Acetylcholine, Histamine, and Cognition: Two Sides of the Same Coin

Learning and Memory

Volumn 11, Issue 1, 2004, Pages 1-8

  Blandina, Patrizio ^a   Efoudebe, Marcel ^a   Cenni, Gabriele ^a   Mannaioni, Pierfrancesco ^a   Passani, Maria Beatrice ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; HISTAMINE;

ACETYLCHOLINE RELEASE; AMYGDALOID NUCLEUS; AROUSAL; CELL INTERACTION; CENTRAL NERVOUS SYSTEM; CHOLINERGIC NERVE CELL; COGNITION; EMOTION; HUMAN; MEMORY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ACETYLCHOLINE; AMYGDALA; ANIMALS; BRAIN; COGNITION; EMOTIONS; HISTAMINE; HUMANS; MEMORY; RECEPTORS, HISTAMINE;

EID: 0842347485     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.68004     Document Type: Review

References (125)

1. Airaksinen, M., Paetau, A., Paljärvi, L., Reinikainen, K., Rienkkinen, P., Suomalainen, R., and Panula, P. 1991. Histamine neurons in human hypothalamus: Anatomy in normal and Alzheimer diseased brain. Neuroscience 44: 465-481.
2. Airaksinen, M.S. 1992. Multiple neurotransmitter in the tuberomammillary nucleus: Comparison of rat, mouse and guinea pig. J. Comp. Neurol. 323: 103-116.
3. Alvarez, E. and Ruarte, M. 2002. Histaminergic neurons of the ventral hippocampus and the baso-lateral amygdala of the rat: Functional interaction on memory and learning mechanisms. Behav. Brain Res. 128: 81-90.
4. 3 receptors in the brain of 6-hydroxydopamine-lesioned rats. Eur. J. Neurosci. 12: 3823-3832.
5. 3 receptors regulating acetylcholine release in rat entorhinal cortex. Br. J. Pharmacol. 114: 1518-1522.
6. Aston-Jones, G., Rogers, J., Shaver, R.D., Dinan, T.G., and Moss, D.E. 1985. Age-impaired impulse flow from nucleus basalis to cortex. Nature 318: 462-464.
7. Bacciottini, L., Passani, M.B., Mannaioni, P.F., and Blandina, P. 2001. Interactions between histaminergic and cholinergic systems in learning and memory. Behav. Brain Res. 124: 183-194.
8. Bacciottini, L., Passani, M., Giovannelli, L., Cangioli, I., Mannaioni, P., Schunack, W., and Blandina, P. 2002. Endogenous histamine in the medial septum-diagonal band complex increases the release of acetylcholine from the hippocampus: A dual-probe microdialysis study in the freely moving animal. Eur. J. Neurosci. 15: 1669-1680.
9. 1) receptor antagonists. Eur. J. Pharmacol. 387: R5-R7.
10. Bartus, R.F. and Johnson, H.R. 1976. Short-term memory in the rhesus monkey: Disruption from the anti-cholinergic scopolamine. Pharmacol. Biochem. Behav. 5: 39-46.
11. Birthelmer, A., Stemmelin, J., Jackisch, R., and Cassel, J.-C. 2003. Presynaptic modulation of acetylcholine, noradrenaline, and serotonin release in the hippocampus of aged rats with various levels of memory impairments. Brain Res. Bull. 60: 283-296.
12. 3 receptor activation in rats. Br. J. Pharmacol. 119: 1656-1664.
13. 3 receptor a target for new drugs (eds. R. Leurs and H. Timmerman) pp. 27-40. Elsevier, Amsterdam, The Netherlands.
14. Brown, R.E., Stevens, D.R., and Haas, H.L. 2001. The physiology of brain histamine. Prog. Neurobiol. 63: 637-672.
15. Brown, R.E., Sergeeva, O.A., Erikson, K.S., and Haas, H.I. 2002. Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J. Neurosci. 15: 8850-8859.
16. Cahill, L. and McGaugh, J. 1995. A novel demonstration of enhanced memory associated with emotional arousal. Conscious Cogn. 4: 410-421.
17. 3 receptors in the rat basolateral amygdala improves expression of fear memory and enhances acetylcholine release. Eur. J. Neurosci. 16: 521-528.
18. Carlsen, J., Zaborszky, L., and Heimer, L. 1985. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: A combined retrograde fluorescent and immunohistochemical study. J. Comp. Neurol. 234: 155-167.
19. 1 receptors in the nucleus basalis magnocellularis: A dual probe microdialysis study in the freely moving rat. Eur. J. Neurosci. 13: 68-78.
20. Cenni, G., Cangioli, I., Yamatodani, A., Passani, M.B., Mannaioni, P.F., Di Felice, A.M., and Blandina, P. 2004. Thioperamide-elicited increase of histamine release from basolateral amygdala of freely moving rats and its therapeutic implications. Inflamm. Res. (in press).
21. Chemelli, R.M., Willie, J.T., Sinton, C.M., Elmquist, J.K., Scammell, T., Lee, C., Richardson, J.A., Williams, S.C., Xiong, Y., Kisanuki, Y., et al. 1999. Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell 98: 409-412.
22. 3 receptor subtypes. Br. J. Pharmacol. 107: 919-923.
23. 3 receptor. Biochem. J. 355: 279-288.
24. Coyle, J., Donald, L., and Delong, M. 1983. Alzheimer's disease: A disorder of cortical cholinergic innervation. Science 219: 1184-1186.
25. Dalmaz, C., Introini-Collison, I.B., and McGaugh, J.L. 1993. Noradrenergic and cholinergic interactions in the amygdala and the modulation of memory storage. Behav. Brain Res. 58: 167-174.
26. Davies, P. and Maloney, A. 1976. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2: 1403-1405.
27. Davis, K., Thai, L., Gamzu, E., Davis, C., Woolson, R., Gracon, S., Drachman, D., Schneider, L., Whitehouse, P., Hoover, T., et al. 1992. A double-blind placebo-controlled multicenter study of tacrine for Alzheimer's disease. N. Engl. J. Med. 327: 1253-1259.
28. Davis, M. 1992. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15: 353-375.
29. Decker, M.W. 1987. The effects of aging and cortical projections of the forebrain cholinergic system. Brain Res. Rev. 12: 423-428.
30. Deutsch, J. 1971. The cholinergic synapse and the site of memory. Science 174: 788-794.
31. 3 receptor isoforms with different brain expression and signaling properties. Mol. Pharmacol. 59: 1-8.
32. Ennaceur, A. and Meliani, K. 1992. Effects of physostigmine and scopolamine on rats performances in object-recognition and radial-maze tests. Psychopharmacology 109: 321-330.
33. Ericson, H. 1991. GABA-like immunoreactivity in the tuberomammillary nucleus in the rat brain: Delineation of subgroups with antibody against L-histidine decarboxilase as a marker. J. Comp. Neurol. 305: 462-469.
34. Ericson, H., Watanabe, T., and Köhler, C. 1987. Morphological analysis of the tuberomammillary nucleus of the rat brain: Delineation of subgroups with antibody against L-histidine decarboxylase as a marker. J. Comp. Neurol. 263: 1-24.
35. Eriksson, K., Sergeeva, O., Brown, R., and Haas, H. 2001. Orexin/Hypocretin excites the histaminergic neurons of the Tuberomammillary Nucleus. J. Neurosci. 21: 9273-9279.
36. 3 receptor antagonists A-304121 and A-317920: 1. In vitro pharmacological effects. J. Pharmacol. Exp. Ther. 305: 887-896.
37. Everitt, B.J. and Robbins, T.W. 1997. Central cholinergic systems and cognition. Anim. Rev. Psychol. 48: 649-684.
38. 3 receptor ligands GT-2331 and ciproxifan in a repeated acquisition avoidance response in the spontaneously hypertensive rat pup. Behav. Brain Res. 131: 151-161.
39. 3 receptor antagonists A-304121 and A-317920: II. In vivo behavioral and neurophysiological characterization. J. Pharmacol. Exp. Ther. 305: 897-908.
40. Freund, T.F. and Meskenaite, V. 1992. g-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc. Natl. Acad. Sci. 89: 738-742.
41. Gallagher, M. and Colombo, P.J. 1995. Aging: The cholinergic hypothesis of cognitive decline. Curr. Opin. Neurobiol. 5: 161-168.
42. Gauthier, S., Gauthier, L., Brochard, R., Quirion, R., and Sultan, S. 1991. Treatment of Alzheimer's disease: Hopes and reality. Can. J. Neurol. Sci. 18: 439-441.
43. +-evoked release of acetylcholine from rat cortex in vivo. Inflamm. Res. 46: S3-S4.
44. Giorgetti, M., Bacciottini, L., Giovannini, M.G., Colivicchi, M.A., Goldfarb, J., and Blandina, P. 2000. Local GABAergic inhibitory tone of acetylcholine release from the cortex of freely moving rats. Eur. J. Neurosci. 12: 1941-1948.
45. Giovannini, M., Efoudebe, M., Passani, M., Baldi, E., Bucherelli, C., Giachi, F., Corradetti, R., and Blandina, P. 2003. Improvement in fear memory by histamine elicited erk2 activation in hippocampal CA3 cells. J. Neurosci. 23: 9016-9023.
46. 3 receptor agonists and antagonists on cognitive performance and scopolamine-induced amnesia. Behav. Brain Res. 104: 147-155.
47. Givens, B. and Sarter, M. 1997. Modulation of cognitive processes by transsynaptic activation of the basal forebrain. Behav. Brain Res. 84: 1-22.
48. Green, J.P., Prell, G.D., Khandelwal, J.K., and Blandina, P. 1987. Aspects of histamine metabolism. Agents Actions 22: 1-15.
49. Gritti, I., Mainville, L., Mancia, M., and Jones, B.E. 1997. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J. Comp. Neurol. 383: 163-177.
50. Haas, H. and Panula, P. 2003. The role of histamine and the tuberomamillary nucleus in the nervous system. Nat. Neurosci. Rev. 4: 121-130.
51. Haas, H.L. and Reiner, P.B. 1988. Membrane properties of histaminergic tuberomammilary neurones of the rat hypothalamus in vitro. J. Physiol. 399: 633-646.
52. Hardy, J., Adolfsson, R., Alafuzoff, I., Bucht, G., Marcusson, J., Nyberg, P., Perdahl, E., Wester, P., and Winblad, B. 1985. Transmitter deficits in Alzheimer's disease. Neurochem. Int. 7: 545-563.
53. Heckers, S., Ohtake, T., Wiley, R.G., Lappi, D.A., Geula, G., and Mesulam, M.M. 1994. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci. 14: 1271-1289.
54. 1 receptors in patients with Alzheimer's disease assessed by positron emission tomography. Neuroscience 99: 721-729.
55. Hill, S.J., Ganellin, C.R., Timmerman, H., Schwartz, J.C., Shankley, N.P., Young, J.M., Schunack, W., Levi, R., and Haas, H.L. 1997. International union of Pharmacology. XIII. Classification of histamine receptors. Pharmacol. Rev. 49: 253-278.
56. Hough, L.B. 2001. Genomics meets histamine receptors: New subtypes, new receptors. Mol. Pharmacol. 59: 415-419.
57. Huang, Z.-L., Qu, W.-M., Li, W.-D., Mochizuki, T., Eguchi, N., Watanabe, T., Urade, Y., and Hayaishi, O. 2001. Arousal effect of orexin A depends on activation of the histaminergic system. Proc. Natl. Acad. Sci. 98: 9965-9970.
58. Inagaki, N., Yamatodani, A., Shinoda, K., Shiotani, Y., Tohyama, M., Watanabe, T., and Wada, H. 1987. The histaminergic innervation of the mesencephalic nucleus of trigeminal nerve in the rat brain: A light and electron microscopic study. Brain Res. 418: 388-391.
59. Inagaki, N., Toda, K., Taniuchi, I., Panula, P., Yamatodani, A., Tohyama, M., Watanabe, T., and Wada, H. 1990. An analysis of histaminergic efferents of the tuberomammillary nucleus to the medial preoptic area and inferior colliculus of the rat. Exp. Brain Res. 80: 374-380.
60. Ingram, D.K., Jücker, M., and Spangler, E.L. 1994. Behavioral manifestations of aging. Pathobiol. Aging Rat 2: 149-170.
61. Introini-Collison, I.B., Dalmaz, C., and McGaugh, J.L. 1996. Amygdala noradrenergic influences on memory storage involve cholinergic activation. Neurobiol. Learn Mem. 65: 57-64.
62. Kelly, J.S. 1999. Alzheimer's disease: The tacrine legacy. Trends Pharmacol. Sci. 20: 127-129.
63. Khateb, A., Fort, P., Pegna, A., Jones, B.E., and Mühlertaler, M. 1995. Cholinergic nucleus basalis neurons are excited by histamine in vitro. Neuroscience 69: 495-506.
64. Köhler, 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.
65. Köhler, C., Ericson, H., Watanabe, T., Polak, J., Palay, S.L., Palay, V., and Chan-Palay, V. 1986. Galanin immunoreactivity in hypothalamic histamine neurons: Further evidence for multiple chemical messengers in the tuberomammillary nucleus. J. Comp. Neurol. 250: 58-64.
66. Kollonitsch, J., Patchett, A.A., Marburg, S., Maycock, A.L., Perkins, L.M., Doldouras, G.A., Duggan, D.E., and Aster, S.D. 1978. Selective inhibitors of biosynthesis of aminergic neurotransmitters. Nature 274: 906-908.
67. Kubanis, P. and Zornetzer, S.F. 1981. Age-related behavioral and neurobiological changes: A review with an emphasis on memory. Behav. Nettrol. Biol. 31: 115-172.
68. Kuhl, D.E., Koeppe, R.A., Minoshima, S., Snyder, S.E., Ficaro, E.P., Foster, N.L., Frey, K.A., and Kilbourn, M.R. 1999. In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer's disease. Neurology 52: 691-699.
69. LeDoux, J.E. 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23: 155-184.
70. 3 receptor agonists and antagonists. Trends Pharmacol. Sci. 19: 177-183.
71. 3-receptor antagonist. J. Pharmacol. Exp. Ther. 287: 658-666.
72. Lin, J., Sakai, K., and Jouvet, M. 1994. Hypothalamo-preoptic histaminergic projections in sleep-wake control in the cat. Eur. J. Neurosci. 6: 618-625.
73. Lin, J.S., Hou, Y., Sakai, K., and Jouvet, M. 1996. Histaminergic descending inputs to the mesopontine tegmentum and their role in the control of cortical activation and wakefulness in the cat. J. Neurosci. 16: 1523-1537.
74. Liu, C., Ma, X.-J., Wilson, S., Hofstra, C., Blevitt, J., Pyati, J., Li, X., Chai, W., Carruthers, N., and Lovenberg, T. 2001a. Cloning and pharmacological characterization of a fourth histamine receptor (H4) expressed in bone marrow. Mol. Pharmacol. 59: 420-426.
75. Liu, C., Wilson, S., Kuei, C., and Lovenberg, T. 2001b. Comparison of human, mouse, rat, and guinea pig histamine H4 receptors reveals substantial pharmacological species variation. J. Pharmacol. Exp. Ther. 299: 121-130.
76. 3 receptor. Mol. Pharmacol. 55: 1101-1107.
77. 1 receptor agonist, 2-(3-trifluoromethylphenyl) histamine, in the rat object recognition test. Inflamm. Res. 52: S33-S34.
78. McCormick, D.A. and Williamson, A. 1991. Modulation of neuronal firing mode in cat and guinea-pig LGNd by histamine: Possible cellular mechanisms of histaminergic control of arousal. J. Neurosci. 11: 3188-3199.
79. McGaugh, J.L. 2000. Memory: A century of consolidation. Science 287: 248-251.
80. McGaugh, J.L. and Izquierdo, I. 2000. The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol. Sci. 21: 208-210.
81. 3 antagonist, on the step-through passive avoidance response and histidine decarboxylase activity in senescence-accelerated mice. Pharmacol. Biochem. Behav. 50: 321-325.
82. Mesulam, M.M., Mufson, E.J., Wainer, B.H., and Levey, A.I. 1983. Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10: 1185-1201.
83. Mignot, E., Taheri, S., and Nishino, S. 2002. Sleeping with the hypothalamus: Emerging therapeutic targets for sleep disorders. Nat. Neurosci. 5: 1071-1075.
84. Mochizuki, T., Okakura-Mochizuki, K., Horii, A., Yamamoto, Y., and Yamatodani, A. 1994. Histaminergic modulation of hippocampal acetylcholine release in vivo. J. Neurochem. 62: 2275-2282.
85. 3 receptors regulates histamine neurons in brain. Nature 408: 860-864.
86. Nicoll, R.A. 1985. The septo-hippocampal projection: A model cholinergic pathway. Trends Neurosci. 8: 533-536.
87. Nicoll, R.A., Malenka, R.C., and Kauer, J.A. 1990. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Psychol. Rev. 70: 513-565.
88. Nishino, S., Fuijiki, N., Ripley, B., Sakurai, E., Kato, M., Watanabe, T., Mignot, E., and Yanai, K. 2001. Decreased brain histamine content in hypocretin/orexin receptor-2 mutated narcoleptic dogs. Neurosci. Lett. 313: 125-128.
89. Oda, T., Morikawa, N., Saito, Y., Masuho, Y., and Matsumoto, S. 2000. Molecular cloning and characterization of novel type of histamine receptor preferentially expressed in leukocytes. J. Biol. Chem. 275: 36781-36786.
90. Okamura, N., Yanai, K., Higuchi, M., Sakai, J., lwata, P., Ido, T., Sasaki, H., Watanabe, T., and Itoh, M. 2000. Functional neuroimaging of cognition impaired by a classical antihistamine, d-chlorpheniramine. Br. J. Pharmacol. 129: 115-123.
91. 3-receptor antagonist, of learning and memory in the elevated plus-maze test in mice. Naunyn Schmiedeberg's Arch. Pharmacol. 357: 508-513.
92. Panula, P., Yang, H.Y., and Costa, E. 1984. Histamine-containing neurons in rat hypothalamus. Proc. Natl. Acad. Sci. 81: 2572-2576.
93. Panula, P., Rinnie, J., Kuokkanen, K., Eriksson, K.S., Sallmen, T., Kalimo, H., and Relja, M. 1997. Neuronal histamine deficit in Alzheimer's disease. Neuroscience 82: 993-997.
94. Parmentier, R., Ohtsu, H., Diebarra-Hannas, Z., Valtx, J.-L., Watanabe, T., and Lin, J.-S. 2002. Anatomical, physiological and pharmacological characteristics of histidine decarboxylase knockout mice: Evidence for the role of brain histamine in behavioral and sleep-wake control. J. Neurosci. 22: 7695-7711.
95. Passani, M.B. and Blandina, P. 2003. The neuronal histaminergic system in cognition. Curr. Med. Chem. (in press).
96. Passani, M.B., Bacciottini, L., Mannaioni, P.F., and Blandina, P. 2000. Central histaminergic system and cognitive processes. Neurosci. Biobehav. Rev. 24: 107-114.
97. 3 receptor-mediated impairment of contextual fear conditioning, and in-vivo inhibition of cholinergic transmission in the rat basolateral amygdala. Eur. J. Neurosci. 14: 1522-1532.
98. Pepeu, G. and Blandina, P. 1998. The acetylcholine, GABA, glutamate triangle in the rat forebrain. J. Physiol. (Paris) 92: 351-355.
99. 1 receptors in rat brain areas. Neuroscience 52: 169-189.
100. Prast, H., Argyriou, A., and Philippu, A. 1996. Histaminergic neurons facilitate social memory in rats. Brain Res. 734: 316-318.
101. Quirion, R., Wilson, A., Rowe, W., Aubert, I., Richard, J., Doods, H., Parent, A., White, N., and Meaney, M.J. 1995. Facilitation of acetylcholine release and cognitive performance by an M2-muscarinic receptor antagonist in aged memory-impaired rats. J. Neurosci. 15: 1455-1462.
102. Rapp, P.R. and Amaral, D.G. 1992. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci. 15: 340-345.
103. Reiner, P.B. 1987. Electrophysiological properties of cortically projecting histamine neurons of rat hypothalamus. Neurosci. Lett. 73: 43-47.
104. 3 receptors. Br. J. Pharmacol. 135: 383-392.
105. Sacchetti, B., Ambrogi Lorenzini, C., Baldi, E., Tassoni, G., and Bucherelli, C. 1999. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J. Neurosci. 19: 9570-9578.
106. Sakai, K., Mansari, M.E., Lin, J., Zhang, J., and Mercier, G.V. 1990. The posterior hypothalamus in the regulation of wakefulness and paradoxical sleep. In The diencephalon and sleep. (ed. M. Mancia). pp. 171-198. Raven Press, New York.
107. Schneider, C., Risser, D., Kirchner, L., Kitzmuller, E., Cairns, N., Prast, H., Singewald, N., and Lubec, G. 1997. Similar deficits of central histaminergic system in patients with Down syndrome and Alzheimer disease. Neurosci. Lett. 222: 183-186.
108. Senba, E., Daddona, P.E., Watanabe, T., Wu, J.Y., and Nagy, J.I. 1985. Coexistence of adenosine deaminase, histidine decarboxylase, and glutamate decarboxylase in hypothalamic neurons of the rat. J. Neurosci. 5: 3393-3420.
109. Sherman, S., Atri, A., Hasselmo, M., Stern, C., and Howard, M. 2003. Scopolamine impairs human recognition memory: Data and modeling. Behav. Neurosci. 117: 526-539.
110. 2 receptors. Proc. Nat. Acad. Sci. 93: 6802-6807.
111. Sperling, R., Greve, D., Dale, A., Killiany, P., Holmes, J., Rosas, H., Cocchiarella, A., Firth, P., Rosen, B., Lake, S., et al. 2002. Functional MRI detection of pharmacologically induced memory impairment. Proc. Natl. Acad. Sci. 99: 455-460.
112. 3-receptor antagonist of high oral in vivo potency with 4-(ω-(arylalkyloxy)alkyl)-1H-imidazole structure. Arch. Pharm. (Weinheim) 331: 211-218.
113. Stemmelin, J., Lazarus, C., Cassel, S., Kelche, C., and Cassel, J.-C. 2000. Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 96: 275-289.
114. Steriade, M. and Buzsaki, G. 1990. Parallel activation of thalamic and cortical neurons by brainstem and basal forebrain cholinergic system. In Brain cholinergic system. (eds. M. Steriade and D. Biesold), pp. 3-64. Oxford United Press, New York.
115. Takeda, N., Inagaki, S., Shiosaka, S., Taguchi, Y., Oertel, W.H., Tohyama, M., Watanabe, T., and Wada, H. 1984. Immunocytochemical evidence for the coexistence of histidine decarboxylase and glutamate decarboxylase-like immunoreactivities in nerve cell of the posterior magnocellular nucleus of hypothalamus of rats. Proc. Nat. Acad. Sci. 81: 7467-7650.
116. 3 receptor: Evidence for two isoforms. Neuroreport 11: 755-759.
117. Tohyama, M., Tamiya, R., Inagaki, N., and Tagaki, H. 1991. Morphology of histaminergic neurons with histidine decarboxylase as a marker. In Histaminergic neurons: Morphology and function (eds. T. Watanabe and H. Wada), pp. 107-126. CRC Press, Boca Raton, FL.
118. Vazdarjanova, A. and McGaugh, J.L. 1999. Basolateral amygdala is involved in modulating consolidation of memory for classical conditioning. J. Neurosci. 19: 6615-6622.
119. Wada, H., Inagaki, N., Yamatodani, A., and Watanabe, T. 1991. Is the histaminergic neuron system a regulatory center for whole-brain activity? Trends Neurosci. 14: 415-418.
120. Watanabe, T., Taguchi, Y., Hayashi, H., Tanaka, J., Shiosaka, S., Tohyama, M., Kubota, H., Terano, Y., and Wada, H. 1983. Evidence for the presence of a histaminergic neuron system in the rat brain: An immunohistochemical analysis. Neurosci. Lett. 39: 249-254.
121. 3) receptor. Neuropharmacology 42: 929-940.
122. Whitehouse, P.J., Price, D.L., Strubble, R.G., Clark, A.W., Coyle, J.T., and DeLong, M.R. 1982. Alzheimer's disease and senile dementia; loss of neurons in the basal forebrain. Science 215: 1237-1239.
123. Wieland, K., Bongers, G., Yamamoto, Y., Hashimoto, T., Yamatodani, A., Menge, W., Timmerman, H., Lovenberg, T., and Leurs, R. 2001. Constitutive activity of histamine h(3) receptors stably expressed in SK-N-MC cells: Display of agonism and inverse agonism by H(3) antagonists. J. Pharmacol. Exp. Ther. 299: 908-914.
124. Woolf, N.J., Eckenstein, F., and Butcher, L.L. 1984. Cholinergic systems in the rat brain. I. Projections to the limbic telencephalon. Brain Res. Bull. 13: 751-784.
125. Zhu, Y., Michalovich, A., Wu, H.-L., Tang, K., and Dytko, G.M. 2001. Cloning, expression, and pharmacological characterization of a novel human histamine receptor. Mol. Pharmacol. 59: 434-441.