Cellular Mechanisms Underlying Neuronal Excitability during Morphine Withdrawal in Physical Dependence: Lessons from the Magnocellular Oxytocin System

References

• Abbadie, C., Pan, Y.X. and Pasternak, G.W. (2000) Differential distribution in rat brain of m-opioid receptor carboxy terminal splice variants MOR-1C-like and MOR-1-like immunoreactivity: evidence for region-specific processing, J. Comp. Neurol. 419, 244–256.
   PubMed Web of Science ®Google Scholar
• Akaoka, H. and Aston-Jones, G. (1991) Opiate withdrawal-induced hyperactivity of locus coeruleus neurons is substantially mediated by augmented excitatory amino acid input, J. Neurosci. 11, 3830–3839.
   PubMed Web of Science ®Google Scholar
• Andrew, R.D. and Dudek, F.E. (1983) Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism, Science 221, 1050–1052.
   PubMed Web of Science ®Google Scholar
• Antonio, M.J., Vargas, M.L., Fuente, T., Del Rio, G.J. and Milane´s, M.V. (1990) Plasma b-endorphin and cortisol levels in morphine-tolerant rats and in naloxone-induced withdrawal, Eur. J. Pharmacol. 182, 117–123.
   PubMed Web of Science ®Google Scholar
• Armstrong, W.E., Smith, B.N. and Tian, M. (1994) Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro, J. Physiol. 475, 115–128.
   Web of Science ®Google Scholar
• Belin, V. and Moos, F. (1986) Paired recordings from supraoptic and paraventricular oxytocin cells in suckled rats: recruitment and synchronization, J. Physiol. 377, 369–390.
   PubMed Web of Science ®Google Scholar
• Bicknell, R.J., Leng, G., Lincoln, D.W. and Russell, J.A. (1988) Naloxone excites oxytocin neurones in the supraoptic nucleus of lactating rats after chronic morphine treatment, J. Physiol. 396, 297–317.
   PubMed Web of Science ®Google Scholar
• Blackburn-Munro, G., Brown, C.H., Neumann, I.D., Landgraf, R. and Russell, J.A. (2000) Verapamil prevents withdrawal excitation of oxytocin neurones in morphine-dependent rats, Neuropharmacology 39, 1596–1607.
   PubMed Web of Science ®Google Scholar
• Bonci, A. and Williams, J.T. (1997) Increased probability of GABA release during withdrawal from morphine, J. Neurosci. 17, 796–803.
   PubMed Web of Science ®Google Scholar
• Bourque, C.W. (1986) Calcium-dependent spike after-current induces burst firing in magnocellular neurosecretory cells, Neurosci. Lett. 70, 204–209.
   PubMed Web of Science ®Google Scholar
• Breton, C. and Zingg, H.H. (1997) Expression and region-specific regulation of the oxytocin receptor gene in rat brain, Endocrinology 138, 1857–1862.
   PubMed Web of Science ®Google Scholar
• Brown, C.H. and Bourque, C.W. (2004) Autocrine feedback inhibition of plateau potentials terminates phasic bursts in magnocellular neurosecretory cells, J. Physiol. 557, 949–960.
   PubMed Web of Science ®Google Scholar
• Brown, C.H. and Leng, G. (2000) In vivo modulation of post-spike excitability in vasopressin cells by k-opioid receptor activation, J. Neuroendocrinol. 12, 711–714.
   PubMed Web of Science ®Google Scholar
• Brown, C.H., Munro, G., Murphy, N.P., Leng, G. and Russell, J.A. (1996) Activation of oxytocin neurones by systemic cholecystokinin is unchanged by morphine dependence or withdrawal excitation in the rat, J. Physiol. 496, 787–794.
   PubMed Web of Science ®Google Scholar
• Brown, C.H., Munro, G., Johnstone, L.E., Robson, A.C., Landgraf, R. and Russell, J.A. (1997) Oxytocin neurone autoexcitation during morphine withdrawal in anaesthetized rats, Neuroreport 8, 951–955.
   PubMed Web of Science ®Google Scholar
• Brown, C.H., Murphy, N.P., Munro, G., Ludwig, M., Bull, P.M., Leng, G. and Russell, J.A. (1998) Interruption of central noradrenergic pathways and morphine withdrawal excitation of oxytocin neurones in the rat, J. Physiol. 507, 831–842.
   PubMed Web of Science ®Google Scholar
• Brown, C.H., Johnstone, L.E., Murphy, N.P., Leng, G. and Russell, J.A. (2000a) Local injection of pertussis toxin attenuates morphine withdrawal excitation of rat supraoptic nucleus neurones, Brain Res. Bull. 52, 115–121.
   PubMed Web of Science ®Google Scholar
• Brown, C.H., Russell, J.A. and Leng, G. (2000b) Opioid modulation of magnocellular neurosecretory cell activity, Neurosci. Res. 36, 97–120.
   PubMed Web of Science ®Google Scholar
• Brussaard, A.B., Kits, K.S. and de Vlieger, T.A. (1996) Postsynaptic mechanism of depression of GABAergic synapses by oxytocin in the supraoptic nucleus of immature rat, J. Physiol. 497, 495–507.
   PubMed Web of Science ®Google Scholar
• Bull, P.M., Ludwig, M., Blackburn-Munro, G.J., Delgado-Cohen, H., Brown, C.H. and Russell, J.A. (2003) The role of nitric oxide in morphine dependence and withdrawal excitation of rat oxytocin neurons, Eur. J. Neurosci. 18, 2545–2551.
   PubMed Web of Science ®Google Scholar
• Buller, K.M., Dayas, C.V. and Day, T.A. (2003) Descending pathways from the paraventricular nucleus contribute to the recruitment of brainstem nuclei following a systemic immune challenge, Neuroscience 118, 189–203.
   PubMed Web of Science ®Google Scholar
• Childers, S.R. (1991) Opioid receptor-coupled second messenger systems, Life Sci. 48, 1991–2003.
   PubMed Web of Science ®Google Scholar
• Coombes, J.E., Robinson, I.C., Antoni, F.A. and Russell, J.A. (1991) Release of oxytocin into blood and into cerebrospinal fluid induced by naloxone in anaesthetized morphine-dependent rats: The role of the paraventricular nucleus, J. Neuroendocrinol. 3, 551–561.
   PubMed Web of Science ®Google Scholar
• Cui, S.S., Bowen, R.C., Gu,G.B., Hannesson, D.K., Yu, P.H. and Zhang, X. (2001) Prevention of cannabinoid withdrawal syndrome by lithium: involvement of oxytocinergic neuronal activation, J. Neurosci. 21, 9867–9876.
   PubMed Web of Science ®Google Scholar
• Decavel, C. and Van den Pol, A.N. (1990) GABA: a dominant neurotransmitter in the hypothalamus, J. Comp. Neurol. 302, 1019–1037.
   PubMed Web of Science ®Google Scholar
• Di, S., Malcher-Lopes, R., Halmos, K.C. and Tasker, J.G. (2003) Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism, J. Neurosci. 23, 4850–4857.
   PubMed Web of Science ®Google Scholar
• Ebner, K., Wotjak, C.T., Landgraf, R. and Engelmann, M. (2000) A single social defeat experience selectively stimulates the release of oxytocin, but not vasopressin, within the septal brain area of male rats, Brain Res. 872, 87–92.
   PubMed Web of Science ®Google Scholar
• Engelmann, M. and Ludwig, M. (2004) The activity of the hypothalamoneurohypophysial system in response to acute stressor exposure: neuroendocrine and electrophysiological observations, Stress 7 (this issue).
   Google Scholar
• Faggiano, F., Vigna-Taglianti, F., Versino, E. and Lemma, P. (2003) Methadone maintenance at different dosages for opioid dependence, Cochrane. Database Syst. Rev., CD002208.
   Google Scholar
• Fuertes, G., Laorden, M.L. and Milane´s, M.V. (2000a) Noradrenergic and dopaminergic activity in the hypothalamic paraventricular nucleus after naloxone-induced morphine withdrawal, Neuroendocrinology 71, 60–67.
   PubMed Web of Science ®Google Scholar
• Fuertes, G., Milane´s, M.V., Rodriguez-Gago, M., Mar?´n, M.T. and Laorden, M.L. (2000b) Changes in hypothalamic paraventricular nucleus catecholaminergic activity after acute and chronic morphine administration, Eur. J. Pharmacol. 388, 49–56.
   Google Scholar
• Gonzalvez, M.L., Milane´s, M.V., Martinez-Pin˜ero, M.G., Mar?´n, M.T. and Vargas, M.L. (1994) Effects of intracerebroventricular clonidine on the hypothalamic noradrenaline and plasma corticosterone levels of opiate naive rats and after naloxone-induced withdrawal, Brain Res. 647, 199–203.
   Google Scholar
• Greffrath,W., Martin, E., Reuss, S. and Boehmer, G. (1998) Components of after-hyperpolarization in magnocellular neurones of the rat supraoptic nucleus in vitro, J. Physiol. 513, 493–506.
   Web of Science ®Google Scholar
• Grudt, T.J. and Williams, J.T. (1995) Opioid receptors and the regulation of ion conductances, Rev. Neurosci. 6, 279–286.
   PubMed Web of Science ®Google Scholar
• Hack, S.P., Vaughan, C.W. and Christie, M.J. (2003) Modulation of GABA release during morphine withdrawal in midbrain neurons in vitro, Neuropharmacology 45, 575–584.
   Google Scholar
• Hatakeyama, S., Kawai, Y., Ueyama, T. and Senba, E. (1996) Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express Fos following stress stimuli, J. Chem. Neuroanat. 11, 243–256.
   PubMed Web of Science ®Google Scholar
• Ibragimov, R., Kovacs, G.L., Szabo, G. and Telegdy, G. (1987) Microinjection of oxytocin into limbic-mesolimbic brain structures disrupts heroin self-administration behavior: a receptor-mediated event?, Life Sci. 41, 1265–1271.
   PubMed Web of Science ®Google Scholar
• Inenaga, K., Nagatomo, T., Nakao, K., Yanaihara, N. and Yamashita, H. (1994) Kappa-selective agonists decrease postsynaptic potentials and calcium components of action potentials in the supraoptic nucleus of rat hypothalamus in vitro, Neuroscience 58, 331–340.
   Google Scholar
• Jhamandas, J.H., Harris, K.H., Petrov, T. and Jhamandas, K.H. (1996) Activation of nitric oxide-synthesizing neurones during precipitated morphine withdrawal, Neuroreport 7, 2843–2846.
   PubMed Web of Science ®Google Scholar
• Johnstone, L.E., Brown, C.H., Meeren, H.K., Vuijst, C.L., Brooks, P.J., Leng, G. and Russell, J.A. (2000) Local morphine withdrawal increases c-fos gene, Fos protein, and oxytocin gene expression in hypothalamic magnocellular neurosecretory cells, J. Neurosci. 20, 1272–1280.
   PubMed Web of Science ®Google Scholar
• Kadowaki, K., Kishimoto, J., Leng, G. and Emson, P.C. (1994) Up-regulation of nitric oxide synthase (NOS) gene expression together with NOS activity in the rat hypothalamo-hypophysial system after chronic salt loading: evidence of a neuromodulatory role of nitric oxide in arginine vasopressin and oxytocin secretion, Endocrinology 134, 1011–1017.
   PubMed Web of Science ®Google Scholar
• Kirkpatrick, K. and Bourque, C.W. (1996) Activity dependence and functional role of the apamin-sensitive Kþ current in rat supraoptic neurones in vitro, J. Physiol. 494, 389–398.
   Web of Science ®Google Scholar
• Kombian, S.B., Mouginot, D. and Pittman, Q.J. (1997) Dendritically released peptides act as retrograde modulators of afferent excitation in the supraoptic nucleus in vitro, Neuron 19, 903–912.
   Google Scholar
• Kovacs, G.L., Laczi, F., Vecsernyes, M., Hodi, K., Telegdy, G. and Laszlo, F.A. (1987) Limbic oxytocin and arginine 8-vasopressin in morphine tolerance and dependence, Exp. Brain Res. 65, 307–311.
   PubMed Web of Science ®Google Scholar
• Lang, R.E., Heil, J.W., Ganten, D., Hermann, K., Unger, T. and Rascher, W. (1983) Oxytocin unlike vasopressin is a stress hormone in the rat, Neuroendocrinology 37, 314–316.
   PubMed Web of Science ®Google Scholar
• Laorden, M.L., Fuertes, G., Gonza´lez-Cuello, A. and Milane´s, M.V. (2000) Changes in catecholaminergic pathways innervating paraventricular nucleus and pituitary-adrenal axis response during morphine dependence: implication of a1- and a2-adrenoceptors, J. Pharmacol. Exp. Ther. 293, 578–584.
   PubMed Web of Science ®Google Scholar
• Leng, G. (2000) Oxytocin, In: Fink, G., ed., Encyclopedia of Stress (Academic Press, San Diego), pp 109–114.
   Google Scholar
• Leng, G., Blackburn, R.E., Dyball, R.E. and Russell, J.A. (1989) Role of anterior peri-third ventricular structures in the regulation of supraoptic neuronal activity and neurohypophysial hormone secretion in the rat, J. Neuroendocrinol. 1, 35–46.
   PubMed Web of Science ®Google Scholar
• Leng, G., Brown, C.H., Bull, P.M., Brown, D., Scullion, S., Currie, J., Blackburn-Munro, R.E., Feng, J., Onaka, T., Verbalis, J.G., Russell, J.A. and Ludwig, M. (2001) Responses of magnocellular neurons to osmotic stimulation involves coactivation of excitatory and inhibitory input: an experimental and theoretical analysis, J. Neurosci. 21, 6967–6977.
   PubMed Web of Science ®Google Scholar
• Li, J., You, Z., Chen, Z., Song, C. and Lu, C. (2001) Chronic morphine treatment inhibits oxytocin release from the supraoptic nucleus slices of rats, Neurosci. Lett. 300, 54–58.
   PubMed Web of Science ®Google Scholar
• Lichtman, A.H. and Martin, B.R. (2002) Marijuana withdrawal syndrome in the animal model, J. Clin. Pharmacol. 42, 20S–27S.
   Google Scholar
• Liu, Q.S., Jia, Y.S. and Ju, G. (1997) Nitric oxide inhibits neuronal activity in the supraoptic nucleus of the rat hypothalamic slices, Brain Res. Bull. 43, 121–125.
   PubMed Web of Science ®Google Scholar
• Liu, Q.S., Han, S., Jia, Y.S. and Ju, G. (1999) Selective modulation of excitatory transmission by m-opioid receptor activation in rat supraoptic neurons, J. Neurophysiol. 82, 3000–3005.
   PubMed Web of Science ®Google Scholar
• Ludwig, M. (1998) Dendritic release of vasopressin and oxytocin, J. Neuroendocrinol. 10, 881–895.
   PubMed Web of Science ®Google Scholar
• Ludwig, M., Brown, C.H., Russell, J.A. and Leng, G. (1997) Local opioid inhibition and morphine dependence of supraoptic nucleus oxytocin neurones in the rat in vivo, J. Physiol. 505, 145–152.
   Web of Science ®Google Scholar
• Ludwig, M., Sabatier, N., Bull, P.M., Landgraf, R., Dayanithi, G. and Leng, G. (2002) Intracellular calcium stores regulate activitydependent neuropeptide release from dendrites, Nature 418, 85–89.
   PubMed Web of Science ®Google Scholar
• Mansour, A., Fox, C.A., Burke, S., Akil, H. and Watson, S.J. (1995) Immunohistochemical localization of the cloned m-opioid receptor in the rat CNS, J. Chem. Neuroanat. 8, 283–305.
   PubMed Web of Science ®Google Scholar
• McKinley, M.J., Pennington, G.L. and Oldfield, B.J. (1996) Anteroventral wall of the third ventricle and dorsal lamina terminalis: headquarters for control of body fluid homeostasis?, Clin. Exp. Pharmacol. Physiol. 23, 271–281.
   PubMed Web of Science ®Google Scholar
• Milane´s, M.V., Laorden, M.L., Chapleur-Chateau, M. and Burlet, A. (1998) Alterations in corticotropin-releasing factor and vasopressin content in rat brain during morphine withdrawal: correlation with hypothalamic noradrenergic activity and pituitary-adrenal response, J. Pharmacol. Exp. Ther. 285, 700–706.
   PubMed Web of Science ®Google Scholar
• Muller, W., Hallermann, S. and Swandulla, D. (1999) Opioidergic modulation of voltage-activated Kþ currents in magnocellular neurons of the supraoptic nucleus in rat, J. Neurophysiol. 81, 1617–1625.
   PubMed Web of Science ®Google Scholar
• Murphy, N.P., Onaka, T., Brown, C.H. and Leng, G. (1997) The role of afferent inputs to supraoptic nucleus oxytocin neurons during naloxone-precipitated morphine withdrawal in the rat, Neuroscience 80, 567–577.
   PubMed Web of Science ®Google Scholar
• Nye, H.E. and Nestler, E.J. (1996) Induction of chronic Fos-related antigens in rat brain by chronic morphine administration, Mol. Pharmacol. 49, 636–645.
   PubMed Web of Science ®Google Scholar
• Ogata, N. and Matsuo, T. (1984) Pharmacological characterization of the magnocellular neuroendocrine cells of the guinea pig supraoptic nucleus in vitro, Neuropharmacology 23, 1215–1218.
   Google Scholar
• Onaka, T., Luckman, S.M., Antonijevic, I., Palmer, J.R. and Leng, G. (1995a) Involvement of the noradrenergic afferents from the nucleus tractus solitarii to the supraoptic nucleus in oxytocin release after peripheral cholecystokinin octapeptide in the rat, Neuroscience 66, 403–412.
   PubMed Web of Science ®Google Scholar
• Onaka, T., Luckman, S.M., Guevara-Guzman, R., Ueta, Y., Kendrick, K. and Leng, G. (1995b) Presynaptic actions of morphine: blockade of cholecystokinin-induced noradrenaline release in the rat supraoptic nucleus, J. Physiol. 482, 69–79.
   PubMed Web of Science ®Google Scholar
• Ozaki, M., Shibuya, I., Kabashima, N., Isse, T., Noguchi, J., Ueta, Y., Inoue, Y., Shigematsu, A. and Yamashita, H. (2000) Preferential potentiation by nitric oxide of spontaneous inhibitory postsynaptic currents in rat supraoptic neurones, J. Neuroendocrinol. 12, 273–281.
   PubMed Web of Science ®Google Scholar
• Pow, D.V. and Morris, J.F. (1989) Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis, Neuroscience 32, 435–439.
   PubMed Web of Science ®Google Scholar
• Pumford, K.M., Leng, G. and Russell, J.A. (1991) Morphine actions on supraoptic oxytocin neurones in anaesthetized rats: tolerance after i.c.v. morphine infusion, J. Physiol. 440, 437–454.
   Web of Science ®Google Scholar
• Rinaman, L., Hoffman, G.E., Dohanics, J., Le, W.W., Stricker, E.M. and Verbalis, J.G. (1995) Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats, J. Comp. Neurol. 360, 246–256.
   PubMed Web of Science ®Google Scholar
• Robinson, S.E. (2002) Buprenorphine: an analgesic with an expanding role in the treatment of opioid addiction, CNS Drug Rev. 8, 377–390.
   PubMedGoogle Scholar
• Russell, J.A., Neumann, I. and Landgraf, R. (1992a) Oxytocin and vasopressin release in discrete brain areas after naloxone in morphine-tolerant and -dependent anesthetized rats: push-pull perfusion study, J. Neurosci. 12, 1024–1032.
   PubMed Web of Science ®Google Scholar
• Russell, J.A., Pumford, K.M. and Bicknell, R.J. (1992b) Contribution of the region anterior and ventral to the third ventricle to opiate withdrawal excitation of oxytocin secretion, Neuroendocrinology 55, 183–192.
   PubMed Web of Science ®Google Scholar
• Russell, J.A., Leng, G. and Bicknell, R.J. (1995) Opioid tolerance and dependence in the magnocellular oxytocin system: a physiological mechanism?, Exp. Physiol. 80, 307–340.
   PubMed Web of Science ®Google Scholar
• Smart, D., Smith, G. and Lambert, D.G. (1995) Mu-opioids activate phospholipase C in SH-SY5Y human neuroblastoma cells via calcium-channel opening, Biochem. J. 305, 577–581.
   PubMed Web of Science ®Google Scholar
• Soldo, B.L. and Moises, H.C. (1998) m-Opioid receptor activation inhibits N- and P-type Ca2þ channel currents in magnocellular neurones of the rat supraoptic nucleus, J. Physiol. 513, 787–804.
   PubMed Web of Science ®Google Scholar
• Srisawat, R., Ludwig, M., Bull, P.M., Douglas, A.J., Russell, J.A. and Leng, G. (2000) Nitric oxide and the oxytocin system in pregnancy, J. Neurosci. 20, 6721–6727.
   PubMed Web of Science ®Google Scholar
• Stern, J.E. and Ludwig, M. (2001) NO inhibits supraoptic oxytocin and vasopressin neurons via activation of GABAergic synaptic inputs, Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R1815–R1822.
   PubMed Web of Science ®Google Scholar
• Tyrey, L. and Murphy, L.L. (1988) Inhibition of suckling-induced milk ejections in the lactating rat by delta 9-tetrahydrocannabinol, Endocrinology 123, 469–472.
   PubMed Web of Science ®Google Scholar
• Van Den Brink, W., Goppel, M. and Van Ree, J.M. (2003) Management of opioid dependence, Curr. Opin. Psychiatr. 16, 297–304.
   Web of Science ®Google Scholar
• Van den Pol, A.N., Wuarin, J.P. and Dudek, F.E. (1990) Glutamate, the dominant excitatory transmitter in neuroendocrine regulation, Science 250, 1276–1278.
   PubMed Web of Science ®Google Scholar
• Vigano, D., Grazia, C.M., Rubino, T., Fezza, F., Vaccani, A., Di, M.V. and Parolaro, D. (2003) Chronic morphine modulates the contents of the endocannabinoid, 2-arachidonoyl glycerol, in rat brain, Neuropsychopharmacology 28, 1160–1167.
   PubMed Web of Science ®Google Scholar
• Wakerley, J.B., Noble, R. and Clarke, G. (1983) Effects of morphine and D-Ala, D-Leu enkephalin on the electrical activity of supraoptic neurosecretory cells in vitro, Neuroscience 10, 73–81.
   Google Scholar
• Wotjak, C.T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R. and Engelmann, M. (1998) Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons, Neuroscience 85, 1209–1222.
   PubMed Web of Science ®Google Scholar
• Yu, G.Z., Kaba, H., Okutani, F., Takahashi, S., Higuchi, T. and Seto, K. (1996) The action of oxytocin originating in the hypothalamic paraventricular nucleus on mitral and granule cells in the rat main olfactory bulb, Neuroscience 72, 1073–1082.
   PubMed Web of Science ®Google Scholar