD, Keane TM, Kerns RD (2003) An examination of the relationship between chronic pain and post-traumatic stress disorder. J Rehabil Res Dev 40(5):397–405

    PubMed  Google Scholar 

  • Otto MW, Dougher MJ, Yeo RA (1989) Depression, pain, and hemispheric activation. J Nerv Ment Dis 177(4):210–218

    CAS  PubMed  Google Scholar 

  • Palermo TM, Drotar D (1996) Prediction of children’s postoperative pain: the role of presurgical expectations and anticipatory emotions. J Pediatr Psychol 21(5):683–698. doi:10.1093/jpepsy/21.5.683

    CAS  PubMed  Google Scholar 

  • Papaioannou M, Skapinakis P, Damigos D, Mavreas V, Broumas G, Palgimesi A (2009) The role of catastrophizing in the prediction of postoperative pain. Pain Med 10(8):1452–1459. doi:10.1111/j.1526-4637.2009.00730.x

    PubMed  Google Scholar 

  • Pardon MC, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA, Mason PA, Morilak DA (2002) Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115(1):229–242

    CAS  PubMed  Google Scholar 

  • Paré WP (1992) The performance of WKY rats on three tests of emotional behavior. Physiol Behav 51(5):1051–1056

    PubMed  Google Scholar 

  • Perrin MH, Vale WW (1999) Corticotropin releasing factor receptors and their ligand family. Ann N Y Acad Sci 885(1):312–328. doi:10.1111/j.1749-6632.1999.tb08687.x

    CAS  PubMed  Google Scholar 

  • Pignatiello MF, Olson GA, Kastin AJ, Ehrensing RH, McLean JH, Olson RD (1989) MIF-1 is active in a chronic stress animal model of depression. Pharmacol Biochem Behav 32(3):737–742

    CAS  PubMed  Google Scholar 

  • Pinto-Ribeiro F, Almeida A, Pêgo JM, Cerqueira J, Sousa N (2004) Chronic unpredictable stress inhibits nociception in male rats. Neurosci Lett 359(1–2):73–76

    CAS  PubMed  Google Scholar 

  • Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, Rawlins JNP (1999) Dissociating pain from its anticipation in the human brain. Science 284(5422):1979–1981. doi:10.1126/science.284.5422.1979

    CAS  PubMed  Google Scholar 

  • Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266(5604):730–732

    CAS  PubMed  Google Scholar 

  • Quintero L, Cuesta MC, Silva JA, Arcaya JL, Pinerua-Suhaibar L, Maixner W, Suarez-Roca H (2003) Repeated swim stress increases pain-induced expression of c-Fos in the rat lumbar cord. Brain Res 965(1–2):259–268

    CAS  PubMed  Google Scholar 

  • Quintero L, Moreno M, Avila C, Arcaya J, Maixner W, Suarez-Roca H (2000) Long-lasting delayed hyperalgesia after subchronic swim stress. Pharmacol Biochem Behav 67(3):449–458

    CAS  PubMed  Google Scholar 

  • Ramos A, Berton O, Mormède P, Chaouloff F (1997) A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85(1):57–69

    CAS  PubMed  Google Scholar 

  • Ramos A, Kangerski AL, Basso PF, Da Silva Santos JE, Assreuy J, Vendruscolo LF, Takahashi RN (2002) Evaluation of Lewis and SHR rat strains as a genetic model for the study of anxiety and pain. Behav Brain Res 129(1–2):113–123

    Google Scholar 

  • Rea K, Olango WM, Okine BN, Madasu MK, McGuire IC, Coyle K, Harhen B, Roche M, Finn DP (2013) Impaired endocannabinoid signalling in the rostral ventromedial medulla underpins genotype-dependent hyper-responsivity to noxious stimuli. Pain. doi:S0304-3959(13)00509-5 [pii] 10.1016/j.pain.2013.09.012

    Google Scholar 

  • Reynolds J, Bilsky EJ, Meng ID (2011) Selective ablation of mu-opioid receptor expressing neurons in the rostral ventromedial medulla attenuates stress-induced mechanical hypersensitivity. Life Sci 89(9–10):313–319. doi:10.1016/j.lfs.2011.06.024 [pii] S0024-3205(11)00316-X

    Google Scholar 

  • Rhudy JL, Dubbert PM, Parker JD, Burke RS, Williams AE (2006) Affective modulation of pain in substance-dependent veterans. Pain Med 7(6):483–500

    PubMed  Google Scholar 

  • Rhudy JL, Meagher MW (2000) Fear and anxiety: divergent effects on human pain thresholds. Pain 84(1):65–75

    CAS  PubMed  Google Scholar 

  • Rhudy JL, Meagher MW (2001a) Noise stress and human pain thresholds: divergent effects in men and women. The Journal of Pain 2(1):57–64

    CAS  PubMed  Google Scholar 

  • Rhudy JL, Meagher MW (2001b) The role of emotion in pain modulation. Curr Opin Psychiatry 14(3):241–245

    Google Scholar 

  • Rhudy JL, Meagher MW (2003a) Individual differences in the emotional reaction to shock determine whether hypoalgesia is observed. Pain Med 4(3):244–256. doi:10.1046/j.1526-4637.2003.03028.x

    PubMed  Google Scholar 

  • Rhudy JL, Meagher MW (2003b) Negative affect: effects on an evaluative measure of human pain. Pain 104(3):617–626

    PubMed  Google Scholar 

  • Rivat C, Becker C, Blugeot A, Zeau B, Mauborgne A, Pohl M, Benoliel JJ (2010) Chronic stress induces transient spinal neuroinflammation, triggering sensory hypersensitivity and long-lasting anxiety-induced hyperalgesia. Pain 150(2):358–368. doi:10.1016/j.pain.2010.05.031 [pii] S0304-3959(10)00334-9

    Google Scholar 

  • Rivat C, Laboureyras E, Laulin J-P, Le Roy C, Richebe P, Simonnet G (2007) Non-nociceptive environmental stress induces hyperalgesia, not analgesia. Pain and Opioid-Experienced Rats. Neuropsychopharmacology 32(10):2217–2228

    CAS  Google Scholar 

  • Robbins MT, DeBerry J, Ness TJ (2007) Chronic psychological stress enhances nociceptive processing in the urinary bladder in high-anxiety rats. Physiol Behav 91(5):544–550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Russell IJ, Vaeroy H, Javors M, Nyberg F (1992) Cerebrospinal fluid biogenic amine metabolites in fibromyalgia/fibrositis syndrome and rheumatoid arthritis. Arthritis Rheum 35(5):550–556

    CAS  PubMed  Google Scholar 

  • Sagami Y, Shimada Y, Tayama J, Nomura T, Satake M, Endo Y, Shoji T, Karahashi K, Hongo M, Fukudo S (2004) Effect of a corticotropin releasing hormone receptor antagonist on colonic sensory and motor function in patients with irritable bowel syndrome. Gut 53(7):958–964. doi:10.1136/gut.2003.018911

    CAS  PubMed Central  PubMed  Google Scholar 

  • Satoh M, Kuraishi Y, Kawamura M (1992) Effects of intrathecal antibodies to substance P, calcitonin gene-related peptide and galanin on repeated cold stress-induced hyperalgesia: comparison with carrageenan-induced hyperalgesia. Pain 49(2):273–278

    CAS  PubMed  Google Scholar 

  • Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, Konishi J, Shibasaki H (2000) 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. The Journal of Neuroscience 20(19):7438–7445

    CAS  PubMed  Google Scholar 

  • Schumacher R, Velden M (1984) Anxiety, pain experience, and pain report: a signal-detection study. Percept Mot Skills 58(2):339–349

    CAS  PubMed  Google Scholar 

  • Schwetz I, Bradesi S, McRoberts JA, Sablad M, Miller JC, Zhou H, Ohning G, Mayer EA (2004) Delayed stress-induced colonic hypersensitivity in male Wistar rats: role of neurokinin-1 and corticotropin-releasing factor-1 receptors. Am J Physiol Gastrointest Liver Physiol 286(4):G683–G691. doi:10.1152/ajpgi.00358.2003

    CAS  PubMed  Google Scholar 

  • Schwetz I, McRoberts JA, Coutinho SV, Bradesi S, Gale G, Fanselow M, Million M, Ohning G, Taché Y, Plotsky PM, Mayer EA (2005) Corticotropin-releasing factor receptor 1 mediates acute and delayed stress-induced visceral hyperalgesia in maternally separated Long-Evans rats. Am J Physiol Gastrointest Liver Physiol 289(4):G704–G712. doi:10.1152/ajpgi.00498.2004

    CAS  PubMed  Google Scholar 

  • Scott LE, Clum GA, Peoples JB (1983) Preoperative predictors of postoperative pain. Pain 15(3):283–293

    Google Scholar 

  • Seo YJ, Kwon MS, Shim EJ, Park SH, Choi OS, Suh HW (2006) Changes in pain behavior induced by formalin, substance P, glutamate and pro-inflammatory cytokines in immobilization-induced stress mouse model. Brain Res Bull 71(1–3):279-286. doi:S0361-9230(06)00274-7 [pii] 10.1016/j.brainresbull.2006.09.012

    Google Scholar 

  • Shen L, Yang XJ, Qian W, Hou XH (2010) The role of peripheral cannabinoid receptors type 1 in rats with visceral hypersensitivity induced by chronic restraint stress. J Neurogastroenterol Motil 16(3):281–290. doi:10.5056/jnm.2010.16.3.281

    PubMed Central  PubMed  Google Scholar 

  • Shi M, Qi WJ, Gao G, Wang JY, Luo F (2010a) Increased thermal and mechanical nociceptive thresholds in rats with depressive-like behaviors. Brain Res 1353:225–233. doi:10.1016/j.brainres.2010.07.023 [pii] S0006-8993(10)01585-4

    Google Scholar 

  • Shi M, Wang JY, Luo F (2010b) Depression shows divergent effects on evoked and spontaneous pain behaviors in rats. J Pain 11 (3):219-229. doi:10.1016/j.jpain.2009.07.002 S1526-5900(09)00634-8 [pii]

    Google Scholar 

  • Shipherd JC, Keyes M, Jovanovic T, Ready DJ, Baltzell D, Worley V, Gordon-Brown V, Hayslett C, Duncan E (2007) Veterans seeking treatment for posttraumatic stress disorder: what about comorbid chronic pain? J Rehabil Res Dev 44(2):153–166

    PubMed  Google Scholar 

  • Siegfried B, Netto CA, Izquierdo I (1987) Exposure to novelty induces naltrexone-reversible analgesia in rats. Behav Neurosci 101(3):436–438

    CAS  PubMed  Google Scholar 

  • Stokes PE, Holtz A (1997) Fluoxetine tenth anniversary update: the progress continues. Clin Ther 19(5):1135–1250

    Google Scholar 

  • Suarez-Roca H, Leal L, Silva JA, Pinerua-Shuhaibar L, Quintero L (2008) Reduced GABA neurotransmission underlies hyperalgesia induced by repeated forced swimming stress. Behav Brain Res 189(1):159–169

    CAS  PubMed  Google Scholar 

  • Suarez-Roca H, Quintero L, Arcaya JL, Maixner W, Rao SG (2006a) Stress-induced muscle and cutaneous hyperalgesia: differential effect of milnacipran. Physiol Behav 88(1–2):82–87

    CAS  PubMed  Google Scholar 

  • Suarez-Roca H, Silva JA, Arcaya JL, Quintero L, Maixner W, Pinerua-Shuhaibar L (2006b) Role of [mu]-opioid and NMDA receptors in the development and maintenance of repeated swim stress-induced thermal hyperalgesia. Behav Brain Res 167(2):205–211

    CAS  PubMed  Google Scholar 

  • Suaudeau C, Costentin J (2000) Long lasting increase in nociceptive threshold induced in mice by forced swimming: involvement of an endorphinergic mechanism. Stress 3(3):221–227. doi:I405J991016 [pii]

    Google Scholar 

  • Taché Y, Martinez V, Wang L, Million M (2004) CRF1 receptor signaling pathways are involved in stress-related alterations of colonic function and viscerosensitivity: implications for irritable bowel syndrome. Br J Pharmacol 141(8):1321–1330. doi:10.1038/sj.bjp.0705760

    PubMed Central  PubMed  Google Scholar 

  • Tanaka M, Yoshida M, Emoto H, Ishii H (2000) Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. Eur J Pharmacol 405(1–3):397–406

    CAS  PubMed  Google Scholar 

  • Terman GW, Morgan MJ, Liebeskind JC (1986) Opioid and non-opioid stress analgesia from cold water swim: importance of stress severity. Brain Res 372(1):167–171

    CAS  PubMed  Google Scholar 

  • Thompson T, Keogh E, French CC, Davis R (2008) Anxiety sensitivity and pain: generalisability across noxious stimuli. Pain 134(1–2):187–196

    PubMed  Google Scholar 

  • Torres ILS, Vasconcellos AP, Silveira Cucco SN, Dalmaz C (2001) Effect of repeated stress on novelty-induced antinociception in rats. Brazilian J Med Biol Res 34:241–244

    Google Scholar 

  • Toulouse M, Coelho AM, Fioramonti J, Lecci A, Maggi C, Buéno L (2000) Role of tachykinin NK2 receptors in normal and altered rectal sensitivity in rats. Br J Pharmacol 129(1):193–199. doi:10.1038/sj.bjp.0703040

    CAS  PubMed Central  PubMed  Google Scholar 

  • Trujillo KA, Akil H (1991) Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251(4989):85–87

    CAS  PubMed  Google Scholar 

  • Tsuda A, Tanaka M, Ida Y, Tsujimaru S, Ushijima I, Nagasaki N (1986) Effects of preshock experience on enhancement of rat brain noradrenaline turnover induced by psychological stress. Pharmacol Biochem Behav 24(1):115–119

    CAS  PubMed  Google Scholar 

  • 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(9):761–768. doi:10.1111/j.1365-2982.2007.00955.x

  • van den Wijngaard RM, Stanisor OI, van Diest SA, Welting O, Wouters MM, de Jonge WJ, Boeckxstaens GE (2012) Peripheral alpha-helical CRF (9–41) does not reverse stress-induced mast cell dependent visceral hypersensitivity in maternally separated rats. Neurogastroenterol Motil 24(3):274–282, e111. doi:10.1111/j.1365-2982.2011.01840.x

  • Van Houdenhove B, Luyten P (2006) Stress, depression and fibromyalgia. Acta Neurol Belg 106(4):149–156

    PubMed  Google Scholar 

  • Vaughn F, Wichowski H, Bosworth G (2007) Does preoperative anxiety level predict postoperative pain? AORN 85(3):589–594, 597–604

    Google Scholar 

  • Verkuyl JM, Hemby SE, Joëls M (2004) Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur J Neurosci 20(6):1665–1673. doi:10.1111/j.1460-9568.2004.03568.x

    PubMed  Google Scholar 

  • Verkuyl JM, Karst H, Joëls M (2005) GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur J Neurosci 21(1):113–121. doi:10.1111/j.1460-9568.2004.03846.x

    PubMed  Google Scholar 

  • Vidal C, Jacob J (1982) Hyperalgesia induced by non-noxious stress in the rat. Neurosci Lett 32(1):75–80

    CAS  PubMed  Google Scholar 

  • Vidal C, Jacob J (1986) Hyperalgesia induced by emotional stress in the rat: an experimental animal model of human anxiogenic hyperalgesia. Ann N Y Acad Sci 467(1):73–81. doi:10.1111/j.1749-6632.1986.tb14619.x

    CAS  PubMed  Google Scholar 

  • Wagner KM, Roeder Z, Desrochers K, Buhler AV, Heinricher MM, Cleary DR (2013) The dorsomedial hypothalamus mediates stress-induced hyperalgesia and is the source of the pronociceptive peptide cholecystokinin in the rostral ventromedial medulla. Neuroscience 238:29–38. doi:10.1016/j.neuroscience.2013.02.009 [pii] S0306-4522(13)00136-X

    Google Scholar 

  • Walters ET (1994) Injury-related behavior and neuronal plasticity: an evolutionary perspective on sensitization, hyperalgesia, and analgesia. Int Rev Neurobiol 36:325–427

    CAS  PubMed  Google Scholar 

  • Ward NG, Bloom VL, Dworkin S, Fawcett J, Narasimhachari N, Friedel RO (1982) Psychobiological markers in coexisting pain and depression: toward a unified theory. J Clin Psychiatry 43(8 Pt 2):32–41

    CAS  PubMed  Google Scholar 

  • Wei H, Zhao W, Wang Y-X, Pertovaara A (2007) Pain-related behavior following REM sleep deprivation in the rat: Influence of peripheral nerve injury, spinal glutamatergic receptors and nitric oxide. Brain Res 1148:105–112

    CAS  PubMed  Google Scholar 

  • Weisenberg M, Aviram O, Wolf Y, Raphaeli N (1984) Relevant and irrelevant anxiety in the reaction to pain. Pain 20(4):371–383

    CAS  PubMed  Google Scholar 

  • Wiech K, Tracey I (2009) The influence of negative emotions on pain: behavioral effects and neural mechanisms. NeuroImage 47(3):987–994

    PubMed  Google Scholar 

  • Wiertelak EP, Yang HYT, Mooney-Heiberger K, Maier SF, Watkins LR (1994) The nature of conditioned anti-analgesia: spinal cord opiate and anti-opiate neurochemistry. Brain Res 634(2):214–226

    CAS  PubMed  Google Scholar 

  • Willer JC, Albe-Fessard D (1980) Electrophysiological evidence for a release of endogenous opiates in stress-induced [‘]analgesia’ in man. Brain Res 198(2):419–426

    CAS  PubMed  Google Scholar 

  • Willer JC, Dehen H, Cambier J (1981) Stress-induced analgesia in humans: endogenous opioids and naloxone-reversible depression of pain reflexes. Science 212(4495):689–691

    CAS  PubMed  Google Scholar 

  • Williams AE, Rhudy JL (2007) The influence of conditioned fear on human pain thresholds: does preparedness play a role? J Pain 8(7):598–606

    PubMed  Google Scholar 

  • Wise TN, Hall WA, Wong O (1978) The relationship of cognitive styles and affective status to post-operative analgesic utilization. J Psychosom Res 22(6):513–518

    CAS  PubMed  Google Scholar 

  • Wood PB (2004) Stress and dopamine: implications for the pathophysiology of chronic widespread pain. Med Hypotheses 62(3):420–424

    CAS  PubMed  Google Scholar 

  • Wouters MM, Van Wanrooy S, Casteels C, Nemethova A, de Vries A, Van Oudenhove L, Van den Wijngaard RM, Van Laere K, Boeckxstaens G (2012) Altered brain activation to colorectal distention in visceral hypersensitive maternal-separated rats. Neurogastroenterol Motil 24(7):678–685, e297. doi:10.1111/j.1365-2982.2012.01919.x

  • Wu Y-L, Yoshida M, Emoto H, Tanaka M (1999) Psychological stress selectively increases extracellular dopamine in the [‘]shell’, but not in the [‘]core’ of the rat nucleus accumbens: a novel dual-needle probe simultaneous microdialysis study. Neurosci Lett 275(1):69–72

    CAS  PubMed  Google Scholar 

  • Zautra A, Parrish B, Van Puymbroeck C, Tennen H, Davis M, Reich J, Irwin M (2007) Depression history, stress, and pain in rheumatoid arthritis patients. J Behav Med 30(3):187–197. doi:10.1007/s10865-007-9097-4

    PubMed  Google Scholar 

  • Zaza C, Baine N (2002) Cancer pain and psychosocial factors: a critical review of the literature. J Pain Symptom Manage 24(5):526–542

    PubMed  Google Scholar 

  • Zeng Q, Wang S, Lim G, Yang L, Mao J, Sung B, Chang Y, Lim J-A, Guo G, Mao J (2008) Exacerbated mechanical allodynia in rats with depression-like behavior. Brain Res 1200:27–38

    CAS  PubMed  Google Scholar 

  • Zhang XJ, Chen HL, Li Z, Zhang HQ, Xu HX, Sung JJ, Bian ZX (2009a) Analgesic effect of paeoniflorin in rats with neonatal maternal separation-induced visceral hyperalgesia is mediated through adenosine A(1) receptor by inhibiting the extracellular signal-regulated protein kinase (ERK) pathway. Pharmacol Biochem Behav 94(1):88–97. doi:10.1016/j.pbb.2009.07.013 S0091-3057(09)00236-6 [pii]

    Google Scholar 

  • Zhang XJ, Li Z, Chung EK, Zhang HQ, Xu HX, Sung JJ, Bian ZX (2009b) Activation of extracellular signal-regulated protein kinase is associated with colorectal distension-induced spinal and supraspinal neuronal response and neonatal maternal separation-induced visceral hyperalgesia in rats. J Mol Neurosci 37(3):274–287. doi:10.1007/s12031-008-9134-y

    CAS  PubMed  Google Scholar 

  • Zhang XJ, Li Z, Leung WM, Liu L, Xu HX, Bian ZX (2008) The analgesic effect of paeoniflorin on neonatal maternal separation-induced visceral hyperalgesia in rats. J Pain 9(6):497–505. doi:10.1016/j.jpain.2007.12.009S1526-5900(08)00352-0 [pii]

    Google Scholar 

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Acknowledgments

Funding from Science Foundation Ireland (10/IN.1/B2976 and 05/YI2/B686) and the Irish Research Council for Science, Engineering and Technology is gratefully acknowledged.

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Authors and Affiliations

  1. Pharmacology and Therapeutics, School of Medicine, NCBES Galway Neuroscience Centre and Centre for Pain Research, National University of Ireland, University Road, Galway, Ireland

    Weredeselam M. Olango & David P. Finn

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  1. Weredeselam M. Olango
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  2. David P. Finn
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Correspondence to David P. Finn .

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Editors and Affiliations

  1. University of Kentucky Medical Center, Lexington, Kentucky, USA

    Bradley K. Taylor

  2. Centre for Pain Research, National University of Ireland, Galway, Ireland

    David P. Finn

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Olango, W.M., Finn, D.P. (2014). Neurobiology of Stress-Induced Hyperalgesia. In: Taylor, B., Finn, D. (eds) Behavioral Neurobiology of Chronic Pain. Current Topics in Behavioral Neurosciences, vol 20. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7854_2014_302

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