Skip to main content

Advertisement

SpringerLink
Log in

Role of thalamic ventral posterolateral nucleus histamine H2 and opiate receptors in modulation of formalin-induced muscle pain in rats

  • Original article
  • Published:
Pharmacological Reports Aims and scope Submit manuscript

Abstract

Background

Histamine and opiate systems contribute to supraspinal processing of pain. In the present study, we investigated the effects of microinjection of histamine and agonists and antagonists of histamine H2 and opiate receptors into the thalamic ventral posterolateral nucleus on muscle pain in rats.

Methods

The thalamic ventral posterolateral nuclei were bilaterally implanted with two guide cannulas. Muscle pain was induced by intramuscular injection of a diluted formalin solution (2.5%, 50 μl) into the belly of gastrocnemius muscle, and pain-related behaviors including paw licking duration and paw flinching number were recorded at five-min blocks for 60 min.

Results

Formalin produced a biphasic pattern of pain-related behaviors. Ranitidine (a histamine H2 receptor antagonist) alone did not affect pain intensity, whereas it prevented the antinociceptive activities of histamine, dimaprit (a histamine H2 receptor agonist) and morphine (an opiate receptor agonist). Naloxone (an opiate receptor antagonist) alone increased pain, and inhibited histamine-, dimaprit-, and morphine-induced antinociception. Locomotor activity was not changed with these chemicals.

Conclusions

Our results showed an interaction between histamine H2 and opiate receptors at the thalamic ventral posterolateral nucleus in modulation of muscle pain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Haas HL, Sergeeva OA, Selbach O. Histamine in the nervous system. Physiol Rev 2008;88(3):1183–241.

    Article  CAS  PubMed  Google Scholar 

  2. Schneider EH, Neumann D, Seifert R. Modulation of behavior by the histaminergic system: lessons from H1R- and H2R-deficient mice. Neurosci Biobehav Rev 2014;42:259–66.

    Article  CAS  Google Scholar 

  3. Schneider EH, Neumann D, Seifert R. Modulation of behavior by the histaminergic system: lessons from HDC-, H3R- and H4R-deficient mice. Neurosci Biobehav Rev 2014;47:101–21.

    Article  PubMed  CAS  Google Scholar 

  4. Catadli M, Borrielo F, Granata F, Annunziato L, Morane G. Histamine receptors and antihistamines: from discovery to clinical applications. Chem Immunol Allergy 2014;100:214–26.

    Article  Google Scholar 

  5. Erfanparast A, Tamaddonfard E, Taati M, Dabaghi M. Role of the thalamic submedius nucleus histamine H1 and H2 and opioid receptors in modulation of formalin-induced orofacial pain in rats. Naunyn Schmiedebergs Arch Pharmacol 2015;388(10):1089–96.

    Article  CAS  PubMed  Google Scholar 

  6. Tamaddonfard E, Erfanparast A, Ghasemi H, Henareh-Chreh F, Hadidi M, Mirzakhani N, et al. The role of histamine H1, H2 and H3 receptors of ventral posteromedial nucleus of thalamus in modulation of trigeminal pain. Eur J Pharmacol 2016;791:696–702.

    Article  CAS  PubMed  Google Scholar 

  7. Hamzeh-Gooshchi N, Tamaddonfard E, Farshid AA. Effects of microinjection of histamine into the anterior cigulate cortex on pain-related behaviors induced by formalin in rats. Pharmacol Rep 2015;67(3):593–9.

    Article  CAS  PubMed  Google Scholar 

  8. Tamaddonfard E, Hamzeh-Gooshchi N. Effects of administration of histamine and its H1, H2, and H3 receptor antagonists into the primary somatosensory cortex on inflammatory pain in rats. Iran J Basic Med Sci 2014;17(1):55–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Khalilzadeh E, Tamaddonfard E, Farshid AA, Erfanparast A. Microinjection of histamine into the dentate gyrus produces antinociception in the formalin test in rats. Pharmacol Biochem Behav 2010;97(2):325–32.

    Article  CAS  PubMed  Google Scholar 

  10. Bodnar RJ. Endogenous opiates and behavior: 2015. Peptides 2017;88:126–88.

    Article  CAS  PubMed  Google Scholar 

  11. Tamaddonfard E, Erfanparast A, Farshid AA, Khalilzadeh E. Interaction between histamine and morphine at the level of hippocampus in the formalin-induced orofacial pain in rats. Pharmacol Rep 2011;63(2):423–32.

    Article  CAS  PubMed  Google Scholar 

  12. Feng J, Jia N, Han LN, Huang FS, Xie YF, Liu J, etal. Microinjection of morphine into thalamus nucleus submedius depresses bee venom-induced inflammatory pain in the rat. J Pharm Pharmacol 2008;60(10):1355–63.

    Article  CAS  PubMed  Google Scholar 

  13. Argoff C. Mechanisms of transmission and pharmacologic management. Curr Med Res Opin 2011;27(10):2019–31.

    Article  CAS  PubMed  Google Scholar 

  14. Yen CT, Lu PL. Thalamus and pain. Acta Anaesthesiol Taiwan 2013;51(2):73–80.

    Article  PubMed  Google Scholar 

  15. Moustafa AA, McMullan DR, Rostron B, Hewedi DH, Haladjian HH. The thalamus as a key station and gatekeeper: relevance to brain disorders. Rev Neurosci 2017;28(2):203–18.

    Article  PubMed  Google Scholar 

  16. Ueda M, Iida Y, Tominaga A, Yoneyama T, Ogawa M, Magata Y, et al. Nicotinic acetylcholine receptorexpressed in the ventralposterolateral thalamic nucleus play an important role in anti-allodynic effects. Br J Pharmacol 2010;159(6):1201–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang JY, Huang J, Chang JY, Woodward DJ, Luo F. Morphine modulation of pain processing in medial and lateral pain pathways. Mol Pain 2009;5:60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Bergman S. Management of musculoskeletal pain. Best Pract Res Clin Rheumatol 2007;21(1):153–66.

    Article  PubMed  Google Scholar 

  19. Kehl U, Fairbanks CA. Experimental animal models of muscle pain analgesia. Excer Sport Sci Rev 2003;31(4):188–94.

    Article  Google Scholar 

  20. Sharma NK, Bylas JM, Liu H, Liu W, Wright DE. Acidic saline-induced primary and secondary hyperalgesia in mice. J Pain 2009;10(12):1231–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Radhakrishna R, Bement UK, Shyba D, Sluka KA, Kehl LJ. Models of muscle pain: carrageenan model and acidic saline model. Curr Protoc Pharmacol 2004, doi:https://doi.org/10.1002/0471141755ph0535s25 Chapter five: Unit 5.35.

  22. Lei J, Sun T, Lumb BM, You HJ. Roles of periaqueductal gray in descending facilitatory and inhibitory controls of intramuscular hypertonic saline induced muscle nociception. Exp Neurol 2014;257:88–94.

    Article  CAS  PubMed  Google Scholar 

  23. Lei J, You HJ. Endogenous descending facilitation and inhibition differ in control of intramuscularly induced persistent muscle nociception. Exp Neurol 2013;248:100–11.

    Article  PubMed  Google Scholar 

  24. You HJ, Lei J, Niu N, Yang L, Fan XL, Tjolsen A, et al. Specific thalamic nuclei function as novel ‘nociceptive discriminators’ in the endogenous control of nociception in rats. Neuroscience 2013;323:53–63.

    Article  CAS  Google Scholar 

  25. Karlstedt K, Senkas A, Ahman M, Panula P. Regional expression of the histamine H2 receptor in adult and developing rat brain. Neuroscience 2001;102(1):201–8.

    Article  CAS  PubMed  Google Scholar 

  26. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, et al. Mu, delta and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 1994;350(3):412–38.

    Article  CAS  PubMed  Google Scholar 

  27. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th edn San Diego: Elsevier Academic Press; 2007.

    Google Scholar 

  28. Tsiklauri N, Nazadze I, Gurtskaia G, Tsagareli MG. Antinociceptive tolerance to NSAIDs in the rat formalin test is mediated by the opioid mechanism. Pharmacol Rep 2017;69(1):168–75.

    Article  CAS  PubMed  Google Scholar 

  29. Potes CS, Pestana AC, Pontes M, Caramelo AS, Neto FL. Amylin modulates the formalin-induced tonic pain behaviors in rats. Eur J Pain 2016;20(10):1741–52.

    Article  CAS  PubMed  Google Scholar 

  30. Porro CA, Spatial Cavazzuti M. temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog Neurobiol 1993;41(5):565–607.

    Article  CAS  PubMed  Google Scholar 

  31. Puig S, Sorkin LS. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain 1996;64(2):345–55.

    Article  CAS  PubMed  Google Scholar 

  32. Laurin J, Pertici V, Dousset E, Marqueste T, Decherchi P. Group III and IV muscle afferents: role on central motor drive and clinical implication. Neuroscience 2015;290:543–51.

    Article  CAS  PubMed  Google Scholar 

  33. Jankowski MP, Rau KK, Ekmann KM, Anderson CE, Koerber HR. Comprehensive phenotyping of group III and IV muscle afferents in mouse. J Neurophysiol 2013;109(9):2374–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mense S. Algesic agents exciting muscle nociceptors. Exp Brain Res 2009;196(1):89–100.

    Article  CAS  PubMed  Google Scholar 

  35. Erfanparast A, Tamaddonfard E, Farshid AA, Khalilzadeh E. Effect of microinjection of histamine into the dorsal hippocampus on the orofacial formalin-induced pain in rats. Eur J Pharmacol 2010;627(1–3):119–23.

    Article  CAS  PubMed  Google Scholar 

  36. Panula P, Pirvola U, Auvinen S, Airaksinen MS. Histamine immunoreactive nerve fibers in the rat brain. Neuroscience 1989;28(3):585–610.

    Article  CAS  PubMed  Google Scholar 

  37. Thoburn KK, Hough LB, Nalwalk JW, Mischler SA. Histamine induced modulation of nociceptive responses. Pain 1994;58(1):29–37.

    Article  CAS  PubMed  Google Scholar 

  38. Wei H, Jin CY, Viisanen H, You HJ, Petrovaara A. Histamine in the locus coeruleus promotes descending noradrenergic inhibition of neuropathic hypersensitivity. Pharmacol Sci 2014;90:58–66.

    CAS  Google Scholar 

  39. Sittig N, Davidowa H. Histamine reduces firing and bursting of anterior and intralaminar thalamic neurons and activates striatal cells in anesthetized rats. Behav Brain Res 2001;24(2):137–43.

    Article  Google Scholar 

  40. Lee KH, Broberger C, Kim U, McCormick DA. Histamine modulates thalamocortical activity by activating a chloride conductance in ferret perigeniculate neurons. Proc Nati Acad Sci U S A 2004 2004;101(17):6716–21.

    Article  CAS  Google Scholar 

  41. Trescot AM, Datta S, Lee M, Hansen H. Opioid pharmacology. Pain Physician 2008;11(Suppl. 2):S133–53.

    PubMed  Google Scholar 

  42. Su YL, Huang J, Wang L, Wang JY, Luo F. The effects of morphine on basal neuronal activities in the lateral and medial pain pathways. Neurosci Lett 2012;525(2):173–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wong JC. Further study on the effects of histamine H2 receptor agonist and antagonists on restraint-induced antinociception in mice. Methods Find Exp Clin Pharmacol 1999;21(6):403–7.

    Article  CAS  PubMed  Google Scholar 

  44. Hough LB, Nalwalk JW. Inhibition of morphine antinociception by centrally administered histamine H2 receptor antagonists. Eur J Pharmacol 1992;215(1):69–74.

    Article  CAS  PubMed  Google Scholar 

  45. Xie YF, Huo FQ, Tang JS. Cerebral cortex modulation of pain. Acta Pharmacol Sin 2009;30(1):31–41.

    Article  CAS  PubMed  Google Scholar 

  46. Quintero GC. Advances in cortical modulation of pain. J Pain Res 2016;6:713–25.

    Google Scholar 

  47. Xiao Y, Lei J, Ye G, Xu H, You HJ. Role of thalamic nuclei in the modulation of Fos expression within cerebral cortex during hypertonic saline-induced muscle nociception. Neuroscience 2015;304:36–46.

    Article  CAS  PubMed  Google Scholar 

  48. Cortright DN, Matson DJ, Broom DC. New frontiers in assessing pain and analgesia in laboratory animals. Expert Opin Drug Discov 2008;3(9):1099–108.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Physiology, Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

    Hamid Ghasemi & Esmaeal Tamaddonfard

  2. Division of Anatomy, Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

    Farhad Soltanalinejad

Authors
  1. Hamid Ghasemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Esmaeal Tamaddonfard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Farhad Soltanalinejad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Esmaeal Tamaddonfard.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghasemi, H., Tamaddonfard, E. & Soltanalinejad, F. Role of thalamic ventral posterolateral nucleus histamine H2 and opiate receptors in modulation of formalin-induced muscle pain in rats. Pharmacol. Rep 69, 1393–1401 (2017). https://doi.org/10.1016/j.pharep.2017.05.001

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.pharep.2017.05.001

Keywords

Search

Navigation