Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice

Neurobiology of Learning and Memory

Volumn 90, Issue 2, 2008, Pages 426-433

  Dillon, Gregory M ^a   Qu, Xianlu ^a   Marcus, Jacob N ^a   Dodart, Jean Cosme ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

C57Bl 6 mice; CA1; Extinction learning; Hippocampus; Lesion; Spatial discrimination; Spontaneous alternation

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; EXCITOTOXICITY; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NONHUMAN; SPATIAL DISCRIMINATION; TASK PERFORMANCE;

ANIMALS; APPETITIVE BEHAVIOR; BRAIN MAPPING; CONDITIONING, OPERANT; DISCRIMINATION LEARNING; DOMINANCE, CEREBRAL; EXTINCTION, PSYCHOLOGICAL; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MENTAL RECALL; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; N-METHYLASPARTATE; ORIENTATION; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 48749094965     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.05.008     Document Type: Article

References (53)

1. Arns M., Sauvage M., and Steckler T. Excitotoxic hippocampal lesions disrupt allocentric spatial learning in mice: Effects of strain and task demands. Behavior and Brain Research 106 (1999) 151-164
2. Bardgett M.E., Baum K.T., O'Connell S.M., Lee N.M., and Hon J.C. Effects of risperidone on locomotor activity and spatial memory in rats with hippocampal damage. Neuropharmacology 51 7-8 (2006) 1156-1162
3. Benveniste H., Drejer J., Schousboe A., and Diemer N.H. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. Journal of Neurochemistry 43 5 (1984) 1369-1374
4. Cain D.P., Boon F., and Corcoran M.E. Thalamic and hippocampal mechanisms in spatial navigation: A dissociation between brain mechanisms for learning how versus learning where to navigate. Behavior and Brain Research 170 2 (2006) 241-256
5. Cho Y.H., Friedman E., and Silva A.J. Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behavioural Brain Research 98 (1999) 77-87
6. Clark B.J., Hines D.J., Hamilton D.A., and Whishaw I.Q. Movements of exploration intact in rats with hippocampal lesions. Behavioural Brain Research 163 (2005) 91-99
7. Corbit L.H., and Balleine B.W. The role of the hippocampus in instrumental conditioning. Journal of Neuroscience 20 11 (2000) 4233-4239
8. Deacon R.M.J., Bannerman D.M., Kirby B.P., Croucher A., Nicholas J., and Rawlins P. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behavioural Brain Research 133 (2002) 57-68
9. Dember W.M., and Fowler H. Spontaneous alternation behavior. Psychology Bulletin 55 6 (1958) 412-428
10. DiMattia B.D., and Kesner R.P. Spatial cognitive maps: Differential role of parietal cortex and hippocampal formation. Behavioral Neuroscience 102 4 (1988) 471-480
11. Engelsen B.A., Fosse V.M., Myrseth E., and Fonnum F. Elevated concentrations of glutamate and aspartate in human ventricular cerebrospinal fluid (vCSF) during episodes of increased CSF pressure and clinical signs of impaired brain circulation. Neuroscience Letters 62 1 (1985) 97-102
12. Gilbert P.E., Kesner R.P., and Lee I. Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1. Hippocampus 11 (2001) 626-636
13. Goddyn H., Leo S., Meert T., and D'Hooge R. Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions. Behavioral Brain Research 173 1 (2006) 138-147
14. Goodrich-Hunsaker N.J., Hunsaker M.R., and Kesner R.P. The interactions and dissociations of the dorsal hippocampus subregions: How the dentate gyrus, CA3, and CA1 process spatial information. Behavioral Neuroscience 122 1 (2008) 16-26
15. Honey R.C., Marshall V.J., McGregor A., Futter J., and Good M. Revisiting places passed: Sensitization of exploratory activity in rats with hippocampal lesions. The Quarterly Journal of Experimental Psychology 60 5 (2007) 625-634
16. Hunsaker M.R., Thorup J.A., Welch T., and Kesner R.P. The role of CA3 and CA1 in the acquisition of an object-trace-place paired-associate task. Behavioral Neuroscience 120 6 (2006) 1252-1256
17. Isseroff A. Limited recovery of spontaneous alternation after extensive hippocampal damage: Evidence for a memory impairment. Experimental Neurology 64 2 (1979) 284-294
18. Jackson W.J., and Strong Jr. P.N. Differential effects of hippocampal lesions upon sequential tasks and maze learning by the rat. Journal of Comparative Physiology and Psychology 68 3 (1969) 442-450
19. Kesner R.P., Gilbert P.E., and Wallenstein G.V. Testing neural network models of memory with behavioral experiments. Current Opinion in Neurobiology 10 (2000) 260-265
20. Kesner R.P., Lee J., and Gilbert P.E. A behavioral assessment of hippocampal function based on a subregional analysis. Reviews in the Neuroscience 119 (2004) 781-786
21. Kim J.J., Rison R.A., and Fanselow M.S. Effects of amygdala, hippocampus and periacqueductal gray lesions on short- and long-term contextual fear. Behavioral Neuroscience 107 (1993) 1093-1098
22. Kimble D.P. Hippocampus and internal inhibition. Psychology Bulletin 70 5 (1968) 285-295
23. Kimble D.P. Choice behavior in rats with hippocampal lesions. In: Isaacson R.L., and Pribram K.H. (Eds). The hippocampus, neurophysiology and behavior Vol. 2 (1975), Plenum Press, New York 309-326
24. Kimble D.P., Bremiller R., Schroeder L., and Smotherman W.P. Hippocampal lesions slow extinction of a conditioned taste aversion in rats. Physiology of Behavior 23 (1979) 217-222
25. Kirkby R.J., Stein D.G., Kimble R.J., and Kimble D.P. Effects of hippocampal lesions and duration of sensory input on spontaneous alternation. Journal Comparative Physiology and Psychology 2 (1967) 342-345
26. Lalonde R. The neurobiological basis of spontaneous alternation. Neuroscience and Biobehavioral Reviews 26 1 (2002) 91-104
27. Lee I., Jerman T.S., and Kesner R.P. Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus. Neurobiology of Learning and Memory 84 (2005) 138-147
28. Leslie J.C., Shaw D., McCabe C., Reynolds D.S., and Dawson G.R. Effects of drugs that potentiate GABA on extinction of positively-reinforced operant behaviour. Neuroscience Biobehavioral Reviews 28 3 (2004) 229-238
29. Logue S.F., Paylor R., and Wehner J.M. Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behavioral Neuroscience 111 (1997) 104-113
30. Means L.W., Leander J.D., and Isaacson R.L. The effects of hippocampectomy on alternation behavior and response of novelty. Physiology of Behavior 6 1 (1971) 17-22
31. Misane I., Tovote P., Meyer M., Spiess J., Ogren S.O., and Stiedl O. Time dependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 15 (2005) 418-426
32. Monaghan D.T., Yao D., and Cotman C.W. L-[3H]Glutamate binds to kainate-, NMDA- and AMPA-sensitive binding sites: an autoradiographic analysis. Brain Research 340 2 (1985) 378-383
33. Morris R.G., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 5868 (1982) 681-683
34. Nakazawa K., Quirk M.C., Chitwood R.A., Wantanabe M., Yeckel M.F., Sun L.D., et al. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297 (2002) 211-215
35. Niewoehner B., Single F.N., Hvalby O., Jensen V., Meyer zum Alten Borgloh S., Seeburg P.H., et al. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. European Journal of Neuroscience 25 (2007) 837-846
36. Okada T., Yamada N., Tsuzuki K., Horikawa H.P.M., Tanaka K., and Ozawa S. Long-term potentiation in the hippocampal CA1 area and dentate gyrus plays different roles in spatial learning. European Journal of Neuroscience 17 (2003) 341-349
37. Olton D.S., and Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 17 6 (1979) 669-682
38. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 2 (1992) 274-285
39. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 1 (2008) 56-72
40. Rempel-Clower N.L., Zola S.M., Squire L.R., and Amaral D.G. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience 16 16 (1996) 5233-5255
41. Rescorla R.A. The psychology of learning: Conditioning and associative learning. Science 223 4634 (1984) 388-389
42. Rescorla R.A., and Heth C.D. Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychology of Animal Behavior Process 1 1 (1975) 88-96
43. Ridley R.M., Timothy C.J., Maclean C.J., and Baker H.F. Conditional learning and memory impairments following neurotoxic lesion of the CA1 field of the hippocampus. Neuroscience 67 2 (1995) 263-275
44. Rogers J.L., Hunsaker M.R., and Kesner R.P. Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning. Neurobiology of Learning and Memory 86 (2006) 72-81
45. Rogers J.L., and Kesner R.P. Hippocampal-parietal cortex interactions: Evidence from a disconnection study in the rat. Behavioral Brain Research 179 1 (2007) 19-27
46. Rondi-Reig L., Petit G.H., Tobin C., Tonegawa S., Mariani J., and Berthoz A. Impaired sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. Journal of Neuroscience 26 15 (2006) 4071-4081
47. Scoville W.B., and Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology and Neurosurgical Psychiatry 20 (1957) 11-21
48. Squire L.R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychology Review 99 (1992) 195-231
49. Stevens R. Effects of duration of sensory input and intertrial interval on spontaneous alternation in rats with hippocampal lesions. Physiology of Psychology 1 (1973) 41-44
50. Tsien J.Z., Huerta P.T., and Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87 (1996) 1327-1338
51. Walsh T.J., Schulz D.W., Tilson H.A., and Schmechel D.E. Colchicine-induced granule cell loss in rat hippocampus: Selective behavioral and histological alterations. Brain Research 198 (1986) 23-36
52. Winocur G., and Olds J. Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. Journal of Comparative Physiology and Psychology 92 2 (1978) 312-321
53. Zola S.M., Squire L.R., Teng E., Stefanacci L., Buffalo E.A., and Clark R.E. Impaired recognition memory in monkeys after damage limited to the hippocampal region. The Journal of Neuroscience 20 1 (2000) 451-463