GABAA receptor activation in the CA1 area of the dorsal hippocampus impairs consolidation of conditioned contextual fear in C57BL/6J mice

Behavioural Brain Research

Volumn 238, Issue 1, 2013, Pages 160-169

  Misane, Ilga ^a,b   Kruis, Ayla ^a   Pieneman, Anton W ^a   Ögren, Sven Ove ^c   Stiedl, Oliver ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b JSC Grindeks   (Latvia)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Auditory and contextual fear conditioning; GABAA receptors; Hippocampal distribution profile; Learning and emotional memory; Muscimol bodipy

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; MUSCIMOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; C57BL 6 MOUSE; CONDITIONING; CONTEXTUAL FEAR; CONTROLLED STUDY; DRUG DISTRIBUTION; FEAR; FLUORESCENCE; HIPPOCAMPAL CA1 REGION; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SHORT TERM MEMORY; TONE DEPENDENT FEAR; TRAINING;

ACOUSTIC STIMULATION; ANIMALS; ASSOCIATION LEARNING; CA1 REGION, HIPPOCAMPAL; CONDITIONING, CLASSICAL; CUES; FEAR; GABA-A RECEPTOR AGONISTS; MALE; MEMORY, LONG-TERM; MICE; MICE, INBRED C57BL; MUSCIMOL;

EID: 84868595771     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.10.027     Document Type: Article

References (59)

1. Selden N.R., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42:335-350.
2. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
3. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 1992, 106:274-285.
4. Maren S., Aharonov G., Fanselow M. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioural Brain Research 1997, 88:261-274.
5. Stiedl O., Birkenfeld K., Palve M., Spiess J. Impairment of conditioned contextual fear of C57BL/6J mice by intracerebral injections of the NMDA receptor antagonist APV. Behavioural Brain Research 2000, 116:157-168.
6. Ambrogi Lorenzini C.G., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of the dorsal hippocampus in acquisition, consolidation and retrieval of the rat's passive avoidance response: a tetrodotoxin functional inactivation study. Brain Research 1996, 730:32-39.
7. Baarendse P.J.J., van Grootheest G., Jansen R.F., Pieneman A.W., ögren S.O., Verhage M., et al. Differential involvement of the dorsal hippocampus in passive avoidance in C57BL/6J and DBA/2J mice. Hippocampus 2008, 18:11-19.
8. Anagnostaras S.G., Maren S., Fanselow M.S. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. Journal of Neuroscience 1999, 19:1106-1114.
9. Fanselow M.S. Contextual fear, gestalt memories, and the hippocampus. Behavioural Brain Research 2000, 110:73-81.
10. Ferreira T.L., Moreira K.M. Effects of dorsal striatum lesions in tone fear conditioning and contextual fear conditioning. Brain Research 2003, 987:17-24.
11. Misane I., Tovote P., Meyer M., Spiess J., ögren S.O., Stiedl O. Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 2005, 15:418-426.
12. Chowdhury N., Quinn J.J., Fanselow M.S. Dorsal hippocampus involvement in trace fear conditioning with long, but not short, trace intervals in mice. Behavioral Neuroscience 2005, 119:1396-1402.
13. Moser M.B., Moser E.I. Functional differentiation in the hippocampus. Hippocampus 1998, 8:608-619.
14. Bannerman D.M., Yee B.K., Good M.A., Heupel M.J., Iversen S.D., Rawlins J.N.P. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behavioral Neuroscience 1999, 113:1170-1188.
15. Fanselow M.S., Dong H-W. Are the dorsal and ventral hippocampus functionally distinct structures. Neuron 2010, 65:7-19.
16. Kenney J.W., Raybuck J.D., Gould T.J. Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning. Hippocampus 2012, 22:1681-1690.
17. Chen C., Kim J.J., Thompson R.F., Tonegawa S. Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behavioral Neuroscience 1996, 110:1177-1180.
18. Goshen I., Brodsky M., Prakash R., Wallace J., Gradinaru V., Ramakrishnan C., et al. Dynamics of retrieval strategies for remote memories. Cell 2011, 147:678-689.
19. Nagahara A.H., McGaugh J.L. Muscimol infused into the medial septal area impairs long-term memory but not short-term memory in inhibitory avoidance, water maze place learning and rewarded alternation tasks. Brain Research 1992, 591:54-61.
20. Holt W.G., Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. Journal of Neuroscience 1999, 19:9054-9062.
21. A agonist muscimol. Experimental Brain Research 2001, 139:39-52.
22. Bast T., Zhang W.N., Feldon J. Dorsal hippocampus and classical fear conditioning to tone and context in rats: effects of local NMDA-receptor blockade and stimulation. Hippocampus 2003, 2003(13):657-675.
23. Gilmartin M.R., Kwapis J.L., Hemstetter F.J. Trace and contextual fear conditioning are impaired following unilateral microinjection of muscimol in the ventral hippocampus or amygdala, but not the medial prefrontal cortex. Neurobiology of Learning and Memory 2012, 97:452-464.
24. Steele P.M., Mauk M.D. Inhibitory control of LTP and LTD: stability of synapse strength. Journal of Neurophysiology 1999, 81:1559-1566.
25. Diamond D.M., Park C.R., Campbell A.M., Woodson J.C. Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the storage of emotional memories and stress-induced amnesia. Hippocampus 2005, 15:1006-1025.
26. Dalton G.L., Wu D.C., Wang Y.T., Floresco S.P., GluN2A Phillips A.G.N.M.D.A GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology 2012, 62:797-806.
27. A receptor agonist muscimol acts preferentially through forebrain high-affinity binding sites. Neuropsychopharmacology 2010, 35:999-1007.
28. Mann E.O., Paulsen O. Role of GABAergic inhibition in hippocampal network oscillations. Trends in Neurosciences 2007, 30:343-349.
29. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 1997, Academic Press, San Diego.
30. Stiedl O., Palve M., Radulovic J., Birkenfeld K., Spiess J. Differential impairment of auditory and contextual fear conditioning by protein synthesis inhibition in C57BL/6N mice. Behavioral Neuroscience 1999, 113:496-506.
31. Stiedl O., Radulovic J., Lohmann R., Birkenfeld K., Palve M., Kammermeier J., et al. Strain and substrain differences in context- and tone-dependent fear conditioning of inbred mice. Behavioural Brain Research 1999, 104:1-12.
32. Bolles R.C., Riley A.L. Freezing as an avoidance response: another look at the operant-respondent distinction. Learning and Motivation 1973, 4:268-275.
33. Fanselow M.S., Bolles R.C. Naloxone and shock-elicited freezing in the rat. Journal of Comparative and Physiological Psychology 1979, 93:736-744.
34. Kirk R.E. Experimental design: procedures for the behavioural sciences 1968, Brooks/Cole, Belmont, CA.
35. Wotjak C.T. C57BLack/BOX? The importance of exact mouse strain nomenclature. Trends in Genetics 2003, 19:183-184.
36. Lewis M.C., Gould T.J. Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice. Hippocampus 2007, 17:462-470.
37. Raybuck J.D., Lattal K.M. Double dissociation of amygdala and hippocampal contributions to trace and delay fear conditioning. PLoS ONE 2011, 6:e15982.
38. Maren S., Holt W.G. Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. Behavioral Neuroscience 2004, 118:97-110.
39. De Zazzo J., Tully T. Dissection of memory formation: from behavioral pharmacology to molecular genetics. Trends in Neurosciences 1995, 18:212-218.
40. Cowan N. What are the differences between long-term, short-term and working memory. Progress in Brain Research 2008, 169:323-338.
41. Kamin L.J. The retention of an incompletely learned avoidance response. Journal of Comparative and Physiological Psychology 1957, 50:457-460.
42. Rudy J.W., Morledge P. Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience 1994, 108:227-234.
43. Yoon T., Okada J., Jung M.W., Kim J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learning and Memory 2008, 15:97-105.
44. Aben B., Stapert S., Blokland A. About the distinction between working memory and short-term memory. Frontiers in Psychology 2012, 3:301.
45. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E.R. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learning and Memory 1998, 5:365-374.
46. Wickelgren W.A. Sparing of short-term memory in an amnestic patient: implications for strength theory of memory. Neuropsychologia 1968, 6:235-244.
47. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience 2003, 23:1517-1523.
48. Moser M-B., Moser E.I. Distributed encoding and retrieval of spatial memory in the hippocampus. Journal of Neuroscience 1998, 18:7537-7542.
49. Walker D.L., Davis M. Involvement of NMDA receptors within the amygdala in short-versus long-term memory for fear conditioning as assessed with fear-potentiated startle. Behavioral Neuroscience 2000, 114:1019-1033.
50. Rosenzweig M.R., Bennett E.L., Colombo P.J., Lee D.W., Serrano P.A. Short-term, intermediate-term, and long-term memories. Behavioural Brain Research 1993, 57:193-198.
51. Morice E., Andreae L.C., Cooke S.F., Vanes L., Fisher E.M.C., Tybulewicz V.L.J., et al. Preservation of long-term memory and synaptic plasticity despite short-term impairments in the Tc1 mouse model of Down syndrome. Learning and Memory 2008, 15:492-500.
52. Jarome T.J., Werner C.T., Kwapis J.L., Helmstetter F.J. Activity dependent protein degradation is critical for the formation and stability of fear memory in the amygdala. PLoS ONE 2011, 6:e24349.
53. Wilensky A.E., Schafe G.E., LeDoux J.E. Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. Journal of Neuroscience 1999, 19:RC48.
54. McEown K., Treit D. Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Research 2010, 1353:145-151.
55. Curran A.K., Peraza D., Elinsky C.A., Leiter J.C. Enhanced baroreflex-mediated inhibition of respiration after muscimol dialysis in the rostroventrolateral medulla. Journal of Applied Physiology 2000, 92:2554-2564.
56. 1A receptors in learning and memory. Behavioural Brain Research 2008, 195:54-77.
57. Klausberger T. GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. European Journal of Neuroscience 2009, 30:947-957.
58. Allen T.A., Narayanan N.S., Kholodar-Smith D.B., Zhao Y., Laubach M., Brown T.H. Imaging the spread of reversible brain inactivations using fluorescent muscimol. Journal of Neuroscience Methods 2008, 171:30-38.
59. Place R., Lykken C., Beer Z., Suh J., McHugh T.J., Tonegawa S., et al. NMDA signaling in CA1 mediates selectively the spatial component of episodic memory. Learning and Memory 2012, 19:164-169.