Transient activation of the CA3 Kappa opioid system in the dorsal hippocampus modulates complex memory processing in mice

Neurobiology of Learning and Memory

Volumn 88, Issue 1, 2007, Pages 94-103

  Daumas, Stéphanie ^a   Betourne, Alexandre ^a   Halley, Hélène ^a   Wolfer, David P ^b   Lipp, Hans Peter ^b   Lassalle, Jean Michel ^a   Francés, Bernard ^a  

^a Université Paul Sabatier   (France)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

CA3 hippocampus; Fear conditioning; Kappa opioid receptor; Mouse; Spatial memory; Water maze

Indexed keywords

DYNORPHIN A; KAPPA OPIATE RECEPTOR; NORBINALTORPHIMINE; WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; DRUG ACTIVATION; DRUG INACTIVATION; DRUG MIXTURE; FEAR; FREEZING; HIPPOCAMPUS; INFORMATION; LEARNING; MALE; MAZE TEST; MEMORY; MICROINJECTION; MODULATION; MOUSE; NONHUMAN; TASK PERFORMANCE; TOPOGRAPHY;

EID: 34249279807     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2007.02.001     Document Type: Article

References (47)

1. D'Adamo P., Wolfer D.P., Kopp C., Tobler I., Toniolo D., and Lipp H.-P. Mice deficient for the synaptic vesicle protein Rab3a show impaired spatial reversal learning and increased explorative activity but none of the behavioral changes shown by mice deficient for the Rab3a regulator Gdi1. European Journal of Neuroscience 19 (2004) 1895-1905
2. Chen G., Chen K.S., Knox J., Inglis J., Bernard A., Martin S.J., et al. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408 (2000) 975-979
3. Chen L., Gu Y., and Huang L.Y. The mechanism of action for the block of NMDA receptor channels by the opioid peptide dynorphin. Journal of Neuroscience 15 (1995) 4602-4611
4. Cohen G.A., Doze V.A., and Madison D.V. Opioid inhibition of GABA release from presynaptic terminals of rat hippoacampal interneurons. Neuron 9 (1992) 325-335
5. Daumas S., Halley H., Francés B., and Lassalle J.M. Encoding, consolidation and retrieval of contextual memory: differential involvement of CA3 and CA1 hippocampal subregions. Learning and Memory 12 (2005) 375-382
6. Daumas S., Halley H., and Lassalle J.M. Disruption of hippocampal CA3 network: effects on episodic-like memory processing in C57Bl/6J mice. European Journal of Neuroscience 20 (2004) 597-600
7. Derrick B.E., Rodriguez S.B., Lieberman D.N., and Martinez J.L. Mu opioid receptors are associated with the induction of hippocampal mossy fiber long-term-potentiation. Journal of Pharmacology and Experimental Therapeutics 263 (1992) 725-733
8. Do V.H., Martinez C.O., Martinez J.L., and Derrick B.E. Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. Journal of Neurophysiology 87 (2002) 669-678
9. Drake C., Terman G., Simmons M., Milner T., Kunkel D., Schwartzkroin P., et al. Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. Journal of Neuroscience 14 (1994) 3736-3750
10. Ergorul C., and Eichenbaum H. The hippocampus and memory for "what", "where" and "when". Learning and Memory 11 (2004) 397-405
11. Franklin K.B.J., and Paxinos G. The mouse brain in stereotaxic coordinates (1997), Academic Press, San Diego
12. 3H]-LY255582 binding sites in mouse brain: comparison with the distribution of mu, delta and kappa binding sites. Neuropeptides 39 (2005) 559-567
13. Gall C. Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers. The Journal of Neuroscience 8 (1988) 1852-1862
14. Gall C., Brecha N., Karten H.J., and Chang K.J. Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. Journal of Comparative Neurology 198 (1981) 335-350
15. Hiramatsu M., and Hoshino T. Involvement of κ-opioid receptors and σ receptors in memory function demonstrated using an antisense strategy. Brain Research 1030 (2004) 247-255
16. Hiramatsu M., Inoue K., and Kameyama T. DynorphinA (1-13) and (2-13) improve β-amyloid peptide-induced amnesia in mice. Neuroreport 11 (2000) 431-435
17. Hiramatsu M., and Kameyama T. Roles of kappa-opioid receptor agonists in learning and memory impairment in animal models. Methods and Findings in Experimental and Clinical Pharmacology 20 (1998) 595-599
18. Itoh J., Ukai M., and Kameyama T. Dynorphin A (1-13) potently improves the impairment of spontaneous alternation performance induced by the mu-selective opioid receptor agonist DAMGO in mice. Journal of Pharmacology and Experimental Therapeutics 269 (1994) 15-21
19. Jamot L., Matthes H.W., Simonin F., Kieffer B.L., and Roder J.C. Differential involvement of the mu and kappa opioid receptors in spatial learning. Genes Brain and Behavior 2 (2003) 80-92
20. Krug M., Brodemann R., and Wagner M. Simultaneous activation and opioid modulation of long-term potentiation in the dentate gyrus and the hippocampal CA3 region after stimulation of the perforant pathway in freely moving rats. Brain Research 913 (2001) 68-77
21. Lassalle J.M., Bataille T., and Halley H. Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning but neither consolidatiion nor memory retrieval in the Morris navigation task. Neurobiology of Learning and Memory 73 (2000) 243-257
22. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 23 (2000) 155-184
23. Lee I., and Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14 (2004) 301-310
24. Levy W.B. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6 (1996) 579-590
25. Mathieu-Kia A.M., Fan L.Q., Kreek M.J., Simon E.J., and Hiller J.M. Mu-, delta- and kappa-opioid receptor populations are differentially altered in distinct areas of postmortem brains of Alzheimer's disease patients. Brain Research 893 (2001) 121-134
26. McDaniel K.L., Mundy W.R., and Tilson H.A. Microinjection of dynorphin into the hippocampus impairs spatial learning in rats. Pharmacology, Biochemistry and Behavior 35 (1990) 429-435
27. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Oxford University Press Clarendon
28. Pan Z.Z. Mu-opposing actions of the kappa-opioid receptor. Trends in Pharmacological Sciences 19 (1998) 94-98
29. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioural Neuroscience 106 (1992) 274-285
30. Racz B., Fuzesi M., and Halasy K. The hippocampal opioidergic system: a comparative immunocytochemical study in four rodents. Neurobiology (Bp) 6 (1998) 429-441
31. Riedel G., Micheau J., Lam A.G., Roloff E., Martin S.J., Bridge H., et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nature Neuroscience 2 (1999) 898-905
32. Rolls E.T., and Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology 79 (2006) 1-48
33. Rolls E.T., and Treves A. Neural networks and brain function (1998), Oxford University Press, New York 418.
34. Rudy J.W., Huff N.C., and Matus-Amat P. Understanding contextual fear conditioning: insights from a two-process model. Neuroscience and Biobehavioral Reviews 28 (2004) 675-685
35. Sagratella S., Longo R., and Domenici M.R. Selective opposite modulation of dentate granule cells excitability by μ and κ opioids in rat hippocampal slices. Neuroscience Letters 205 (1996) 53-56
36. Salin P.A., Weisskopf M.G., and Nicoll R.A. A comparison of the role of dynorphin in the hippocampal mossy fiber pathway in guinea pig and rat. Journal of Neuroscience 15 (1995) 6939-6945
37. Sandin J., Nylander I., Georgieva J., Schott P.A., Ogren S.O., and Terenius L. Hippocampal dynorphin B injections impair spatial learning in rats: a kappa-opioid receptor-mediated effect. Neuroscience 85 (1998) 375-382
38. Schwegler H., and Lipp H.-P. Hereditary covariations of neuronal circuitry and behavior: correlations between the proportions of hippocampal synaptic fields in the regio inferior and two-way avoidance in mice and rats. Behavioral Brain Research 7 (1983) 1-39
39. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Reviews 99 (1992) 195-231
40. Steele R.J., and Morris R.G. Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9 (1999) 118-136
41. Terman G.W., Drake C.T., Simmons M.L., Milner T.A., and Chavkin C. Opioid modulation of recurrent excitation in the hippocampal dentate gyrus. Journal of Neuroscience 20 (2000) 4379-4388
42. Ukai M., Itoh J., Kobayashi T., Shinkai N., and Kameyama T. Effects of kappa-opioid dynorphin A (1-13) on learning and memory in mice. Behavioral Brain Research 83 (1997) 169-172
43. Wagner J.J., Terman G.W., and Chavkin C. Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363 (1993) 451-454
44. Weisskopf M.G., Zalutsky R.A., and Nicoll R.A. The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fiber synapses and modulates long-term potentiation. Nature 362 (1993) 423-427
45. Williams S.H., and Johnston D. Actions of endogenous opioids on NMDA receptor-independent long term potentiation in area CA3 of the hippocampus. Journal of Neuroscience 16 (1996) 3652-3660
46. Xie C.W., and Lewis D.V. Endogenous opioids regulate long-term potentiation of synaptic inhibition in the dentate gyrus of rat hippocampus. Journal of Neurosciences 15 (1995) 3788-3795
47. Yeckel M.F., and Berger T.W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proceedings of the National Academy of Sciences (USA) 87 (1990) 5832-5836