Activation of histaminergic H3 receptors in the rat basolateral amygdala improves expression of fear memory and enhances acetylcholine release

European Journal of Neuroscience

Volumn 16, Issue 3, 2002, Pages 521-528

  Cangioll, Iacopo ^a   Baldi, Elisabetta ^a   Mannaioni, Pier Francesco ^a   Bucherelli, Corrado ^a   Blandina, Patrizio ^a   Passani, M Beatrice ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

ACh; Amygdala; Conditioned freezing; Fear memory; H3 receptors; Microdialysis; Oxotremorine

Indexed keywords

ALPHA METHYLHISTAMINE; HISTAMINE H3 RECEPTOR; HISTAMINE H3 RECEPTOR AGONIST; IMMEPIP; UNCLASSIFIED DRUG; 4 (1H IMIDAZOL 4 YLMETHYL)PIPERIDINE; 4-(1H-IMIDAZOL-4-YLMETHYL)PIPERIDINE; ACETYLCHOLINE; ALPHA-METHYLHISTAMINE; CHOLINESTERASE INHIBITOR; DRUG DERIVATIVE; HISTAMINE; HISTAMINE AGONIST; HISTAMINE DERIVATIVE; IMIDAZOLE DERIVATIVE; MUSCARINIC AGENT; OXOTREMORINE; OXOTREMORINE M; PIPERIDINE DERIVATIVE;

ACETYLCHOLINE RELEASE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL TISSUE; BRAIN PERFUSION; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONDITIONING; CONFERENCE PAPER; CONTROLLED STUDY; DRUG EFFECT; FEAR; FREEZING; HISTAMINE RELEASE; MALE; MEMORY; MEMORY CONSOLIDATION; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SHOCK; ANIMAL; ARTICLE; DOSE RESPONSE; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPTIC TRANSMISSION; WISTAR RAT;

ACETYLCHOLINE; AMYGDALA; ANIMALS; CHOLINESTERASE INHIBITORS; CONDITIONING (PSYCHOLOGY); DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; HISTAMINE; HISTAMINE AGONISTS; IMIDAZOLES; MALE; MEMORY; METHYLHISTAMINES; MUSCARINIC AGONISTS; NEURONS; OXOTREMORINE; PIPERIDINES; RATS; RATS, WISTAR; RECEPTORS, HISTAMINE H3; SYNAPTIC TRANSMISSION;

EID: 0036689646     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02092.x     Document Type: Conference Paper

References (75)

1. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669-672.
2. Alvarez, E.O. & Banzan, A.M. (1995) Effects of localized microinjections into the hippocampal formation on the retrieval of a one-way active avoidance response in rats. J. Neural TransmGen. Sect., 101, 201-211.
3. Alvarez, E. & Ruarte, M. (2002) Histaminergic neurons of the ventral hippocampus and the baso-lateral amygdala of the rat: Functional interaction on memory and learning mechanisms. BehavBrain Res., 128, 81-90.
4. Alves-Rodrigues, A., Lemstra, S., Vollinga, R., Menge, W., Timmerman, H. & Leurs, R. (2001) Pharmacological analysis of immepip amd imetit homologous. Further evidence for histamine H3 receptor heterogeneity. BehavBrain Res., 124, 121-127.
5. Anagnostaras, S., Maren, S., Goodrich, J.S. & Fanselow, M. (1999) Scopolamine and Pavlovian fear conditioning in rats: Dose-effect analysis. Neuropsychopharmacology, 21, 731-744.
6. Anderson, A. & Phelps, E. (2001) Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305-309.
7. 3 receptors regulating acetylcholine release in rat entorhinal cortex. Br. J. Pharmacol., 114, 1518-1522.
8. 3) of histamine receptor. Nature, 302, 832-837.
9. 3 receptors. Nature, 327, 117-123.
10. Atkins, C.M. (1998) The MAPK cascade is required for mammalian associative learning. Nature Neurosci., 1, 602-609.
11. Bacciottini, L., Passani, M.B., Giovannelli, L., Cangioli, I., Mannaioni, P.F., Schunack, W. & 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 rat. Eur. J. Neurosci., 15, 1669-1680.
12. Bacciottini, L., Passani, M.B., Mannaioni, P.F. & Blandina, P. (2001) Interactions between histaminergic and cholinergic systems in learning and memory. Behav. Brain Res., 124, 183-194.
13. Ben-Ari, Y., Zigmond, R.E., Shute, C.C.D. & Lewis, P.R. (1977) Regional distribution of cholinergic acetyltransferase and acetylcholinesterase within the amygdala complex and stria terminalis. Brain Res., 120, 435-445.
14. Birbaumer, N., Grodd, W., Diedrich, O., Klose, U., Erb, M., Lotze, M., Scheider, F. & Weiss & Flor, H. (1998) fMRI reveals amygdala activation to human faces in social phobia. Neuroreport, 9, 1223-1226.
15. +-evoked release of acetylcholine from rat cortex in vivo. Inflamm. Res., 45, S54-S55.
16. Blandina, P., Mannaioni, P.F. & Giovannini, M.G. (2001) Histamine receptors activate MAPK signaling pathway in rat hippocampus: Soc. Neurosci. Abstr., 27, 824.2.
17. Brown, R.E., Fedorov, N.B., Haas, H.L. & Reymann, K.G. (1995) Histaminergic modulation of synaptic plasticity in area CA1 of rat hippocampal slices. Neuropharmacology, 34, 181-190.
18. Brown, R.E., Stevens, D.R. & Haas, H.L. (2001) The physiology of brain histamine. Prog. Neurobiol., 63, 637-672.
19. Carlsen, J., Zaborszky, L. & Heimer, L. (1985) Cholinergic projections from the basal forebrain to the basolateral amygdala complex: A combined retrograde fluorescent and immunohistochemical study. J. Comp. Neurol., 234, 155-167.
20. Cecchi, M., Passani, M.B., Bacciottini, L., Mannaioni, P.F. & Blandina, P. (2001) Cortical acetylcholine release elicited by stimulation of histamine H1 receptors in the nucleus basalis magnocellularis: A dual probe microdialysis study in the freely moving rat. Eur. J. Neurosci., 13, 68-78.
21. Davidson, R., Putnam, K. & Larson, C. (2000) Dysfunction in the neural cisrcuitry of emotion regulation-A possible prelude to violence. Science, 289, 591-594.
22. Drutel, G., Peitsaro, N., Karlstedt, K., Wieland, K., Smit, M., Timmerman, H., Panula, P. & Leurs, R. (2001) Identification of rat H3 receptor isoforms with different brain expression and signaling properties. Mol. Pharmacol., 59, 1-8.
23. Emery, N. & Amaral, D. (2000) In Lane, R.D. & Nadel, L. (Eds), The Cognitive Neuroscience of Emotion. Oxford University, New York, NY.
24. Eriksson, K., Sergeeva, O., Brown, R. & Haas, H. (2001) Orexin/hypocretin excites the histaminergic neurons of the tuberomammillary nucleus. J. Neurosci., 21, 9273-9279.
25. Flood, J.F., Uezu, K. & Morley, J.E. (1998) Effect of histamine H2 and H3 receptor modulation in the septum on post-training memory processing. Psychopharmacology, 140, 279-284.
26. Giorgetti, M., Bacciottini, L., Giovannini, M.G., Colivicchi, M.A., Goldfarb, J. & Blandina, P. (2000) Local GABAergic inhibitory tone of acetylcholine release from the cortex of freely moving rats. Eur. J. Neurosci., 12, 1941-1948.
27. 3 receptor agonists and antagonists on cognitive performance and scopolamine-induced amnesia. Behav. Brain Res., 104, 147-155.
28. Haas, H.L. & Reiner, P.B. (1988) Membrane properties of histaminergic tuberomammilary neurones of the rat hypothalamus in vitro. J. Physiol. (Lond.), 399, 633-646.
29. Huang, Z.-L., Qu, W.-M., Li, W.-D., Mochizuki, T., Eguchi, N., Watanabe, T., Urade, Y. & Hayaishi, O. (2001) Arousal effect of orexin A depends on activation of the histaminergic system. Proc. Natl. Acad. Sci. USA, 98, 9965-9970.
30. Inagaki, N., Toda, K., Taniuchi, I., Panula, P., Yamatodani, A., Tohyama, M., Watanabe, T. & 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.
31. Introini-Collison, I.B., Dalmaz, C. & McGaugh, J.L. (1996) Amygdala beta noradrenergic influences on memory storage involve cholinergic activation. Neurobiol. Learn. Mem., 65, 57-64.
32. Knoche, A., Yokoyama, H. & Haas, H. (1999) Histaminergic modulation of 200 Hz oscillations in the hippocampus in vivo. Pflugers Arch., 437, P22-P23.
33. Köhler, C., Swanson, L.W., Haglund, L. & Wu, J.Y. (1985) The cytoarchitecture, histochemistry, and projections of the tuberomammillary nucleus in the rat. Neuroscience, 16, 85-110.
34. Liang, K., Juler, R. & McGaugh, J. (1986) Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Res., 368, 125-133.
35. Lin, J.S., Hou, Y., Sakai, K. & 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.
36. Lin, C.-H., Yeh, S.-H., Lin, C.-H., Lu, K.-T. & Leu, Chang, T.-H., W.-C.&.Geanl, P.-W. (2002) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron, 31, 841-851.
37. Lovenberg, T.W., Roland, B.L., Wilson, S.J., Jiang, A., Pyati, J., Huvar, A., Jackson, M.R. & Erlander, M.G. (1999) Cloning and functional expression of the human histamine H3 receptor. Mol. Pharmacol., 55, 1101-1107.
38. Maren, S. (2001) Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci., 24, 897-931.
39. McGaugh, J.L. (2000) Memory: A century of consolidation. Science, 287, 248-251.
40. McGaugh, J.L., Cahill, L. & Roozendaal, B. (1996) Involvement of the amygdala in memory storage: Interaction with other brain systems. Proc. Natl. Acad. Sci. USA, 93, 13508-13514.
41. McGaugh, J.L. & Izquierdo, I. (2000) The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol. Sci., 21, 208-210.
42. Meguro, K.-I., Yanai, K., Sakai, N., Sakurai, E., Maeyama, K., Sasaki, H. & Watanabe, T. (1995) Effects of thioperamide, a histamine H3 antagonist, on the step-through passive avoidance response and histidine decarboxylase activity in senescence-accelerated mice. Pharmacol. Biochem. Behav., 50, 321-325.
43. Mesulam, M.M., Mufson, E.J., Wainer, B.H. & Levey, A.I. (1983) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience, 10, 1185-1201.
44. Morris, J., Ohman, A. & Dolan, R. (1999) A subcortical pathway to the right amygdala mediating 'unseen' fear. Proc. Natl. Acad. Sci. USA, 96, 1680-1685.
45. Nader, K. & LeDoux, J. (1999) Inhibition of the mesoamygdala dopaminergic pathway impairs the retreival of conditioned fear associations. Behav. Neurosci., 113, 891-901.
46. Onodera, K., Yamatodani, A., Watanabe, T. & Wada, H. (1994) Neuropharmacology of the histaminergic neuron system in the brain and its relationship with behavioral disorders. Progr. Neurobiol., 42, 685-702.
47. Panula, P., Pirvola, U., Auvinen, S. & Airaksinen, M.N. (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience, 28, 585-610.
48. Passani, M.B., Bacciottini, L., Mannaioni, P.F. & Blandina, P. (2000) Central histaminergic system and cognitive processes. Neurosci. Biobehav. Rev., 24, 107-114.
49. 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.
50. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
51. Philippu, A. & Prast, H. (2001) Importance of histamine in modulatory processes, locomotion and memory. Behav. Brain Res., 124, 151-159.
52. 3 receptors in rat brain areas. Neuroscience, 52, 169-189.
53. Ponomarenko, A., Knoche, A., Yokoyama, H., Vogel, Y., Brown, R. & Haas, H. (2001) Histaminergic modulation of the hippocampal high-frequency (200 Hz) oscillations in the rat. 30th European Histamine Research Society Meeting, March 9-12, 2001, Turku Finland, pp. 64.
54. Power, A.E. & McGaugh, J.L. (2002) Phthalic acid amigdalopetal lesion of the nucleus basalis magnocellularis indeces reversible memory deficits in rats. Neurobiol. Learn. Mem., 77, 372-388.
55. Power, A.E., Thal, L.J. & McGaugh, J.L. (2002) Lesions of the nucleus basalis magnocellularis induced by 192 IgG-saporin block memory enhancement with posttraining norepinephrine in the basolateral amygdala. Proc. Natl. Acad. Sci. USA, 99, 2315-2319.
56. Prast, H., Argyriou, A. & Philippu, A. (1996) Histaminergic neurons facilitate social memory in rats. Brain Res., 734, 316-318.
57. Prast, H., Saxer, A. & Philippu, A. (1988) Pattern of in vivo release of endogenous histamine in the mammilary body and the amygdala. Naunyn-Schmiedeberg's Arch. Pharmacol., 337, 53-57.
58. Prast, H., Tran, M., Fischer, H., Kraus, M., Lamberti, C., Grass, K. & Philippu, A. (1999) Histaminergic neurons modulate acethylcholine release in the ventral striatum: Role for H3 histamine receptors. Naunyn-Schmiedeberg's Arch. Pharmacol., 360, 558-564.
59. Reiner, P.B. (1987) Electrophysiological properties of cortically projecting histamine neurons of rat hypothalamus. Neurosci. Lett., 73, 43-47.
60. Roozendaal, B. & McGaugh, J.L. (1997) Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol. Learn. Mem., 67, 176-179.
61. Rudy, J. (1996) Scopolamine administered before and after training impairs both contextual and auditory-cue fear conditioning. Neurobiol. Learn. Mem., 65, 73-81.
62. Sacchetti, B., Ambrogi-Lorenzini, C., Baldi, E., Tassoni, G. & 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.
63. Sakai, K., Mansari, M.E., Lin, J., Zhang, J. & Mercier, G.V. (1990) The posterior hypothalamus in the regulation of wakefulness and paradoxical sleep. In: Mancia, M. (ed.) The Diencephalon and Sleep. Raven Press, New York, pp. 171-198.
64. Schafe, G. & LeDoux, J. (2000) Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci., 20, RC96.
65. Schafe, G.E., Atkins, C.M., Swank, M.W., Bauer, E.P., Sweatt, J.D. & LeDoux, J.E. (2000) Activation of ERK/MAP kinase is required for memory consolidation of Pavlovian fear conditioning. J. Neurosci., 20, 8177-8187.
66. Schafe, G., Nader, K., Blair, H. & LeDoux, J. (2001) Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends Neurosci., 24, 540-546.
67. Selbach, O., Brown, R. & Haas, H. (1997) Long-term increase of hippocampal excitability by histamine and cyclic AMP. Neuropharmacology, 36, 1539-1548.
68. 3 receptor. [28th Annual Meeting of the Society of Neuroscience, San Diego.] Soc. Neurosci. Abstr., 27.
69. Uhlrich, D., Manning, K. & Xue, J.-T. (2002) Effects of activation of the histaminergic tuberomammillary nucleus on visual responses of neurons in the dorsal lateral geniculate nucleus. J. Neurosci., 22, 1098-1107.
70. Vazdarjanova, A. & McGaugh, J.L. (1999) Basolateral amygdala is involved in modulating consolidation of memory for classical conditioning. J. Neurosci., 19, 6615-6622.
71. Vollinga, R.C., deKoning, J.P., Jansen, F.P., Leurs, R., Menge, W.M.P.B. & Timmerman, H. (1994) A new potent and selective histamine H3 receptor agonist, 4-(1H-imidazol-4-yl-methyl) piperidine (immepip). J. Med. Chem., 37, 332-333.
72. Watanabe, T., Taguchi, Y., Shiosaka, S., Tanaka, J., Kubota, H., Terano, Y., Tohyama, M. & Wada, H. (1984) Distribution of the histaminergic neuron system in the central nervous system of rats: A fluorescent immunohistochemical analysis with histidine decarboxylase as a marker. Brain Res., 295, 13-25.
73. Weeber, E., Atkins, C., Selcher, J., Varga, A., Mirnikjoo, B., Paylor, R., Leitges, M. & Sweatt, J. (2000) A role of the b isoform of protein kinase C in fear conditioning. J. Neurosci., 20, 5906.
74. Weiler, H.-T., Hasenöhrl, R., Landeghem, A.V., Landeghem, M.V., Brankack, J., Huston, J. & Haas, H. (1998) Differential modulation of hippocampal signal transfer by tuberomammillary nucleaus stimulation in freely moving rats dependent on behavioral state. Synapse, 28, 294-301.
75. Whalen, P., Rauch, S., Etcoff, N., McInerney, S., Lee, M. & Jenike, M. (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci., 18, 411-418.