Functional interactions between the paraventricular hypothalamic nucleus and raphe magnus. A comparative study of an integrated homeostatic analgesic mechanism

Neuroscience

Volumn 209, Issue , 2012, Pages 196-207

  Condes Lara M ^a,b   Rojas Piloni, G ^a   Martinez Lorenzana G ^a   Diez Martínez, D Condés ^c   Rodriguez Jimenez J ^a  

^a CENTRO DE FÍSICA APLICADA Y TECNOLOGÍA AVANZADA   (Mexico)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c UNIVERSIDAD AUTÓNOMA DE QUERÉTARO   (Mexico)

Author keywords

Analgesia; Homeostasis; Oxytocin; Pain mechanism; Rats

Indexed keywords

NALOXONE; OXYTOCIN ANTAGONIST;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED RESPONSE; HOMEOSTASIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; INNERVATION; LATENT PERIOD; MALE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; RECEPTIVE FIELD; SPINAL CORD NERVE CELL;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; NEURAL PATHWAYS; PAIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RAPHE NUCLEI; RATS; RATS, WISTAR; SPINAL CORD;

EID: 84859266300     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.02.032     Document Type: Article

References (42)

1. Arletti R., Benelli A., Bertolini A. Influence of oxytocin on nociception and morphine antinociception. Neuropeptides 1993, 24:125-129.
2. Breton J.D., Veinante P., Uhl-Bronner S., Vergnano A.M., Freund-Mercier M.J., Schlichter R., Poisbeau P. Oxytocin-induced antinociception in the spinal cord is mediated by a subpopulation of glutamatergic neurons in lamina I-II which amplify GABAergic inhibition. Mol Pain 2008, 29:4-19.
3. Budai D., Fields H.L. Endogenous opioid peptide acting at μ-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons. J Neurophysiol 1998, 79:677-687.
4. Buritova J., Larrue S., Aliaga M., Besson J.M., Colpaert F. Effects of the high-efficacy 5-HT1A receptor agonist, F 13640 in the formalin pain model: a c-Fos study. Eur J Pharmacol 2005, 514:121-130.
5. Cannon J.T., Prieto G.J., Lee A., Liebeskind J.C. Evidence for opioid and non-opioid forms of stimulation-produced analgesia in the rat. Brain Res 1982, 243:315-321.
6. Condés-Lara M., González N.M., Martínez-Lorenzana G., Delgado O.L., Freund-Mercier M.J. Actions of oxytocin and interactions with glutamate on spontaneous and evoked dorsal spinal cord neuronal activities. Brain Res 2003, 976:75-81.
7. Condés-Lara M., Maie I.A., Dickenson A.H. Oxytocin actions on afferent evoked spinal cord neuronal activities in neuropathic but not in normal rats. Brain Res 2005, 1045:124-133.
8. Condés-Lara M., Martínez-Lorenzana G., Rojas-Piloni G., Rodríguez-Jiménez J. Branched oxytocinergic innervations from the paraventricular hypothalamic nuclei to superficial layers in the spinal cord. Brain Res 2007, 1160:20-29.
9. Condés-Lara M., Rojas-Piloni G., Martínez-Lorenzana G., López-Hidalgo M., Rodríguez-Jiménez J. Hypothalamospinal oxytocinergic antinociception is mediated by GABAergic and opiate neurons that reduce A-delta and C fiber primary afferent excitation of spinal cord cells. Brain Res 2009, 1247:38-49.
10. Condés-Lara M., Rojas-Piloni G., Martínez-Lorenzana G., Rodríguez-Jiménez J. Paraventricular hypothalamic oxytocinergic cells responding to noxious stimulation and projecting to the spinal dorsal horn represent a homeostatic analgesic mechanism. Eur J Neurosci 2009, 30:1056-1063.
11. Condés-Lara M., Rojas-Piloni G., Martínez-Lorenzana G., Rodríguez-Jiménez J., López-Hidalgo M., Freund-Mercier M.J. Paraventricular hypothalamic influences on spinal nociceptive processing. Brain Res 2006, 1081:126-137.
12. Fields H.L., Basbaum A.I., Heinricher M.M. Central nervous system mechanisms of pain modulation. Wall and Melzack's textbook of pain 2006, 125-142. Elsevier, London. 5th ed. S. McMahon, M. Koltzenburg (Eds.).
13. Fields H.L., Bry J., Hentall I., Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 1983, 3:2545-2552.
14. Ge Y., Lundeberg T., Yu L.C. Blockade effect of mu and kappa opioid antagonists on the anti-nociception induced by intra-periaqueductal grey injection of oxytocin in rats. Brain Res 2002, 927:204-207.
15. Geerling J.C., Shin J.-W., Chimenti P.C., Loewy A.D. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol 2010, 518:1460-1499.
16. Heinricher M.M., Tavares I., Leith J.L., Lumb B.M. Descending control of nociception: specificity, recruitment and plasticity. Brain Res Rev 2009, 60:214-225.
17. Kishi R., Bongiovanni R., de Nadai T.R., Freitas R.L., de Oliveira R., Ferreira C.M., Coimbra N.C. Dorsal raphe nucleus and locus coeruleus neural networks and the elaboration of the sweet-substance-induced antinociception. Neurosci Lett 2006, 395:12-17.
18. Larsen P.J., Hay-Schmidt A., Vrang N., Mikkelsen J.D. Origin of projections from the midbrain raphe nuclei to the hypothalamic paraventricular nucleus in the rat: a combined retrograde and anterograde tracing study. Neuroscience 1996, 70:963-988.
19. Luiten P.J., ter Horst G.J., Karst H., Steffens A.A. The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res 1985, 329:374-378.
20. Martínez-Lorenzana G., Espinosa-López L., Carranza M., Aramburo C., Paz-Tres C., Rojas-Piloni G., Condés-Lara M. PVN electrical stimulation prolongs withdrawal latencies and releases oxytocin in cerebrospinal fluid, plasma, and spinal cord tissue in intact and neuropathic rats. Pain 2008, 140:265-273.
21. Millar J., Williams G.V. Effects of iontophoresis of noradrenaline and stimulation of the periaqueductal gray on single-unit activity in the rat superficial dorsal horn. J Comp Neurol 1989, 287:119-133.
22. Miranda-Cardenas Y., Rojas-Piloni G., Martínez-Lorenzana G., Rodríguez-Jiménez J., López-Hidalgo M., Freund-Mercier M.J., Condés-Lara M. Oxytocin and electrical stimulation of the paraventricular hypothalamic nucleus produce antinociceptive effects that are reversed by an oxytocin antagonist. Pain 2006, 122:182-189.
23. Oliveras J.L., Sierralta F., Fardin V., Besson J.M. Involvement of serotoninergic systems in analgesia induced by electrical stimulation of brain stem areas. J Physiol (Paris) 1981, 77:473-482.
24. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Elsevier Academic, San Diego. 6th ed.
25. Pinto-Ribeiro F., Ansah O.B., Almeida A., Pertovaara A. Influence of arthritis on descending modulation of nociception from the paraventricular nucleus of the hypothalamus. Brain Res 2008, 1197:63-75.
26. Pinto-Ribeiro F., Ansah O.B., Almeida A., Pertovaara A. Response properties of nociceptive neurons in the caudal ventrolateral medulla (CVLM) in monoarthritic and healthy control rats: modulation of responses by the paraventricular nucleus of the hypothalamus (PVN). Brain Res Bull 2011, 86:82-90.
27. Prieto G.J., Cannon J.T., Liebeskind J.C. Nucleus raphe magnus lesions disrupt stimulation-produced analgesia from ventral but not in dorsal midbrain areas in the rat. Brain Res 1983, 261:53-57.
28. Rojas-Piloni G., López-Hidalgo M., Martínez-Lorenzana G., Rodríguez-Jiménez J., Condés-Lara M. GABA-mediated oxytocinergic inhibition in dorsal horn neurons by hypothalamic paraventricular nucleus stimulation. Brain Res 2007, 1137:69-77.
29. Rojas-Piloni G., Martínez-Lorenzana G., DelaTorre S., Condés-Lara M. Nociceptive spinothalamic tract and postsynaptic dorsal column neurons are modulated by paraventricular hypothalamic activation. Eur J Neurosci 2008, 28:546-558.
30. Rousselot P., Papadopoulos G., Merighi A., Poulain D.A., Theodosis D.T. Oxytocinergic innervation of the rat spinal cord. An electron microscopic study. Brain Res 1990, 529:178-184.
31. Saper C.B., Loewy A.D., Swanson L.W., Cowan W.M. Direct hypothalamo-autonomic connections. Brain Res 1976, 117:305-312.
32. Shiraishi T., Onoe M., Kojima T., Sameshima Y., Kageyama T. Effects of hypothalamic paraventricular nucleus: electrical stimulation produce marked analgesia in rats. Neurobiology 1995, 3:393-403.
33. Stamford J.A. Descending control of pain. Br J Anaesth 1995, 75:217-227.
34. Swanson L.W., Kuypers H.G. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 1980, 194:555-570.
35. Swanson L.W., McKellar S. The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey. J Comp Neurol 1979, 188:87-106.
36. Vanegas H., Schaible H.G. Descending control of persistent pain: inhibitory or facilitatory?. Brain Res Rev 2004, 46:295-309.
37. Willcockson W.S., Gerhart K.D., Cargill C.L., Willis W.D. Effects of biogenic amines on raphe-spinal tract cells. J Pharmacol Exp Ther 1983, 225:637-645.
38. Yang J. Intrathecal administration of oxytocin induces analgesia in low back pain involving the endogenous opiate peptide system. Spine 1994, 19:867-871.
39. Ying B., Lü N., Zhang Y.Q., Zhao Z.Q. Involvement of spinal glia in tetanically sciatic stimulation-induced bilateral mechanical allodynia in rats. Biochem Biophys Res Commun 2006, 340:1264-1272.
40. Yirmiya R., Ben-Eliyahu S., Shavit Y., Marek P., Liebeskind J.C. Stimulation of the hypothalamic paraventricular nucleus produces analgesia not mediated by vasopressin or endogenous opioids. Brain Res 1990, 537:169-174.
41. Zheng J.Q., Seki M., Hayakawa T., Ito H., Zyo K. Descending projections from paraventricular hypothalamic nucleus to the spinal cord: anterograde tracing study in the rat. Okajimas Folia Anat Jpn 1995, 72:119-135.
42. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.