Abstract
Aim:
The conditioned place preference (CPP) paradigm was used to investigate the effects of endogenous histamine on the processes leading to morphine-induced reward-seeking behavior in Sprague-Dawley rats.
Methods:
The model of CPP was used to assess the rewarding effect of morphine. The levels of histamine, glutamate, γ-aminobutyric acid (GABA), dopamine (DA) and 3,4-dihydroxyphenyl-acetic acid (DOPAC) in rat brains were measured with high-performance liquid chromatography. Immunohistochemistry technique was used to observe the morphological changes of neurons.
Results:
Intraperitoneal injection of morphine (2, 5 or 10 mg/kg) induced the development of CPP in a dose-dependent manner. In addition, morphine administrations (10 mg/kg) decreased the histamine content and reduced the number and size of histaminergic neurons in the tuberomammillary nucleus (TM), as well as markedly increasing the DOPAC/DA ratios in the ventral tegmental area (VTA) and nucleus accumbens (NAc). Intraperitoneal injection of histidine (50,100 or 200 mg/kg) dose-dependently inhibited the development of morphine-induced CPP. Bilateral lesions of the TM, which decreased the histamine levels in the VTA and NAc, potentiated the development of CPP induced by morphine (1 mg/kg, a dose that produced no appreciable effect when given alone) and increased the DOPAC/DA ratios in the VTA and NAc, but did not change the glutamate or GABA levels in these nuclei. Histidine reversed the effects of the TM lesions.
Conclusion:
These results indicate that endogenous histamine plays a role in inhibiting the development of morphine-induced reward-seeking behavior, and the inhibition may involve the modulation of dopaminergic activity.
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References
Masukawa Y, Suzuki T, Misawa M . Differential modification of the rewarding effects of methamphetamine and cocaine by opioids and antihistamines. Psychopharmacology (Berl) 1993; 111: 139–43.
Houdi AA, Bardo MT, Van Loon GR . Opioid mediation of cocaine-induced hyperactivity and reinforcement. Brain Res 1989; 497: 195–8.
Schechter MD, Calcagnetti DJ . Trends in place preference conditioning with a cross-indexed bibliography; 1957-1991. Neurosci Biobehav Rev 1993; 17: 21–41.
Schwartz JC, Arrang JM, Garbarg M, Pollard H, Ruat M . Hista-minergic transmission in the mammalian brain. Physiol Rev 1991; 71: 1–51.
Haas H, Panula P . The role of histamine and the tuberomamillary nucleus in the nervous system. Nat Rev Neurosci 2003; 4: 121–30.
Wada H, Inagaki N, Yamatodani A, Watanabe T . Is the histamin-ergic neuron system a regulatory center for whole-brain activity?. Trends Neurosci 1991; 14: 415–8.
Panula P, Pirvola U, Auvinen S, Airaksinen MS . Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 1989; 28: 585–610.
Privou C, Knoche A, Hasenohrl RU, Huston JP . The H1- and H2-histamine blockers chlorpheniramine and ranitidine applied to the nucleus basalis magnocellularis region modulate anxiety and reinforcement related processes. Neuropharmacology 1998; 37: 1019–32.
Cohn CK, Ball GG, Hirsch J . Histamine: effect on self-stimulation. Science 1973; 180: 757–8.
Rassnick S, Kornetsky C . L-Histidine attenuates the effects of pentazocine on rewarding brain-stimulation. Life Sci 1991; 48: 1729–36.
Nath C, Patnaik GK, Saxena RC, Gupta MB . Evaluation of inhibitory effect of diphenhydramine on benzodiazepine dependence in rats. Indian J Physiol Pharmacol 1997; 41: 42–6.
Halpert AG, Olmstead MC, Beninger RJ . Mechanisms and abuse liability of the anti-histamine dimenhydrinate. Neurosci Biobehav Rev 2002; 26: 61–7.
Paxinos G, Watson C . The rat brain in stereotaxic coordinates, 4th ed. San Diego: Academic Press, 1998.
Jin CL, Yang LX, Wu XH, Li Q, Ding MP, Fan YY, et al. Effects of carnosine on amygdaloid kindled seizures in Sprague-Dawley rats. Neuroscience 2005; 135: 939–47.
Doyon WM, York JL, Diaz LM, Samson HH, Czachowski CL, Gonzales RA . Dopamine activity in the nucleus accumbens during consummatory phases of oral ethanol self-administration. Alcohol Clin Exp Res 2003; 27: 1573–82.
Moore KE, Demarest KT, Lookingland KJ . Stress, prolactin and hypothalamic dopaminergic neurons. Neuropharmacology 1987; 26: 801–8.
Mucha RF, van der Kooy D, O'Shaughnessy M, Bucenieks P . Drug reinforcement studied by the use of place conditioning in rat. Brain Res 1982; 243: 91–105.
Suzuki T, Funada M, Narita M, Misawa M, Nagase H . Morphine-induced place preference in the CXBK mouse: characteristics of μ-opioid receptor subtypes. Brain Res 1993; 602: 45–52.
Huang EY, Liu TC, Tao PL . Co-administration of dextromethorphan with morphine attenuates morphine rewarding effect and related dopamine releases at the nucleus accumbens. Naunyn-Schmiedebergs Arch Pharmacol 2003; 368: 386–92.
Bals-Kubik R, Ableitner A, Herz A, Shippenberg TS . Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 1993; 264: 489–95.
Olmstead MC, Franklin KB . The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci 1997; 111: 1324–34.
Onodera K, Yamatodani A, Watanabe T, Wada H . Neuropharma-cology of the histaminergic neuron system in the brain and its relationship with behavioral disoders. Prog Neourobiol 1994; 42: 685–702.
Barke KE, Hough LB . Characterization of basal and morphine-induced histamine release in the rat periaqueductal gray. J Neurochem 1994; 63: 238–44.
Suzuki T, Takamori K, Misawa M, Onodera K . Effects of the histaminergic system on the morphine-induced conditioned place preference in mice. Brain Res 1995; 675: 195–202.
Itzhak Y, Martin JL . Scopolamine inhibits cocaine-conditioned but not unconditioned stimulant effects in mice. Psychopharmacology (Berl) 2000; 52: 216–23.
Schroeder JP, Packard MG . Posttraining intra-basolateral amygdala scopolamine impairs food- and amphetamine-induced conditioned place preferences. Behav Neurosci 2002; 116: 922–7.
Kamei C, Tasaka K . Effect of histamine on memory retrieval in old rats. Biol Pharm Bull 1993; 16: 128–32.
Huang YW, Chen Z, Hu WW, Zhang LS, Wu W, Ying LY, et al. Facilitating effect of histamine on spatial memory deficits induced by dizocilpine as evaluated by 8-arm radial maze in SD rats. Acta Pharmacol Sin 2003; 24: 1270–6.
Wagner U, Weiler HT, Huston JP . Amplification of rewarding hypothalamic stimulation following a unilateral lesion in the region of the tuberomammillary nucleus. Neuroscience 1993; 52: 927–32.
Wagner U, Segura-Torres P, Weiler T, Huston JP . The tuberomammillary nucleus region as a reinforcement inhibiting substrate: facilitation of ipsihypothalamic self-stimulation by unilateral ibotenic acid lesions. Brain Res 1993; 613: 269–74.
Frisch C, Hasenohrl RU, Huston JP . Memory improvement by post-trial injection of lidocaine into the tuberomammillary nucleus, the source of neuronal histamine. Neurobiol Learn Mem 1999; 72: 69–77.
Kohler C, Swanson LW, Haglund L, Wu JY . The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat. Neuroscience 1985; 16: 85–110.
Bannon MJ, Roth RH . Pharmacology of mesocortical dopamine neuron. Pharmacol Rev 1983; 35: 53–68.
Fleckenstein AE, Lookingland KJ, Moore KE . Activation of mesolimbic dopaminergic neurons following central administration of histamine is mediated by H1 receptors. Naunyn-Schmiedebergs Arch Pharmacol 1993; 347: 50–4.
Chiavegatto S, Nasello AG, Bernardi MM . Histamine and spontaneous motor activity: biphasic changes, receptors involved and participation of the striatal dopamine system. Life Sci 1998; 62: 1875–88.
Huston JP, Wagner U, Hasenohrl RU . The tuberomammillary nucleus projections in the control of learning, memory and reinforcement processes: evidence for an inhibitory role. Behav Brain Res 1997; 83: 97–105.
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Project supported by a National Basic Research of China grant (No 2003CB515400), National Natural Science Foundation of China grants (No 30371638, 30472013 and 30572176) and partly supported by the Zhejiang Provincial Natural Science Foundation of China (No R303779).
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Gong, Yx., Lv, M., Zhu, Yp. et al. Endogenous histamine inhibits the development of morphine-induced conditioned place preference. Acta Pharmacol Sin 28, 10–18 (2007). https://doi.org/10.1111/j.1745-7254.2007.00470.x
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DOI: https://doi.org/10.1111/j.1745-7254.2007.00470.x
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