Aging Ensembles: Circuit Contributions to Memory Deficits

Hippocampal Place Fields: Relevance to Learning and Memory

Volumn , Issue , 2008, Pages

  Burke, Sara N ^a   Barnes, Carol A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

CA1 place fields; Hippocampal place cells; Hippocampus; Memory decline; Neurons

Indexed keywords

EID: 84920642544     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1093/acprof:oso/9780195323245.003.0028     Document Type: Chapter

References (144)

1. Agnihotri NT, Hawkins RD, Kandel ER, Kentros C (2004) The long-term stability of new hippocampal place fields requires new protein synthesis. PNAS 101:3656-3661.
2. Amaral D, Witter M (1995) Hippocampal formation. In: The Rat Nervous System second edition (Paxinos G, ed.), pp 443-486. San Diego: Academic Press.
3. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93:74-104.
4. Barnes CA, McNaughton BL, O'Keefe J (1983) Loss of place specificity in hippocampal complex spike cells of senescent rat. Neurobiol Aging 4:113-119.
5. Barnes CA, Rao G, McNaughton BL (1996) Functional integrity of NMDA-dependent LTP induction mechanisms across the lifespan of F-344 rats. Learn Mem 3:124-137.
6. Barnes CA, Rao G, Houston FP (2000) LTP induction threshold change in old rats at the perforant path-granule cell synapse. Neurobiol Aging 21:613-620.
7. Barnes CA, Suster MS, Shen J, McNaughton BL (1997) Multistability of cognitive maps in the hippocampus of old rats. Nature 388:272-275.
8. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
9. Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237:42-48.
10. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
11. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243-2246.
12. Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7:30-40.
13. Burke SN, Maurer AP, Navratilova Z, McNaughton BL, Barnes CA (2005) The noncompetitive NMDA receptor antagonist memantine reinstates experience-dependent plasticity in aged rats. Soc Neurosci Abstr 317:12.
14. Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242-252.
15. Buzsaki G (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31:551-570.
16. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52:445-459.
17. Chrobak JJ, Buzsaki G (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14:6160-6170.
18. Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056-3066.
19. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
20. Deupree DL, Turner DA, Watters CL (1991) Spatial performance correlates with in vitro potentiation in young and aged Fischer 344 rats. Brain Res 554:1-9.
21. Dieguez D, Jr., Barea-Rodriguez EJ (2004) Aging impairs the late phase of long-term potentiation at the medial perforant path-CA3 synapse in awake rats. Synapse 52:53-61.
22. Ekstrom AD, Meltzer J, McNaughton BL, Barnes CA (2001) NMDA receptor antagonism blocks experience-dependent expansion of hippocampal "place fields". Neuron 31:631-638.
23. Farr SA, Banks WA, La Scola ME, Flood JF, Morley JE (2000) Permanent and temporary inactivation of the hippocampus impairs T-maze footshock avoidance acquisition and retention. Brain Res 872:242-249.
24. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
25. Fletcher BR, Calhoun ME, Rapp PR, Shapiro ML (2006) Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity. J Neurosci 26:1507-1515.
26. Flood DG (1991) Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. II. Subiculum. Brain Res 540:83-95.
27. Flood DG (1993) Critical issues in the analysis of dendritic extent in aging humans, primates, and rodents. Neurobiol Aging 14:649-654.
28. Flood DG, Guarnaccia M, Coleman PD (1987) Dendritic extent in human CA2-3 hippocampal pyramidal neurons in normal aging and senile dementia. Brain Res 409:88-96.
29. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683.
30. Foster TC, Norris CM (1997) Age-associated changes in Ca(2+)-dependent processes:relation to hippocampal synaptic plasticity. Hippocampus 7:602-612.
31. Gazzaley AH, Thakker MM, Hof PR, Morrison JH (1997) Preserved number of entorhinal cortex layer II neurons in aged macaque monkeys. Neurobiol Aging 18:549-553.
32. Gerrard JL, Kudrimoti H, McNaughton BL, Barnes CA (2001) Reactivation of hippocampal ensemble activity patterns in the aging rat. Behav Neurosci 115:1180-1192.
33. Gerrard JL, Kudrimoti HK, Cowen SL, Redish AD, Rosenzweig ES, Barnes CA, McNaughton BL (2002) Dissociation of pattern and sequence reactivation efficiency in the aged rat hippocampus. Soc Neurosci Abstr 678:7.
34. Gothard KM, Skaggs WE, McNaughton BL (1996a) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16:8027-8040.
35. Gothard KM, Skaggs WE, Moore KM, McNaughton BL (1996b) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16:823-835.
36. Guzowski JF, McNaughton BL, Barnes CA, Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120-1124.
37. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20:3993-4001.
38. Guzowski JF, Miyashita T, Chawla MK, Sanderson J, Maes LI, Houston FP, Lipa P, McNaughton BL, Worley PF, Barnes CA (2006) Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. PNAS 103:1077-1082.
39. Hanks SD, Flood DG (1991) Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. I. CA1 of hippocampus. Brain Res 540:63-82.
40. Hebb D (1949) The Organization of Behavior: A Neurophysiological Theory. New York:Wiley.
41. Hirase H, Leinekugel X, Czurko A, Csicsvari J, Buzsaki G (2001) Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. PNAS 98:9386-9390.
42. Hoffman KL, McNaughton BL (2002) Coordinated reactivation of distributed memory traces in primate neocortex. Science 297:2070-2073.
43. Insausti R, Munoz M (2001) Cortical projections of the non-entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis). Eur J Neurosci 14:435-451.
44. Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7:146-183.
45. Jackson JC, Johnson A, Redish AD (2006) Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J Neurosci 26:12415-12426.
46. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107.
47. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165-182.
48. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280:2121-2126.
49. Keuker JI, Luiten PG, Fuchs E (2003) Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 24:157-165.
50. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
51. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109:195-203.
52. Kowalska DM (1995) Effects of hippocampal lesions on spatial delayed responses in dog. Hippocampus 5:363-370.
53. Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19:4090-4101.
54. Kumar A, Foster TC (2005) Intracellular calcium stores contribute to increased susceptibility to LTD induction during aging. Brain Res 1031:125-128.
55. Landfield PW (1988) Hippocampal neurobiological mechanisms of age-related memory dysfunction. Neurobiol Aging 9:571-579.
56. Lavenex P, Suzuki WA, Amaral DG (2002) Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J Comp Neurol 447:394-420.
57. Lavenex PB, Amaral DG, Lavenex P (2006) Hippocampal lesion prevents spatial relational learning in adult macaque monkeys. J Neurosci 26:4546-4558.
58. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183-1194.
59. Lee HK, Min SS, Gallagher M, Kirkwood A (2005) NMDA receptor-independent long-term depression correlates with successful aging in rats. Nat Neurosci 8:1657-1659.
60. Lee I, Rao G, Knierim JJ (2004a) A double dissociation between hippocampal subfields:differential time course of CA3 and CA1 place cells for processing changed environments. Neuron 42:803-815.
61. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004b) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456-459.
62. Leutgeb JK, Leutgeb S, Moser E, Moser MB (2007) Pattern separation in the dentate gyrus. Science 315:961-966.
63. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295-1298.
64. Malenka RC (2003) Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci 1003:1-11.
65. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
66. Markham JA, McKian KP, Stroup TS, Juraska JM (2005) Sexually dimorphic aging of dendritic morphology in CA1 of hippocampus. Hippocampus 15: 97-103.
67. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410-421.
68. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079-7094.
69. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23-81.
70. Maurer AP, Cowen SL, Burke SN, Barnes CA, McNaughton BL (2006) Organization of hippocampal cell assemblies based on theta phase precession. Hippocampus 16:785-794.
71. McClelland JL, McNaughton BL, O'Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457.
72. McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol 369:302-318.
73. McNaughton BL, Morris RG (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neurosciences 10:408-415.
74. McNaughton BL, Barnes CA, O'Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41-49.
75. Mehta MR, Barnes CA, McNaughton BL (1997) Experience-dependent, asymmetric expansion of hippocampal place fields. PNAS 94:8918-8921.
76. Mehta MR, Quirk MC, Wilson MA (2000) Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25:707-715.
77. Merrill DA, Roberts JA, Tuszynski MH (2000) Conservation of neuron number and size in entorhinal cortex layers II, III, and V/VI of aged primates. J Comp Neurol 422:396-401.
78. Merrill DA, Chiba AA, Tuszynski MH (2001) Conservation of neuronal number and size in the entorhinal cortex of behaviorally characterized aged rats. J Comp Neurol 438:445-456.
79. Mizumori SJ, Lavoie AM, Kalyani A (1996) Redistribution of spatial representation in the hippocampus of aged rats performing a spatial memory task. Behav Neurosci 110:1006-1016.
80. Moore CI, Browning MD, Rose GM (1993) Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3:57-66.
81. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
82. Muller RU, Kubie JL, Ranck JB, Jr. (1987) Spatial firing patterns of hippocampal complexspike cells in a fixed environment. J Neurosci 7:1935-1950.
83. Muller RU, Bostock E, Taube JS, Kubie JL (1994) On the directional firing properties of hippocampal place cells. J Neurosci 14:7235-7251.
84. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19:9497-9507.
85. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7:217-227.
86. Norris CM, Korol DL, Foster TC (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 16:5382-5392.
87. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
88. O'Keefe J, Nadel L (1978) The Hippocampus as a Cognitive Map. Oxford: Claredon Press.
89. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
90. Oler JA, Markus EJ (1998) Age-related deficits on the radial maze and in fear conditioning:hippocampal processing and consolidation. Hippocampus 8:402-415.
91. Oler JA, Markus EJ (2000) Age-related deficits in the ability to encode contextual change:a place cell analysis. Hippocampus 10:338-350.
92. O'Neill J, Senior T, Csicsvari J (2006) Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49:143-155.
93. Pakkenberg B, Gundersen HJ (1997) Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384:312-320.
94. Parsons CG, Quack G, Bresink I, Baran L, Przegalinski E, Kostowski W, Krzascik P, Hartmann S, Danysz W (1995) Comparison of the potency, kinetics and voltagedependency of a series of uncompetitive NMDA receptor antagonists in vitro with anticonvulsive and motor impairment activity in vivo. Neuropharmacology 34:1239-1258.
95. Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9:2907-2918.
96. Peters A, Leahu D, Moss MB, McNally KJ (1994) The effects of aging on area 46 of the frontal cortex of the rhesus monkey. Cereb Cortex 4:621-635.
97. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bosl MR, Lipp HP, Grant SG, Bliss TV, Wolfer DP, Kuhl D (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52:437-444.
98. Pyapali GK, Turner DA (1996) Increased dendritic extent in hippocampal CA1 neurons from aged F344 rats. Neurobiol Aging 17:601-611.
99. Qin YL, McNaughton BL, Skaggs WE, Barnes CA (1997) Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos Trans R Soc Lond B Biol Sci 352:1525-1533.
100. Rapp PR, Gallagher M (1996) Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci U S A 93:9926-9930.
101. Rasmussen T, Schliemann T, Sorensen JC, Zimmer J, West MJ (1996) Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol Aging 17:143-147.
102. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52:461-474.
103. Rogawski MA, Wenk GL (2003) The neuropharmacological basis for the use of memantine in the treatment of Alzheimer's disease. CNS Drug Rev 9:275-308.
104. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179.
105. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA (1997) Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7:549-558.
106. Rosenzweig ES, Redish AD, McNaughton BL, Barnes CA (2003) Hippocampal map realignment and spatial learning. Nat Neurosci 6:609-615.
107. Ryan L, Nadel L, Keil K, Putnam K, Schnyer D, Trouard T, Moscovitch M (2001) Hippocampal complex and retrieval of recent and very remote autobiographical memories: evidence from functional magnetic resonance imaging in neurologically intact people. Hippocampus 11:707-714.
108. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurochem 20:11-21.
109. Shen B, McNaughton BL (1996) Modeling the spontaneous reactivation of experiencespecific hippocampal cell assembles during sleep. Hippocampus 6:685-692.
110. Shen J, Kudrimoti HS, McNaughton BL, Barnes CA (1998) Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience. J Sleep Res 7 Suppl 1:6-16.
111. Shen J, Barnes CA, McNaughton BL, Skaggs WE, Weaver KL (1997) The effect of aging on experience-dependent plasticity of hippocampal place cells. J Neurosci 17:6769-6782.
112. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 Mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52:475-484.
113. Sirota A, Csicsvari J, Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rodents. PNAS 100:2065-2069.
114. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.
115. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-172.
116. Small SA, Tsai WY, DeLaPaz R, Mayeux R, Stern Y (2002) Imaging hippocampal function across the human life span: is memory decline normal or not? Ann Neurol 51:290-295.
117. Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA (2004) Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. PNAS 101:7181-7186.
118. Smith AC, Gerrard JL, Barnes CA, McNaughton BL (2000) Effect of age on burst firing characteristics of rat hippocampal pyramidal cells. Neuroreport 11:3865-3871.
119. Squire LR, Knowlton B, Musen G (1993) The structure and organization of memory. Annu Rev Psychol 44:453-495.
120. Stanis J, Dees J, Gerrard J, Lipa P, VanRhoads S, McNaughton B, Barnes C (2004) Reactivation of hippocampal neural ensemble patterns is NMDA receptor-dependent. Soc Neurosci Abstr 329:20.
121. Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180-186.
122. Swanson LW, Kohler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010-3023.
123. Tanila H, Shapiro M, Gallagher M, Eichenbaum H (1997a) Brain aging: changes in the nature of information coding by the hippocampus. J Neurosci 17:5155-5166.
124. Tanila H, Sipila P, Shapiro M, Eichenbaum H (1997b) Brain aging: impaired coding of novel environmental cues. J Neurosci 17:5167-5174.
125. Teng E, Squire LR (1999) Memory for places learned long ago is intact after hippocampal damage. Nature 400:675-677.
126. Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton BL (2005) Selfmotion and the hippocampal spatial metric. J Neurosci 25:8085-8096.
127. Teyler TJ, DiScenna P (1986) The hippocampal memory indexing theory. Behav Neurosci 100:147-154.
128. Thibault O, Landfield PW (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272:1017-1020.
129. Thompson LT, Best PJ (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509:299-308.
130. Toescu EC, Verkhratsky A, Landfield PW (2004) Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci 27:614-620.
131. Tombaugh GC, Rowe WB, Chow AR, Michael TH, Rose GM (2002) Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats. J Neurosci 22:9932-9940.
132. Turner DA, Deupree DL (1991) Functional elongation of CA1 hippocampal neurons with aging in Fischer 344 rats. Neurobiol Aging 12:201-210.
133. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
134. Vanderwolf CH, Kramis R, Robinson TE (1977) Hippocampal electrical activity during waking behaviour and sleep: analyses using centrally acting drugs. Ciba Found Symp (58):199-226.
135. Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489-6496.
136. West MJ, Coleman PD, Flood DG, Troncoso JC (1994) Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344:769-772.
137. Wilson I, S I, Gallagher M, Eichenbaum H, Tanila H (2005) Age-associated alterarions in place cells are subregion specific. J Neurosci 25:6877-6886.
138. Wilson IA, Gallagher M, Eichenbaum H, Tanila H (2006) Neurocognitive aging: prior memories hinder new hippocampal encoding. Trends Neurosci 29:662-670.
139. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055-1058.
140. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679.
141. Winocur G (1990) Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behav Brain Res 38:145-154.
142. Winter JC (1997) The effects of age on continuous learning in the radial maze. Physiol Behav 61:609-612.
143. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G (1995) Sharp waveassociated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30-46.
144. Zola-Morgan SM, Squire LR (1990) The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 250:288-290.