Reverberation, storage, and postsynaptic propagation of memories during sleep

Learning and Memory

Volumn 11, Issue 6, 2004, Pages 686-696

  Ribeiro, Sidarta ^a   Nicolelis, Miguel A L ^a,b,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Duke University   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DREAMING; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY CONSOLIDATION; MOLECULAR MECHANICS; NEOCORTEX; NERVE CELL; NERVE STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; REM SLEEP; REVIEW; SLEEP; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; SOMATOSENSORY CORTEX; SYNAPSE;

ANIMALS; BRAIN; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NEOCORTEX; NEURONS; RABBITS; RATS; SLEEP STAGES; SYNAPSES; THINKING;

EID: 10044230783     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.75604     Document Type: Review

References (170)

1. Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R., and Bourtchouladze, R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626.
2. Abraham, W.C., Mason, S.E., Demmer, J., Williams, J.M., Richardson, C.L., Tate, W.P., Lawlor, P.A., and Dragunow, M. 1993. Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 56: 717-727.
3. Adey, W.R., Dunlop, C.W., and Hendrix, C.E. 1960. Hippocampal slow waves: Distribution and phase relationship in the course of approach learning. Arch. Neurol. 3: 74-90.
4. Agranoff, B.W., Davis, R.E., and Brink, J.J. 1966. Chemical studies on memory fixation in goldfish. Brain Res. 1: 303-309.
5. Arnolds, D.E., Lopes da Silva, F.H., Aitink, J.W., Kamp, A., and Boeijinga, P. 1980. The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalogr. Clin. Neurophysiol. 50: 324-328.
6. Aserinsky, E. and Kleitman, N. 1953. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118: 273-274.
7. Ayala-Guerrero, F., Mexicano, G., and Ramos, J.I. 2003. Sleep characteristics in the turkey Meleagris gallopavo. Physiol. Behav. 78: 435-440.
8. Basheer, R., Sherin, J.E., Saper, C.B., Morgan, J.I., McCarley, R.W., and Shiromani, P.J. 1997. Effects of sleep on wake-induced c-fos expression. J. Neurosci. 17: 9746-9750.
9. Beckmann, A.M., Davidson, M.S., Goodenough, S., and Wilce, P.A. 1997. Differential expression of Egr-1-like DNA-binding activities in the naive rat brain and after excitatory stimulation. J. Neurochem. 69: 2227-2237.
10. Bennett, T.L. 1973. The effects of centrally blocking hippocampal theta activity on learning and retention. Behav. Biol. 9: 541-552.
11. Bennett, T.L., Nunn Hebert, P., and Moss, D.E. 1973. Hippocampal theta activity and the attention component of discrimination learning. Behav. Biol. 8: 173-181.
12. Bliss, T.V. and Collingridge, G.L. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
13. Bliss, T.V.P. and Lømo, T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232: 331-356.
14. Bontempi, B., Laurent-Demir, C., Destrade, C., and Jaffard, R. 1999. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400: 671-675.
15. Bozon, B., Kelly, A., Josselyn, S.A., Silva, A.J., Davis, S., and Laroche, S. 2003. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B 358: 805-814.
16. Brown, B.B. 1968. Frequency and phase of hippocampal theta activity in the spontaneously behaving cat. Electroencephalogr. Clin. Neurophysiol. 24: 53-62.
17. Bryson, D. and Schacher, S. 1969. Behavioral analysis of mammalian sleep and learning. Perspect. Biol. Med. 13: 71-79.
18. Buzsaki, G., Chen, L.S., and Gage, F.H. 1990. Spatial organization of physiological activity in the hippocampal region: Relevance to memory formation. Prog. Brain Res. 83: 257-268.
19. Cantero, J.L., Atienza, M., Stickgold, R., Kahana, M.J., Madsen, J.R., and Kocsis, B. 2003. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23: 10897-10903.
20. Cermak, L. and Craik, F. 1979. Levels of processing in human memory. John Wiley & Sons, Indianapolis, IN.
21. Changelian, P.S., Feng, P., King, T.C., and Milbrandt, J. 1989. Structure of the NGFI-A gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor. Proc. Natl. Acad. Sci. 86: 377-381.
22. Christy, B. and Nathans, D. 1989. DNA binding site of the growth factor-inducible protein Zif268. Proc. Natl. Acad. Sci. 86: 8737-8741.
23. Cirelli, C. and Tononi, G. 2000a. Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J. Neurosci. 20: 9187-9194.
24. _. 2000b. Gene expression in the brain across the sleep-waking cycle. Brain Res. 885: 303-321.
25. Cole, A.J., Saffen, D.W., Baraban, J.M., and Worley, F.F. 1989. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340: 474-476.
26. Corkin, S., Amaral, D.G., Gonzalez, R.G., Johnson, K.A., and Hyman, B.T. 1997. H.M.'s medial temporal lobe lesion: Findings from magnetic resonance imaging. J. Neurosci. 17: 3964-3979.
27. Craik, F. and Lockhart, R. 1972. Levels of processing: A framework for memory research. J. Verb. Learn. Verb. Behav. 11: 671-684.
28. Datta, S. 2000. Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci. 20: 8607-8613.
29. Dave, A.S. and Margoliash, D. 2000. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: 812-816.
30. Deisseroth, K. and Tsien, R.W. 2002. Dynamic multiphosphorylation passwords for activity-dependent gene expression. Neuron 34: 179-182.
31. Dement, W.C. 1958. The occurrence of low voltage, fast, electroencephalogram patterns during behavioral sleep in the cat. Electroenceph. Clin. Neurophysiol. 10: 291-296.
32. Dement, W. and Kleitman, N. 1957a. Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencephalogr. Clin. Neurophysiol. Suppl 9: 673-690.
33. _. 1957b. The relation of eye movements during sleep to dream activity: An objective method for the study of dreaming. J. Exp. Psychol. 53: 339-346.
34. Destexhe, A. and Sejnowski, T.J. 2003. Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol. Rev. 83: 1401-1453.
35. Destexhe, A., Contreras, D., and Steriade, M. 1999. Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J. Neurosci. 19: 4595-4608.
36. Eichenbaum, H. 2000. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1: 41-50.
37. Elazar, Z. and Adey, W.R. 1967. Electroencephalographic correlates of learning in subcortical and cortical structures. Electroencephalogr. Clin. Neurophysiol. 23: 306-319.
38. Emberger, K.M. 2001. To sleep perchance to ski: The involuntary appearance of visual and kinesthetic imagery at sleep onset following play on the Alpine Racer II. Ph.D. thesis, Harvard University, Cambridge, MA.
39. Fenn, K.M., Nusbaum, H.C., and Margoliash, D. 2003. Consolidation during sleep of perceptual learning of spoken language. Nature 425: 614-616.
40. Fishbein, W. 1971. Disruptive effects of rapid eye movement sleep deprivation on long-term memory. Physiol. Behav. 6: 279-282.
41. Fishbein, W., Kastaniotis, C., and Chattman, D. 1974. Paradoxical sleep: Prolonged augmentation following learning. Brain Res. 79: 61-75.
42. Fowler, M.J., Sullivan, M.J., and Ekstrand, B.R. 1973. Sleep and memory. Science 179: 302-304.
43. Frank, M.G., Issa, N.P., and Stryker, M.P. 2001. Sleep enhances plasticity in the developing visual cortex. Neuron 30: 275-287.
44. Gerrard, J.L. 2002. øReactivation of hippocampal ensemble activity patterns in the aging rat: Insights into memory consolidation within the aged brainø Ph.D. thesis, University of Arizona, Tucson.
45. Giuditta, A., ed. 1985. A sequential hypothesis for the function of sleep. Fisher-Verlag, Stuttgart, Germany.
46. Giuditta, A., Ambrosini, M.V., Montagnese, P., Mandile, P., Cotugno, M., Zucconi, G.G., and Vescia, S. 1995. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69: 157-166.
47. Green, J.D. and Arduini, A.A. 1954. Hippocampal electrical activity in arousal. J. Neurophysiol. 17: 533-557.
48. Grimm, R. and Tischmeyer, W. 1997. Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining. Behav. Brain Res. 84: 109-116.
49. Gutwein, B.M., Shiromani, P.J., and Fishbein, W. 1980. Paradoxical sleep and memory: long-term disruptive effects of Anisomycin. Pharmacol. Biochem. Behav. 12: 377-384.
50. Haist, F., Bowden Gore, J., and Mao, H. 2001. Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat. Neurosci. 4: 1139-1145.
51. Harper, R.M. 1971. Frequency changes in hippocampal electrical activity during movement and tonic immobility. Physiol. Behav. 7: 55-58.
52. Hebb, D.O. 1942. The effects of early and late brain injury upon test scores, and the nature of normal adult intelligence. Proc. Am. Philos. Soc. 85: 275-292.
53. _. 1949. The organization of behavior: A neuropsychological theory. John Wiley & Sons, New York.
54. Hirase, H., Leinekugel, X., Czurko, A., Csicsvari, J., and Buzsaki, G. 2001. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proc. Natl. Acad. Sci. 98: 9386-9390.
55. Hoffman, K.L. and McNaughton, B. 2002. Coordinated reactivation of distributed memory traces in primate neocortex. Science 297: 2070-2073.
56. Izquierdo, I. and Medina, J.H. 1997. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn. Mem. 68: 285-316.
57. Jenkins, J.B. and Dallenbach, K.M. 1924. Oblivescence during sleep and waking. Am. J. Psychol. 35: 605-612.
58. Jones, M.W., Errington, M.L., French, P.J., Fine, A., Bliss, T.V., Garel, S., Charnay, P., Bozon, B., Laroche, S., and Davis, S. 2001. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4: 289-296.
59. Jouvet, M. 1967. The states of sleep. Sci. Am. 216: 62-68.
60. Jouvet, M., Michel, F., and Courjon, J. 1959. Sur un stade d'activité électrique cérébrale rapide au cours du sommeil physiologique. C.R. Soc. Biol. (Paris) 153: 1024-1028.
61. Kahana, M.J., Sekuler, R., Caplan, J.B., Kirschen, M., and Madsen, J.R. 1999. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399: 781-784.
62. Kami, A., Tanne, D., Rubenstein, B.S., Askenasy, J.J., and Sagi, D. 1994. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265: 679-682.
63. Kesner, R.P. and Novak, J.M. 1982. Serial position curve in rats: Role of the dorsal hippocampus. Science 218: 173-175.
64. Kim, J.J., Clark, R.E., and Thompson, R.F. 1995. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109: 195-203.
65. Kudrimoti, H.S., Barnes, C.A., and McNaughton, B.L. 1999. Reactivation of hippocampal cell assemblies: Effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19: 4090-4101.
66. Kuhn, T.S. 1962. The structure of scientific revolutions. University of Chicago Press, Chicago.
67. Lamprecht, R. and LeDoux, J. 2004. Structural plasticity and memory. Nat. Rev. Neurosci. 5: 45-54.
68. Landfield, P.W., McGaugh, J.L., and Tusa, R.J. 1972. Theta rhythm: A temporal correlate of memory storage processes in the rat. Science 7: 87-89.
69. Laureys, S., Peigneux, P., Perrin, F., and Maquet, P. 2002. Sleep and motor skill learning. Neuron 35: 5-7.
70. Lavenex, P. and Amaral, D.G. 2000. Hippocampal-neocortical interaction: A hierarchy of associativity. Hippocampus 10: 420-430.
71. Leconte, P. and Bloch, V. 1970. Déficit de la rétention d'un conditionnement après privation de sommeil paradoxal chez le rat. Comptes Rendus de l' Académie des Sciences (Paris) 271D: 226-229.
72. Leconte, P. and Hennevin, E. 1971. Augmentation de la durée de sommeil paradoxal consécutive à un apprentissage chez le rat. C.R. Acad. Sci. (Paris) 273: 86-88.
73. Lee, A.K. and Wilson, M.A. 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36: 1183-1194.
74. Lemaire, P., Vesque, C., Schmitt, J., Stunnenberg, H., Frank, R., and Charnay, P. 1990. The serum-inducible mouse gene Krox-24 encodes a sequence-specific transcriptional activator. Mol. Cell. Biol. 10: 3456-3467.
75. Linden, E.R., Bern, D., and Fishbein, W. 1975. Retrograde amnesia: Prolonging the fixation phase of memory consolidation by paradoxical sleep deprivation. Physiol. Behav. 14: 409-412.
76. Lisman, J., Schulman, H., and Cline, H. 2002. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3: 175-190.
77. Lonze, B.E. and Ginty, D.D. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35: 605-623.
78. Lorente de Nó, R. 1938. Analysis of the activity of the chains of internuncial neurons. J. Neurophysiol. 1: 207-244.
79. Louie, K. and Wilson, M.A. 2001. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29: 145-156.
80. Lucero, M.A. 1970. Lengthening of REM sleep duration consecutive to learning in the rat. Brain Res. 20: 319-322.
81. Maquet, P., Laureys, S., Peigneux, P., Fuchs, S., Petiau, C., Phillips, C., Aerts, J., Del Fiore, G., Degueldre, C., Meulemans, T., et al. 2000. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 3: 831-836.
82. Maquet, P., Schwartz, S., Passingham, R., and Frith, C. 2003. Sleep-related consolidation of a visuomotor skill: Brain mechanisms as assessed by functional magnetic resonance imaging. J. Neurosci. 23: 1432-1440.
83. Marks, G.A., Shaffery, J.P., Oksenberg, A., Speciale, S.G., and Roffwarg, H.P. 1995. A functional role for REM sleep in brain maturation. Behav. Brain Res. 69: 1-11.
84. Marr, D. 1971. Simple memory: a theory for archicortex. Phil. Trans. R. Soc. B262: 23-81.
85. Massimini, M. and Amzica, F. 2001. Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. J. Neurophysiol. 85: 1346-1350.
86. 2+ of NMDA responses in spinal cord neurones. Nature 309: 261-263.
87. Mayr, B. and Montminy, M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell. Biol. 2: 599-609.
88. McCarley, R.W. and Hobson, J.A. 1970. Cortical unit activity in desynchronized sleep. Science 167: 901-903.
89. McClelland, J.L., McNaughton, B.L., and O'Reilly, R.C. 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.
90. Mednick, S.C., Nakayama, K., and Stickgold, R. 2003. Sleep-dependent learning: A nap is as good as a night. Nat Neurosci. 6: 697-698.
91. Mello, C.V., Vicario, D.S., and Clayton, D.F. 1992. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. 89: 6818-6822.
92. Melton, A.W. and Irwin, J.M. 1940. The influence of degree of interpolated learning on retroactive inhibition and the overt transfer of specific responses. Am. J. Psychol. 53: 173-203.
93. Milbrandt, J. 1987. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238: 797-799.
94. Mishkin, M. 1978. Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273: 297-298.
95. Morgan, J.I. and Curran, T. 1989. Stimulus-transcription coupling in neurons: Role of cellular immediate-early genes. Trends Neurosci. 12: 459-462.
96. Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J., and Buzsaki, G. 1999. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19: 9497-9507.
97. Nikolaev, E., Kaminska, B., Tischmeyer, W., Matthies, H., and Kaczmarek, L. 1992. Induction of expression of genes encoding transcription factors in the rat brain elicited by behavioral training. Brain Res. Bull. 28: 479-484.
98. Nowak, L., Bregestovski, P., Ascher, P., Herbet, A., and Prochiantz, A. 1984. Magnesium gates glutamate-activated channels in mouse central neurons. Nature (Lond) 307: 462-465.
99. Pavlides, C. and Ribeiro, S. 2003. Recent evidence of memory processing in sleep. In Sleep and brain plasticity (eds. P. Maquet et al.), pp. 327-362. Oxford University Press, Oxford, UK.
100. Pavlides, C. and 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.
101. Pearlman, C.A. 1969. Effect of rapid eye movement (dreaming) sleep deprivation on retention of avoidance learning in rats. Rep. U.S. Naval Submarine Med. Center 22: 1-4.
102. _. 1973. REM sleep deprivation impairs latent extinction in rats. Physiol. Behav. 11: 233-237.
103. Pearlman, C. and Becker, M. 1974. REM sleep deprivation impairs bar-press acquisition in rats. Physiol. Behav. 13: 813-817.
104. Peigneux, P., Laureys, S., Fuchs, S., Destrebecqz, A., Collette, F., Delbeuck, X., Phillips, C., Aerts, J., Del Fiore, G., Degueldre, C., et al. 2003. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage 20: 125-134.
105. Pennartz, C.M., Lee, E., Verheul, J., Lipa, P., Barnes, C.A., and McNaughton, B.L. 2004. The ventral striatum in off-line processing: Ensemble reactivation during sleep and modulation by hippocampal ripples. J. Neurosci. 24: 6446-6456.
106. Petersohn, D., Schoch, S., Brinkmann, D.R., and Thiel, G. 1995. The human synapsin II gene promoter: Possible role for the transcription factor zif268/egr-1, polyoma enhancer activator 3, and AP2. J. Biol. Chem. 270: 24361-24369.
107. Poe, G.R., Nitz, D.A., McNaughton, B.L., and Barnes, C.A. 2000. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855:176-180.
108. Pompeiano, M., Cirelli, C., and Tononi, G. 1994. Immediate-early genes in spontaneous wakefulness and sleep: Expression of c-fos and NGIF-A mRNA protein. J. Sleep Res. 3: 80-96.
109. Pompeiano, M., Cirelli, C., Arrighi, P., and Tononi, G. 1995. c-Fos expression during wakefulness and sleep. Neurophysiol. Clin. 25: 329-341.
110. Pompeiano, M., Cirelli, C., Ronca-Testoni, S., and Tononi, G. 1997. NGFI-A expression in the rat brain after sleep deprivation. Brain Res. Mol. Brain Res. 46: 143-153.
111. Qin, Y.L., McNaughton, B.L., Skaggs, W.E., and Barnes, C.A. 1997. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos. Trans. R. Soc. Lond. B 352: 1525-1533.
112. Rechtschaffen, A. and Kales, A. 1968. A manual of standardized terminology, techniques and scoring system for sleep stages in human subjects. National Institutes of Health, Washington, DC.
113. Ribeiro, S., Goyal, V., Mello, C.V., and Pavlides, C. 1999. Brain gene expression during REM sleep depends on prior waking experience. Learn. Mem. 6: 500-508.
114. Ribeiro, S., Mello, C.V., Velho, T., Gardner, T.J., Jarvis, E.D., and Pavlides, C. 2002. Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J. Neurosci. 22: 10914-10923.
115. Ribeiro, S., Gervasoni, D., Soares, E.S., Zhou, Y., Lin, S.C., Pantoja, P., Lavine, M., and Nicolelis, M. 2004. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol. 2: 126-137.
116. Roffwarg, H.P., Dement, W.C., Muzio, J.N., and Fisher, C. 1962. Dream imagery: Relationship to rapid eye movements of sleep. Arch. Gen. Psychiatry 7: 235-258.
117. Rosahl, T.W., Spillane, D., Missler, M., Herz, J., Selig, D.K., Wolff, J.R., Hammer, R.E., Malenka, R.C., and Sudhof, T.C. 1995. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375: 488-493.
118. Sainsbury, R.S. 1970. Hippocampal activity during natural behavior in the guinea pig. Physiol. Behav. 5: 317-324.
119. Scoville, W.B. and Milner, B. 1957. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psych. 20: 11-21.
120. Sederberg, P.E., Kahana, M.J., Howard, M.W., Donner, E.J., and Madsen, J.R. 2003. Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 23: 10809-10814.
121. Sejnowski, T.J. and Destexhe, A. 2000. Why do we sleep? Brain Res. 886: 208-223.
122. Shaffery, J.P., Oksenberg, A., Marks, G.A., Speciale, S.G., Mihailoff, G., and Roffwarg, H.P. 1998. REM sleep deprivation in monocularly occluded kittens reduces the size of cells in LGN monocular segment. Sleep 21: 837-845.
123. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252: 1427-1430.
124. Shiromani, P., Gutwein, B.M., and Fishbein, W. 1979. Development of learning and memory in mice after brief paradoxical sleep deprivation. Physiol Behav. 22: 971-978.
125. Siegel, J.M. 2001. The REM sleep-memory consolidation hypothesis. Science 294: 1058-1063.
126. Skaggs, W.E. and McNaughton, B.L. 1996. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271: 1870-1873.
127. Smith, C. 1995. Sleep states and memory processes. Behav. Brain Res. 69: 137-145.
128. _. 2001. Sleep states and memory processes in humans: Procedural versus declarative memory systems. Sleep Med. Rev. 5: 491-506.
129. Smith, C. and Butler, S. 1982. Paradoxical sleep at selective times following training is necessary for learning. Physiol. Behav. 29: 469-473.
130. Smith, C. and Kelly, G. 1988. Paradoxical sleep deprivation applied 2 days after end of training retards learning. Physiol. Behav. 43: 213-216.
131. Smith, C. and Lapp, L. 1986. Prolonged increases in both PS and number of REMS following a shuttle avoidance task. Physiol. Behav. 36: 1053-1057.
132. _. 1991. Increases in number of REMS and REM density in humans following an intensive learning period. Sleep 14: 325-330.
133. Smith, C. and MacNeill, C. 1993. A paradoxical sleep-dependent window for memory 53-56-H after the end of avoidance training. Psychobiology 21: 109-112.
134. Smith, C. and Rose, G.M. 1996. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol. Behav. 59: 93-97.
135. Smith, C. and Wong, P.T.P. 1991. Paradoxical sleep increases predict successful learning in a complex operant task. Behav. Neurosci. 105: 282-288.
136. Smith, C., Kitahama, K., Valatx, J.L., and Jouvet, M. 1974. Increased paradoxical sleep in mice during acquisition of a shock avoidance task. Brain Res. 77: 221-230.
137. Smith, C., Young, J., and Young, W. 1980. Prolonged increases in paradoxical sleep during and after avoidance-task acquisition. Sleep 3: 67-68.
138. Squire, L.R. 1992. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99: 195-231.
139. Steriade, M. and McCarley, R.W. 1990. Brainstem control of wakefulness and sleep. Plenum Press, New York.
140. Steriade, M., McCormick, D.A., and Sejnowski, T.J. 1993. Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.
141. Stewart, M. and Fox, S.E. 1991. Hippocampal theta activity in monkeys. Brain Res. 538: 59-63.
142. Stickgold, R. 1998. Sleep: Off-line memory reprocessing. Trends Cogn. Sci. 2: 484-492.
143. _. 2003. Memory, cognition, and dreams. In Sleep and brain plasticity (eds. P. Maquet et al.), pp. 17-39. Oxford University Press, Oxford, UK.
144. Stickgold, R., James, L., and Hobson, J.A. 2000a. Visual discrimination learning requires sleep after training. Nat. Neurosci. 3: 1237-1238.
145. Stickgold, R., Whidbee, D., Schirmer, B., Patel, V., and Hobson, J.A. 2000b. Visual discrimination task improvement: A multi-step process occurring during sleep. J. Cogn. Neurosci. 12: 246-254.
146. Thiel, G., Schoch, S., and Petersohn, D. 1994. Regulation of synapsin I gene expression by the zinc finger transcription factor zif268/egr-1. J. Biol. Chem. 269: 15294-15301.
147. Thompson, R.F. and Kim, J.J. 1996. Memory systems in the brain and localization of a memory. Proc. Natl. Acad. Sci. 93: 13438-13444.
148. Timo-Iaria, C., Negrao, N., Schmidek, W.R., Hoshino, K., Lobato de Menezes, C.E., and Lerne da Rocha, T. 1970. Phases and states of sleep in the rat. Physiol. Behav. 5: 1057-1062.
149. Tononi, G. and Cirelli, C. 2001. Some considerations on sleep and neural plasticity. Arch. Ital. Biol. 139: 221-241.
150. _. 2003. Sleep and synaptic homeostasis: A hypothesis. Brain Res. Bull. 62: 143-150.
151. Tradardi, V. 1966. Sleep in the pigeon. Arch. Ital. Biol. 104: 516-521.
152. Vanderwolf, C.H. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. Clin. Neurophysiol. 26: 407-418.
153. Vertes, R.P. and Eastman, K.E. 2000. The case against memory consolidation in REM sleep. Behav. Brain Sci. 23: 867-876.
154. Wagner, U., Gais, S., Haider, H., Verleger, R., and Born, J. 2004. Sleep inspires insight. Nature 427: 352-355.
155. Walker, M.P., Brakefield, T., Morgan, A., Hobson, J.A., and Stickgold, R. 2002. Practice with sleep makes perfect: Sleep-dependent motor skill learning. Neuron 35: 205-211.
156. Walker, M.P., Brakefield, T., Seidman, J., Morgan, A., Hobson, J.A., and Stickgold, R. 2003. Sleep and the time course of motor skill learning. Learn. Mem. 10: 275-284.
157. Wallace, C.S., Withers, G.S., Weiler, I.J., George, J.M., Clayton, D.F., and Greenough, W.T. 1995. Correspondence between sites of NGFI-A induction and sites of morphological plasticity following exposure to environmental complexity. Brain Res. Mol. Brain Res. 32: 211-220.
158. Wang, X.J. 2001. Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci. 24: 455-463.
159. Wetzel, W., Wagner, T., and Balschun, D. 2003. REM sleep enhancement induced by different procedures improves memory retention in rats. Eur. J. Neurol. 18: 2611-2617.
160. Wilson, M.A. and McNaughton, B.L. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265: 676-679.
161. Winocur, G., McDonald, R.M., and Moscovitch, M. 2001. Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus 11: 18-26.
162. Winson, J. 1972. Interspecies differences in the occurrence of theta. Behav. Biol. 7: 479-487.
163. _. 1974. Patterns of hippocampal theta rhythm in the freely moving rat. Electroenceph. Clin. Neurophysiol. 36: 291-301.
164. _. 1978. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201: 160-163.
165. _. 1985. Brain and psyche. Anchor Press, New York.
166. _. 1990. The meaning of dreams. Sci. Am. 263: 86-96.
167. _. 1993. The biology and function of rapid eye movement sleep. Curr. Opin. Neurobiol. 3: 243-248.
168. Wisden, W., Errington, M.L., Williams, S., Dunnett, S.B., Waters, C., Hitchcock, D., Evan, G., Bliss, T.V., and Hunt, S.P. 1990. Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4: 603-614.
169. Worley, P.P., Bhat, R.V., Baraban, J.M., Erickson, C.A., McNaughton, B.L., and Barnes, C.A. 1993. Thresholds for synaptic activation of transcription factors in hippocampus: Correlation with long-term enhancement. J. Neurosci. 13: 4776-4786.
170. Zola-Morgan, S.M. and Squire, L.R. 1990. The primate hippocampal formation: Evidence for a time-limited role in memory storage. Science 250: 288-290.