Effects of ibotenate hippocampal and extrahippocampal destruction on delayed-match and -nonmatch-to-sample behavior in rats

Journal of Neuroscience

Volumn 19, Issue 4, 1999, Pages 1492-1507

  Hampson, Robert E ^a   Jarrard, Leonard E ^b   Deadwyler, Sam A ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b WASHINGTON AND LEE UNIVERSITY   (United States)

Author keywords

Delay tasks; Entorhinal cortex; Hippocampus; Ibotenate lesion; Memory; Subiculum; Training

Indexed keywords

IBOTENIC ACID;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ENTORHINAL CORTEX; HIPPOCAMPUS; HISTOLOGY; LEARNING; MALE; MEMORY; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL ORIENTATION; SUBICULUM; TASK PERFORMANCE; TIME;

EID: 0033558062     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-04-01492.1999     Document Type: Article

References (80)

1. Aggleton JP, Mishkin M (1985) Mammillary-body lesions and visual recognition in monkeys. Exp Brain Res 58:190-197.
2. Aggleton JP, Blindt HS, Rawlins JNP (1989) Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats. Behav Neurosci 103:962-974.
3. Alvarez-Royo P, Zola-Morgan S, Squire LR (1992) Impairment of long-term memory and sparing of short-term memory in monkeys with medial temporal lobe lesions: a response to Ringo. Behav Brain Res 53:1-5.
4. Alvarez-Royo P, Zola-Morgan S, Squire LR (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci 15:3796-3807.
5. Angeli SJ, Murray EA, Mishkin M (1993) Hippocampectomized monkeys can remember one place but not two. Neuropsychologia 31:1021-1030.
6. Bolhuis JJ, Van Kampen HS (1988) Serial position curves in spatial memory of rats: primacy and recency effects. Q J Exp Psychol 40B:135-149.
7. Burwell RD, Amaral DG (1998) Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with entorhinal cortex. J Comp Neurol 391:293-321.
8. Burwell RD, Witter M, Amaral DG (1995) The perirhinal and postrhinal cortices of the rat: a review of neuroanatomical literature and comparison with findings in the monkey brain. Hippocampus 5:390-408.
9. Cassaday HJ, Rawlins JN (1995) Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. Behav Neurosci 109:594-606.
10. Chudasama Y, Muir JI (1997) A behavioral analysis of delayed non-matching to position task: the effects of scopolamine, lesions of the fornix and the prelimbic region in mediating behaviors by rats. Psychopharmacology (Berl) 134:73-82.
11. Coffey PJ, Perry VH, Rawlins JN (1990) An investigation into the early stages of the inflammatory response following ibotenic acid-induced neuronal degeneration. Neuroscience 35:121-132.
12. Correll RE, Scoville WB (1965) Performance on delayed match following lesions of medial temporal lobe structures. J Comp Physiol Psychol 60:360-367.
13. Davidson TL, Jarrard LE (1993) The hippocampus and metabolic state cues. Behav Neural Biol 59:107-111.
14. Deacon RMJ, Rawlins JN P (1995) Serial position effects and duration of memory for nonspatial stimuli in rats. J Exp Psychol Gen 21:285-292.
15. Deadwyler SA, Hampson RE (1997) The significance of neural ensemble codes during behavior and cognition. In: Annual review of neuroscience, Vol 20 (Cowan WM, Shooter EM, Stevens CF, Thompson RF, eds), pp 217-244. Palo Alto, CA: Annual Reviews.
16. Deadwyler SA, Bunn T, Hampson RE (1996) Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J Neurosci 16:354-372.
17. Dunnett SB (1989) Comparison of short-term memory deficits in animal models of aging using an operant delayed response task in rats. In: The biology of memory (Squire LR, Lindenlaub E, eds), pp 581-603. New York: Schattauer Verlag.
18. Eichenbaum H (1997) How does the brain organize memories? Science 277:330-332.
19. Eichenbaum H, Otto T, Cohen NJ (1994) Two functional components of the hippocampal memory system. Behav Brain Sci 17:449-518.
20. Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the CNS. Brain Res 4:269-274.
21. Gaffan D, Murray EA (1992) Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr inertial intervals and fail at matching to sample despite double sample presentations. Behav Neurosci 106:30-38.
22. Gaffan EA, Gaffan D (1992) Less-than-expected variability in evidence for primacy and von Restorff effects in rats non-spatial memory. J Exp Psychol Gen 18:298-301.
23. Glasier MM, Sutton RL, Stein DG (1995) Effects of unilateral entorhinal cortex lesion and ganglioside GM1 treatment on performance in a novel water maze. Neurobiol Learning Memory 64:203-214.
24. Gutnikov SA, Rawlins JNP (1996) Systemic NMDA antagonist CGP-37849 produces non-specific impairment in a working memory task: the effect does not resemble those of AP5 and of lesions of the hippocampus or fornix. Neuropsychologia 34:311-314.
25. Gutnikov SA, Barnes JC, Rawlins JN (1994) Working memory tasks in five-choice operant chambers: use of relative and absolute spatial memories. Behav Neurosci 108:899-910.
26. Hampson RE, Deadwyler SA (1996a) LTP and LTD and the encoding of memory in small ensembles of hippocampal neurons. In: Long-term potentiation, Vol 3 (Baudry M, Davis J, eds), pp 199-214. Cambridge, MA: MIT.
27. Hampson RE, Deadwyler SA (1996b) Ensemble codes involving hippocampal neurons are at risk during delayed performance tests. Proc Natl Acad Sci USA 93:13487-13493.
28. Hampson RE, Heyser CJ, Deadwyler SA (1993) Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav Neurosci 107:715-739.
29. Hampson RE, Byrd DR, Konstantopoulos JK, Bunn T, Deadwyler SA (1995) Proactive interference and short-term memory during performance of a DNMS task in normal rats and rats with hippocampus removed. Soc Neurosci Abstr 21:1215.
30. Hampson RE, Rogers G, Lynch G, Deadwyler SA (1998a) Facilitative effects of the ampakine CX516 on short-term memory in rats: enhancement of delayed-nonmatch-to-sample performance. J Neurosci 18:2740-2747.
31. Hampson RE, Rogers G, Lynch G, Deadwyler SA (1998b) Facilitative effects of the ampakine CX516 on short-term memory in rats: correlations with hippocampal neuronal activity. J Neurosci 18:2748-2763.
32. Holscher C, Schmidt WJ (1994) Quinolinic acid lesion of the rat entorhinal cortex pars medialis produces selective amnesia in allocentric working memory (WM) but not in egocentric WM. Behav Brain Res 63:187-194.
33. Honey RC, Good M (1993) Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. Behav Neurosci 107:23-33.
34. Irle E, Markowitsch HJ (1990) Functional recovery after limbic lesions in monkeys. Brain Res Bull 25:79-92.
35. Jarrard LE (1989) On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. J Neurosci Methods 29:251-259.
36. Jarrard LE (1991) Use of ibotenic acid to selectively lesion brain structures. In: Methods in neurosciences, Vol 7, pp 58-69. New York: Academic.
37. Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9-26.
38. Jarrard LE (1995) What does the hippocampus really do? Behav Brain Res 71:1-10.
39. Jarrard LE, Davidson TL (1994) The hippocampus and complex, nonspatial discrimination: is learning still "not possible"? In: Neurobehavioral plasticity: learning, development and response to brain insults (Spear NE, Spear LP, Woodruff M, eds).
40. Jarrard LE, Feldon J, Rawlins JNP, Sinden JD, Gray JA (1986) The effects of intrahippocampal ibotenate on resistance to extinction after continuous or partial reinforcement. Exp Brain Res 61:519-530.
41. Leonard BW, Amaral DG, Squire LR, Zola-Morgan S (1995) Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. J Neurosci 15:5637-5659.
42. Lyford GL, Gutnikov SA, Clark AM, Rawlins JN (1993) Determinants of non-spatial working memory deficits in rats given intraventricular infusions of the NMDA antagonist AP5. Neuropsychologia 31:1079-1098.
43. Marcn S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88:261-274.
44. McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex of the rat. J Comp Neurol 369:302-318.
45. Meunier M, Bachevalier J, Mishkin M, Murray EA (1993) Effects of visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13:5418-5432.
46. Morris RGM (1991) Distinctive computations and relevant associative processes: hippocampal role in processing, retrieval, but not storage of allocentric spatial memory. Hippocampus 1:287-290.
47. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
48. Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys. J Neurosci 4:2565-2580.
49. Murray EA, Mishkin M (1998) Object recognition and location memory in moneys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18:6568-6582.
50. Naber PA, Witter M (1998) Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284-297.
51. Naber PA, Caballero-Bleda M, Jorritsma-Byham B, Witter M (1997) Parallel input to the hippocampal memory system through peri-and postrhinal cortices. NeuroReport 8:2617-2621.
52. Olton DS, Feustle WA (1981) Hippocampal function required for nonspatial working memory. Exp Brain Res 41:380-389.
53. Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159-4167.
54. Raffaele KC, Olton DS (1988) Hippocampal and amygdaloid involvement in working memory for nonspatial stimuli. Behav Neurosci 102:349-355.
55. Rawlins JNP (1985) Associations across time: the hippocampus as a temporary memory store. Behav Brain Sci 8:479-528.
56. Rawlins JNP, Maxwell TJ, Sinden JD (1988) The effect of fornix section on win-stay/lose-shift and win-shift/lose-stay performance in the rat. Behav Brain Res 31:17-28.
57. Rawlins JNP, Lyford GL, Seferiades A, Deacon RM, Cassaday HJ (1993) Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. Behav Neurosci 107:420-433.
58. Reed JM, Squire LR (1998) Retrograde amnesia for facts and events: findings from four new cases. J Neurosci 18:3943-3954.
59. Ridley RM, Baker HF, Harder JA, Person C (1996) Effects of lesions of different parts of the septo-hippocampal system in primates on learning and retention of information acquired before or after surgery. Brain Res Bull 40:21-32.
60. Ringo JL (1991) Memory decays at the same rate in macaques with and without brain lesions when expressed in d' or arcsine terms. Behav Brain Res 42:123-134.
61. Rothblat LA, Kromer LF (1991) Object recognition memory in the rat: the role of the hippocampus. Behav Brain Res 42:25-32.
62. Rothblat LA, Vnek N, Gleason TC, Kromet LF (1993) Role of parahippocampal region in spatial and non-spatial memory: effects of parahippocampal lesions on rewarded alternation and concurrent object discrimination learning. Behav Brain Res 55:93-100.
63. Shaw C, Aggleton JP (1995) Evidence for the independence of recognition and recency memory in amnesic subjects. Cortex 31:57-71.
64. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195-231.
65. Squire LR, Zola SM (1997) Episodic memory, semantic memory and amnesia. Hippocampus 8:205-211.
66. Steele K, Rawlins JNP (1993) The effects of hippocampectomy on performance by rats of a running recognition task using long lists of non-spatial items. Behav Brain Res 54:1-10.
67. Stefanacci L, Suzuki WA, Amaral DG (1996) Organization of connections between the amygdala complex and the perirhinal and parahippocampal cortices in macaque monkeys. J Comp Neurol 375:552-582.
68. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430-2451.
69. Tamamaki N, Nojyo Y (1995) Preservation of topography in the connections between the subiculum, field CA1 and the entorhinal cortex in rats. J Comp Neurol 353:379-390.
70. Tulving E, Markowitsch HJ (1997) Episodic and declarative memory: role of hippocampus. Hippocampus 8:198-204.
71. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277: 376-380.
72. Wiig K, Burwell RD (1998) Memory impairment on a delayed non-matching-to-position task after lesions of the perirhinal cortex in the rat. Behav Neurosci 112:827-838.
73. Yee BK, Rawlins JN (1994) The effects of hippocampal formation ablation or fimbria-fornix section on performance of a nonspatial radial arm maze task by rats. J Neurosci 14:3766-3774.
74. Yee BK, Feldon J, Rawlins JNP (1997) Cytotoxic lesions of the retrohippocampal region attenuate latent inhibition but spare the partial reinforcement extinction effect. Exp Brain Res 115:247-256.
75. Zola-Morgan S, Squire LR (1990) Identification of the memory system damaged in medial temporal lobe amnesia. In: The biology of memory (Squire LR, Lindelaub E, eds), pp 509-521. Stuttgart: Schattauer.
76. Zola-Morgan S, Squire LR, Mishkin M (1982) The neuroanatomy of amnesia: amygdala-hippocampus versus temporal stem. Science 218:1337-1339.
77. Zola-Morgan S, Squire LR, Amaral DG (1989a) Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in the monkey. J Neurosci 9:897-912.
78. Zola-Morgan S, Squire LR, Amaral DG (1989b) Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation. J Neurosci 9:1922-1936.
79. Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA (1989c) Lesions of the perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci 9:4355-4370.
80. Zola-Morgan S, Squire LR, Clower RP, Rempel NL (1993) Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. J Neurosci 13:251-265.