In vivo electrochemical evidence for simultaneous 5-HT and histamine release in the rat substantia nigra pars reticulata following medial forebrain bundle stimulation

Journal of Neurochemistry

Volumn 118, Issue 5, 2011, Pages 749-759

  Hashemi, Parastoo ^a   Dankoski, Elyse C ^b   Wood, Kevin M ^a   Ambrose, Rebecca Ellen ^a   Wightman, Robert Mark ^a,b  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

fast scan cyclic voltammetry; histamine N methyltransferase; medial forebrain bundle; serotonin; SKF 91488; substantia nigra pars reticulata

Indexed keywords

HISTAMINE; HISTAMINE H3 RECEPTOR ANTAGONIST; HISTAMINE METHYLTRANSFERASE; HOMODIMAPRIT; SEROTONIN; THIOPERAMIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DORSAL RAPHE NUCLEUS; ELECTROCHEMICAL DETECTION; ELECTROSTIMULATION; ENZYME INHIBITION; HISTAMINE RELEASE; IN VITRO STUDY; IN VIVO STUDY; MALE; MEDIAL FOREBRAIN BUNDLE; NERVE STIMULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONIN RELEASE; SEROTONIN UPTAKE; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; SUBSTANTIA NIGRA PARS RETICULATA;

ANIMALS; DIMAPRIT; ELECTRIC STIMULATION; ELECTROCHEMISTRY; HISTAMINE; HISTAMINE AGONISTS; HISTAMINE H3 ANTAGONISTS; LINEAR MODELS; MALE; MEDIAL FOREBRAIN BUNDLE; NEURAL PATHWAYS; PIPERIDINES; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SUBSTANTIA NIGRA;

RATTUS;

EID: 80051800807     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07352.x     Document Type: Article

References (68)

1. Anichtchik O. V., Huotari M., Peitsaro N., Haycock J. W., Mannisto P. T., and, Panula P., (2000) Modulation of histamine H3 receptors in the brain of 6-hydroxydopamine-lesioned rats. Eur. J. Neurosci. 12, 3823-3832.
2. Arrang J. M., Garbarg M., Lancelot J. C., Lecomte J. M., Pollard H., Robba M., Schunack W., and, Schwartz J. C., (1987) Highly potent and selective ligands for histamine H3-receptors. Nature 327, 117-123. (Pubitemid 17062756)
3. Azmitia E. C., and, Segal M., (1978) Autoradiographic analysis of differential ascending projections of dorsal and median raphe nuclei in rat. J. Comp. Neurol. 179, 641-667. (Pubitemid 8372646)
4. Barnes N. M., and, Sharp T., (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38, 1083-1152. (Pubitemid 29292403)
5. Beaven M. A., and, Shaff R. E., (1979) New inhibitors of histamine-N-methyltransferase. Biochem. Pharmacol. 28, 183-188.
6. Blier P., Pineyro G., el Mansari M., Bergeron R., and, de Montigny C., (1998) Role of somatodendritic 5-HT autoreceptors in modulating 5-HT neurotransmission. Ann. N Y Acad. Sci. 861, 204-216. (Pubitemid 29047718)
7. Borue X., Cooper S., Hirsh J., Condron B., and, Venton B. J., (2009) Quantitative evaluation of serotonin release and clearance in Drosophila. J. Neurosci. Methods 179, 300-308.
8. Borue X., Condron B., and, Venton B. J., (2010) Both synthesis and reuptake are critical for replenishing the releasable serotonin pool in Drosophila. J. Neurochem. 113, 188-199.
9. Brown R. E., Stevens D. R., and, Haas H. L., (2001) The physiology of brain histamine. Prog. Neurobiol. 63, 637-672. (Pubitemid 32119421)
10. Bull D. R., Palij P., Sheehan M. J., Millar J., Stamford J. A., Kruk Z. L., and, Humphrey P. P., (1990) Application of fast cyclic voltammetry to measurement of electrically evoked dopamine overflow from brain slices in vitro. J. Neurosci. Methods 32, 37-44. (Pubitemid 20111976)
11. Bunin M. A., and, Wightman R. M., (1998) Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J. Neurosci. 18, 4854-4860. (Pubitemid 28285394)
12. Bunin M. A., Prioleau C., Mailman R. B., and, Wightman R. M., (1998) Release and uptake rates of 5-hydroxytryptamine in the dorsal raphe and substantia nigra reticulata of the rat brain. J. Neurochem. 70, 1077-1087. (Pubitemid 28113641)
13. Cechova S., and, Venton B. J., (2008) Transient adenosine efflux in the rat caudate-putamen. J. Neurochem. 105, 1253-1263. (Pubitemid 351590786)
14. Corvaja N., Doucet G., and, Bolam J. P., (1993) Ultrastructure and synaptic targets of the raphe-nigral projection in the rat. Neuroscience 55, 417-427. (Pubitemid 23211353)
15. Cumming P., Shaw C., and, Vincent S. R., (1991) High affinity histamine binding site is the H3 receptor: characterization and autoradiographic localization in rat brain. Synapse (New York, NY) 8, 144-151.
16. Davidson C., and, Stamford J. A., (1996) Serotonin efflux in the rat ventral lateral geniculate nucleus assessed by fast cyclic voltammetry is modulated by 5-HT1B and 5-HT1D autoreceptors. Neuropharmacology 35: 1627-1634. (Pubitemid 27026492)
17. Daws L. C., Gould G. G., Teicher S. D., Gerhardt G. A., and, Frazer A., (2000) 5-HT(1B) receptor-mediated regulation of serotonin clearance in rat hippocampus in vivo. J. Neurochem. 75, 2113-2122.
18. Dib B., (1994) New technique for cannulae implantation into the dorsal raphe nucleus using layer 5 of cerebellum reference in rat stereotaxic surgery. Pharmacol. Biochem. Behav. 49, 639-642. (Pubitemid 24335648)
19. Dray A., Gonye T. J., Oakley N. R., and, Tanner T., (1976) Evidence for the existence of a raphe projection to the substantia nigra in rat. Brain Res. 113, 45-57.
20. Fibiger H. C., and, Miller J. J., (1977) Anatomical and electrophysiological investigation of serotonergic projection from dorsal raphe nucleus to substantia nigra in rat. Neuroscience 2, 975-987.
21. Garbarg M., Barbin G., Feger J., and, Schwartz J. C., (1974) Histaminergic pathway in rat brain evidenced by lesions of the medial forebrain bundle. Science 186, 833-835.
22. Garbarg M., Barbin G., Bischoff S., Pollard H., and, Schwartz J. C., (1976) Dual localization of histamine in an ascending neuronal pathway and in non-neuronal cells evidenced by lesions in the lateral hypothalamic area. Brain Res. 106, 333-348.
23. Garcia M., Floran B., Arias-Montano J. A., Young J. M., and, Aceves J., (1997) Histamine H3 receptor activation selectively inhibits dopamine D1 receptor-dependent [3H]GABA release from depolarization-stimulated slices of rat substantia nigra pars reticulata. Neuroscience 80, 241-249. (Pubitemid 27323689)
24. Garris P. A., and, Wightman R. M., (1994) Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J. Neurosci. 14, 442-450. (Pubitemid 24022128)
25. Hafizi S., Kruk Z. L., and, Stamford J. A., (1990) Fast cyclic voltammetry: improved sensitivity to dopamine with extended oxidation scan limits. J. Neurosci. Methods 33, 41-49. (Pubitemid 20264013)
26. Hashemi P., Dankoski E. C., Petrovic J., Keithley R. B., and, Wightman R. M., (2009) Voltammetric detection of 5-hydroxytryptamine release in the rat brain. Anal. Chem. 81, 9462-9471.
27. Heeringa M. J., and, Abercrombie E. D., (1995) Biochemistry of somatodendritic dopamine release in substantia nigra: an in vivo comparison with striatal dopamine release. J. Neurochem. 65, 192-200.
28. Heien M. L., Phillips P. E., Stuber G. D., Seipel A. T., and, Wightman R. M., (2003) Overoxidation of carbon-fiber microelectrodes enhances dopamine adsorption and increases sensitivity. Analyst 128, 1413-1419. (Pubitemid 38082985)
29. Imai H., Steindler D. A., and, Kitai S. T., (1986) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J. Comp. Neurol. 243, 363-380. (Pubitemid 16179241)
30. Invernizzi R. W., Pierucci M., Calcagno E., Di Giovanni G., Di Matteo V., Benigno A., and, Esposito E., (2007) Selective activation of 5-HT(2C) receptors stimulates GABA-ergic function in the rat substantia nigra pars reticulata: a combined in vivo electrophysiological and neurochemical study. Neuroscience 144, 1523-1535. (Pubitemid 46138024)
31. Jackson B. P., Dietz S. M., and, Wightman R. M., (1995) Fast-scan cyclic voltammetry of 5-hydroxytryptamine. Anal. Chem. 67, 1115-1120.
32. John C. E., and, Jones S. R., (2007) Voltammetric characterization of the effect of monoamine uptake inhibitors and releasers on dopamine and serotonin uptake in mouse caudate-putamen and substantia nigra slices. Neuropharmacology 52, 1596-1605. (Pubitemid 46843135)
33. John C. E., Budygin E. A., Mateo Y., and, Jones S. R., (2006) Neurochemical characterization of the release and uptake of dopamine in ventral tegmental area and serotonin in substantia nigra of the mouse. J. Neurochem. 96, 267-282.
34. Kita J. M., Kile B. M., Parker L. E., and, Wightman R. M., (2009) In vivo measurement of somatodendritic release of dopamine in the ventral tegmental area. Synapse 63, 951-960.
35. Kohler C., Swanson L. W., Haglund L., and, Wu J. Y., (1985) The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat. Neuroscience 16, 85-110. (Pubitemid 16233316)
36. van der Kooy D., and, Hattori T., (1980) Dorsal raphe cells with collateral projections to the caudate-putamen and substantia nigra: a fluorescent retrograde double labeling study in the rat. Brain Res. 186, 1-7. (Pubitemid 10131856)
37. Korotkova T. M., Haas H. L., and, Brown R. E., (2002) Histamine excites GABAergic cells in the rat substantia nigra and ventral tegmental area in vitro. Neurosci. Lett. 320, 133-136. (Pubitemid 34164433)
38. Kristensen E. W., Wilson R. L., and, Wightman R. M., (1986) Dispersion in flow-injection analysis measured with microvoltammetric electrodes. Anal. Chem. 58, 986-988.
39. Kristensen E. W., Kuhr W. G., and, Wightman R. M., (1987) Temporal characterization of perfluorinated ion exchange coated microvoltammeteric electrodes for in vivo use. Anal. Chem. 59, 1752-1757. (Pubitemid 17616713)
40. Michael D., Travis E. R., and, Wightman R. M., (1998) Color images for fast-scan CV measurements in biological systems. Anal. Chem. 70, 586A-592A. (Pubitemid 128669939)
41. Miller J. J., Richardson T. L., Fibiger H. C., and, McLennan H., (1975) Anatomical and electrophysiological identification of a projection from the mesencephalic raphe to the caudate-putamen in the rat. Brain Res. 97, 133-136.
42. Moore R. Y., Halaris A. E., and, Jones B. E., (1978) Serotonin neurons of the midbrain raphe: ascending projections. J. Comp. Neurol. 180, 417-438.
43. Mosko S. S., Haubrich D., and, Jacobs B. L., (1977) Serotonergic afferents to the dorsal raphe nucleus: evdience from HRP and synaptosomal uptake studies. Brain Res. 119, 269-290. (Pubitemid 8006247)
44. O'Connor J. J., and, Kruk Z. L., (1991) Fast cyclic voltammetry can be used to measure stimulated endogenous 5-hydroxytryptamine release in untreated rat brain slices. J. Neurosci. Methods 38, 25-33.
45. Panula P., Pirvola U., Auvinen S., and, Airaksinen M. S., (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 28, 585-610. (Pubitemid 19081018)
46. Parent A., Descarries L., and, Beaudet A., (1981) Organization of ascending serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of [3H]5-hydroxytryptamine. Neuroscience 6, 115-138. (Pubitemid 11095918)
47. Park J., Kile B. M., and, Wightman R. M., (2009) In vivo voltammetric monitoring of norepinephrine release in the rat ventral bed nucleus of the stria terminalis and anteroventral thalamic nucleus. Eur. J. Neurosci. 30, 2121-2133.
48. Paxinos G., and, Watson C., (2007) The Rat Brain in Stereotaxic Coordinates, 6th Edn. Elsevier, London, UK.
49. Pellegrino de Iraldi A., (1992) Compartmentalization of monoaminergic synaptic vesicles in the storage and release of neurotransmitter. Mol. Neurobiol. 6, 323-337.
50. Petty F., Davis L. L., Kabel D., and, Kramer G. L., (1996) Serotonin dysfunction disorders: a behavioral neurochemistry perspective. J. Clin. Psychiatry 57 (Suppl 8), 11-16. (Pubitemid 26282186)
51. Pihel K., Hsieh S., Jorgenson J. W., and, Wightman R. M., (1995) Electrochemical detection of histamine and 5-hydroxytryptamine at isolated mast cells. Anal. Chem. 67, 4514-4521. (Pubitemid 126634619)
52. Pihel K., Hsieh S., Jorgenson J. W., and, Wightman R. M., (1998) Quantal corelease of histamine and 5-hydroxytryptamine from mast cells and the effects of prior incubation. Biochemistry 37, 1046-1052. (Pubitemid 28100606)
53. Pollard H., Llorens-Cortes C., Barbin G., Garbarg M., and, Schwartz J. C., (1978) Histamine and histidine decarboxylase in brain stem nuclei: distribution and decrease after lesions. Brain Res. 157, 178-181.
54. Pollard H., Moreau J., Arrang J. M., and, Schwartz J. C., (1993) A detailed autoradiographic mapping of histamine H3 receptors in rat brain areas. Neuroscience 52, 169-189. (Pubitemid 23026616)
55. Rice M. E., Richards C. D., Nedergaard S., Hounsgaard J., Nicholson C., and, Greenfield S. A., (1994) Direct monitoring of dopamine and 5-HT release in substantia nigra and ventral tegmental area in vitro. Exp. Brain Res. 100, 395-406. (Pubitemid 24281989)
56. Robinson D. L., and, Wightman R. M., (2007) Rapid dopamine release in freely moving rats, in Electrochemical Methods for Neuroscience (, Michael A. C., and, Borland L. M., eds), pp. 17-36. CRC Press, Boca Raton, FL.
57. Rueter L. E., Fornal C. A., and, Jacobs B. L., (1997) A critical review of 5-HT brain microdialysis and behavior. Rev. Neurosci. 8, 117-137. (Pubitemid 27466534)
58. Sanford A. L., Morton S. W., Whitehouse K. L., Oara H. M., Lugo-Morales L. Z., Roberts J. G., and, Sombers L. A., (2010) Voltammetric detection of hydrogen peroxide at carbon fiber microelectrodes. Anal. Chem. 82, 5205-5210.
59. Schwartz J. C., Arrang J. M., Garbarg M., Pollard H., and, Ruat M., (1991) Histaminergic transmission in the mammalian brain. Physiol. Rev. 71, 1-51.
60. Shaskan E. G., and, Snyder S. H., (1970) Kinetics of serotonin accumulation into slices from rat brain: relationship to catecholamine uptake. J. Pharmacol. Exp. Ther. 175, 404-418.
61. Steinbusch H. W., van der Kooy D., Verhofstad A. A., and, Pellegrino A., (1980) Serotonergic and non-serotonergic projections from the nucleus raphe dorsalis to the caudate-putamen complex in the rat, studied by a combined immunofluorescence and fluorescent retrograde axonal labeling technique. Neurosci. Lett. 19, 137-142. (Pubitemid 11239137)
62. Steinbusch H. W., Nieuwenhuys R., Verhofstad A. A., and, Van der Kooy D., (1981) The nucleus raphe dorsalis of the rat and its projection upon the caudatoputamen. A combined cytoarchitectonic, immunohistochemical and retrograde transport study. J. Physiol. (Paris) 77, 157-174. (Pubitemid 11032665)
63. Takmakov P., Zachek M. K., Keithley R. B., Walsh P. L., Donley C., McCarty G. S., and, Wightman R. M., (2010) Carbon microelectrodes with a renewable surface. Anal. Chem. 82, 2020-2028.
64. Threlfell S., Cragg S. J., Kallo I., Turi G. F., Coen C. W., and, Greenfield S. A., (2004) Histamine H3 receptors inhibit serotonin release in substantia nigra pars reticulata. J. Neurosci. 24, 8704-8710. (Pubitemid 39362965)
65. Threlfell S., Greenfield S. A., and, Cragg S. J., (2010) 5-HT(1B) receptor regulation of serotonin (5-HT) release by endogenous 5-HT in the substantia nigra. Neuroscience 165, 212-220.
66. Whishaw I. Q., Cioe J. D., Previsich N., and, Kolb B., (1977) The variability of the interaural line vs the stability of bregma in rat stereotaxic surgery. Physiol. Behav. 19, 719-722. (Pubitemid 8263503)
67. Wightman R. M., Amatore C., Engstrom R. C., Hale P. D., Kristensen E. W., Kuhr W. G., and, May L. J., (1988) Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25, 513-523.
68. Wirtshafter D., Stratford T. R., and, Asin K. E., (1987) Evidence that serotonergic projections to the substantia nigra in the rat arise in the dorsal, but not the median, raphe nucleus. Neurosci. Lett. 77, 261-266.