Hippocampal lesions impair rapid learning of a continuous spatial alternation task

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Kim, Steve M ^a   Frank, Loren M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID; N METHYLASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING DISORDER; LEARNING TEST; LOCOMOTION; MALE; MEMORY CONSOLIDATION; MENTAL TASK; MOTIVATION; NONHUMAN; RAT; RECALL; SPATIAL ORIENTATION; TASK PERFORMANCE; WORKING MEMORY; ANIMAL; BEHAVIOR; DRUG EFFECT; LEARNING; LONG EVANS RAT; PATHOLOGY; STEREOTACTIC PROCEDURE;

RATTUS;

ANIMALS; HIPPOCAMPUS; LEARNING; MALE; N-METHYLASPARTATE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, LONG-EVANS; SPATIAL BEHAVIOR; STEREOTAXIC TECHNIQUES;

EID: 65549112962     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005494     Document Type: Article

References (78)

1. Amaral DG, Witter MP (1995) Hippocampal Formation. In: Paxinos C, ed. The Rat Nervous System Academic Press. pp 443-493.
2. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20: 11-21.
3. Rempel-Clower NL, Zola SM, Squire LR, Amaral DG (1996) Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci 16: 5233-5255.
4. Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, et al. (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20: 451-463.
5. Spiers HJ, Maguire EA, Burgess N (2001) Hippocampal amnesia. Neurocase 7: 357-382.
6. Pouzet B, Welzl H, Gubler MK, Broersen L, Veenman CL, et al. (1999) The effects of NMDA-induced retrohippocampal lesions on performance of four spatial memory tasks known to be sensitive to hippocampal damage in the rat. Eur J Neurosci 11: 123-140.
7. Riedel G, Micheau J, Lam AG, Roloff EL, Martin SJ, et al. (1999) Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2: 898-905.
8. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20: 8853-8860.
9. Cimadevilla JM, Wesierska M, Fenton AA, Bures J (2001) Inactivating one hippocampus impairs avoidance of a stable room-defined place during dissociation of arena cues from room cues by rotation of the arena. Proc Natl Acad Sci U S A 98: 3531-3536.
10. Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5: 458-462.
11. Brun VH, Ytterbo K, Morris RG, Moser MB, Moser EI (2001) Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation. J Neurosci 21: 356-362.
12. Day M, Langston R, Morris RG (2003) Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424: 205-209.
13. Jarrard LE, Davidson TL, Bowring B (2004) Functional differentiation within the medial temporal lobe in the rat. Hippocampus 14: 434-49.
14. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, et al. (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313: 1141-1144.
15. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397: 613-616.
16. Wiebe SP, Staubli UV (1999) Dynamic filtering of recognition memory codes in the hippocampus. J Neurosci 19: 10562-10574.
17. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27: 169-178.
18. Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227-1239.
19. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37: 485-497.
20. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, et al. (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-623.
21. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, et al. (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312: 758-762.
22. Hok V, Lenck-Santini PP, Roux S, Save E, Muller RU, et al. (2007) Goal-related activity in hippocampal place cells. J Neurosci 27: 472-82.
23. Lipton PA, White JA, Eichenbaum H (2007) Disambiguation of overlapping experiences by neurons in the medial entorhinal cortex. J Neurosci 27: 5787-5795.
24. Manns JR, Howard MW, Eichenbaum H (2007) Gradual changes in hippocampal activity support remembering the order of events. Neuron 56: 530-540.
25. Huxter JR, Senior TJ, Allen K, Csicsvari J (2008) Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci 11: 587-594.
26. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321: 1322-1327.
27. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322: 1865-1868.
28. Bostock E, Muller RU, Kubie JL (1991) Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1: 193-205.
29. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261: 1055-1058.
30. Lee I, Rao G, Knierim JJ (2004) A double dissociation between hippocampal subfields: differential time course of CA3 and CA1 place cells for processing changed environments. Neuron 42: 803-815.
31. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305: 1295-1298.
32. Frank LM, Stanley GB, Brown EN (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24: 7681-7689.
33. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806.
34. Anderson MI, Killing S, Morris C, O'Donoghue A, Onyiagha D, et al. (2006) Behavioral correlates of the distributed coding of spatial context. Hippocampus 16: 730-742.
35. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, et al. (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079-7094.
36. Kobayashi T, Nishijo H, Fukuda M, Bures J, Ono T (1997) Task-dependent representations in rat hippocampal place neurons. J Neurophysiol 78: 597-613.
37. Kobayashi T, Tran AH, Nishijo H, Ono T, Matsumoto G (2003) Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats. Neuroscience 117: 1025-1035.
38. Lee I, Griffin AL, Zilli EA, Eichenbaum H, Hasselmo ME (2006) Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron 51: 639-650.
39. Ji D, Wilson MA (2008) Firing rate dynamics in the hippocampus induced by trajectory learning. J Neurosci 28: 4679-4689.
40. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93: 74-104.
41. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
42. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, et al. (2003) Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358: 773-786.
43. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI (2001) Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21: 1635-1644.
44. Hollup SA, Kjelstrup KG, Hoff J, Moser MB, Moser EI (2001) Impaired recognition of the goal location during spatial navigation in rats with hippocampal lesions. J Neurosci 21: 4505-4513.
45. Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227-1239.
46. Jeffery KJ, Gilbert A, Burton S, Strudwick A (2003) Preserved performance in a hippocampal-dependent spatial task despite complete place cell remapping. Hippocampus 13: 175-189.
47. Smith DM, Mizumori SJ (2006) Hippocampal place cells, context, and episodic memory. Hippocampus 16: 716-729.
48. Ainge JA, Tamosiunaite M, Woergoetter F, Dudchenko PA (2007) Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. J Neurosci 27: 9769-9779.
49. Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5: 458-462.
50. Manns JR, Howard MW, Eichenbaum H (2007) Gradual changes in hippocampal activity support remembering the order of events. Neuron 56: 530-540.
51. Karlsson MP, Frank LM (2008) Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neurosci 28: 14271-14281.
52. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623-633.
53. Ainge JA, van der Meer MA, Langston RF, Wood ER (2007) Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 17: 988-1002.
54. Brunner E, Domhof S, Langer F (2002) Nonparametric Analysis of Longitudinal Data in Factorial Experiments. Wiley. 261 p.
55. Olton DS, Becker JT, Handelmann GE (1979) Hippocampus, space, and memory. Behav Brain Sci 2: 313-365.
56. Smith AC, Frank LM, Wirth S, Yanike M, Hu D, et al. (2004) Dynamic analysis of learning in behavioral experiments. J Neurosci 24: 447-461.
57. McNish KA, Gewirtz JC, Davis M (1997) Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J Neurosci 17: 9353-9360.
58. Good M, Honey RC (1997) Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111: 487-493.
59. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, et al. (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113: 1170-1188.
60. Godsil BP, Stefanacci L, Fanselow MS (2005) Bright light suppresses hyperactivity induced by excitotoxic dorsal hippocampus lesions in the rat. Behav Neurosci 119: 1339-1352.
61. Faraji J, Lehmann H, Metz GA, Sutherland RJ (2008) Rats with hippocampal lesion show impaired learning and memory in the ziggurat task: a new task to evaluate spatial behavior. Behav Brain Res 189: 17-31.
62. Davidson TL, Chan K, Jarrard LE, Kanoski SE, Clegg DJ, et al. (2008) Contributions of the hippocampus and medial prefrontal cortex to energy and body weight regulation. Hippocampus.
63. Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65: 65-72.
64. Gluck MA, Meeter M, Myers CE (2003) Computational models of the hippocampal region: linking incremental learning and episodic memory. Trends Cogn Sci 7: 269-276.
65. Foster DJ, Morris RG, Dayan P (2000) A model of hippocampally dependent navigation, using the temporal difference learning rule. Hippocampus 10: 1-16.
66. Johnson A, Redish AD (2005) Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model. Neural Netw 18: 1163-71.
67. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440: 680-683.
68. Schmelzeis MC, Mittleman G (1996) The hippocampus and reward: effects of hippocampal lesions on progressive-ratio responding. Behav Neurosci 110: 1049-1066.
69. Whishaw IQ, Tomie JA (1997) Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus 7: 361-370.
70. Flaherty CF, Coppotelli C, Hsu D, Otto T (1998) Excitotoxic lesions of the hippocampus disrupt runway but not consummatory contrast. Behav Brain Res 93: 1-9.
71. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, et al. (1999) Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113: 1170-1188.
72. Holland PC, Lamoureux JA, Han JS, Gallagher M (1999) Hippocampal lesions interfere with Pavlovian negative occasion setting. Hippocampus 9: 143-157.
73. Best PJ, White AM, Minai A (2001) Spatial processing in the brain: the activity of hippocampal place cells. Annu Rev Neurosci 24:459-86.: 459-486.
74. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330.
75. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440: 680-683.
76. Paxinos G, Watson C (2004) The Rat Brain in Stereotaxic Coordinates. Academic Press. 209 p.
77. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263.
78. Hen I, Sakov A, Kafkafi N, Golani I, Benjamini Y (2004) The dynamics of spatial behavior: how can robust smoothing techniques help? J Neurosci Methods 133: 161-172.