Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory

Neurobiology of Learning and Memory

Volumn 109, Issue , 2014, Pages 122-130

  Prince, Toni Moi ^a   Wimmer, Mathieu ^a   Choi, Jennifer ^a   Havekes, Robbert ^a   Aton, Sara ^b   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Hippocampus; Long term potentiation; Sleep loss; Spatial memory

Indexed keywords

3 HOUR TIME WINDOW; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NONREM SLEEP; OBJECT PLACE RECOGNITION; REM SLEEP; SLEEP DEPRIVATION; SPATIAL MEMORY; SPATIAL MEMORY TEST; TIME;

HIPPOCAMPUS; LONG-TERM POTENTIATION; SLEEP LOSS; SPATIAL MEMORY;

ANIMALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MEMORY, LONG-TERM; MICE; MICE, INBRED C57BL; RECOGNITION (PSYCHOLOGY); SLEEP DEPRIVATION; SPACE PERCEPTION; TIME FACTORS;

EID: 84893066330     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.11.021     Document Type: Article

References (70)

1. Abel T., Havekes R., Saletin J.M., Walker M.P. Sleep, plasticity and memory from molecules to whole-brain networks. Current Biology: CB 2013, 23(17). R774-88.
2. Abel T., Lattal K.M. Molecular mechanisms of memory acquisition, consolidation and retrieval. Current Opinion in Neurobiology 2001, 11(2):180-187.
3. Benca R.M., Obermeyer W.H., Thisted R.A., Gillin J.C. Sleep and psychiatric disorders. A meta-analysis. Archives of General Psychiatry 1992, 49(8):651-668. discussion 669-70.
4. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proceedings of the National Academy of Sciences 1997, 94(13):7041-7046.
5. Bernabeu R., Cammarota M., Izquierdo I., Medina J.H. Involvement of hippocampal AMPA glutamate receptor changes and the cAMP/protein kinase A/CREB-P signalling pathway in memory consolidation of an avoidance task in rats. Brazilian Journal of Medical and Biological Research 1997, 30(8):961-965.
6. Binder S., Baier P.C., Mölle M., Inostroza M., Born J., Marshall L. Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats. Neurobiology of Learning and Memory 2012, 97(2):213-219.
7. Born J., Feld G.B. Sleep to upscale, sleep to downscale: Balancing homeostasis and plasticity. Neuron 2012, 75(6):933-935.
8. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E.R. Different training procedures for contextual memory in mice can recruit either one or two critical periods for memory consolidation that require protein synthesis and PKA. Learning & Memory 1998, 5:365-374.
9. Bussey T.J., Duck J., Muir J.L., Aggleton J.P. Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behavioural Brain Research 2000, 111(1-2):187-202.
10. Campbell I.G., Guinan M.J., Horowitz J.M. Sleep deprivation impairs long-term potentiation in rat hippocampal slices. Journal of Neurophysiology 2002, 88(2):1073-1076.
11. Chauvette S., Seigneur J., Timofeev I. Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 2012, 75(6):1105-1113.
12. Chee M.W.L., Choo W.C. Functional imaging of working memory after 24h of total sleep deprivation. The Journal of Neuroscience 2004, 24(19):4560-4567.
13. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee C., et al. Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell 1999, 98(4):437-451.
14. Clarke J.R., Cammarota M., Gruart A., Izquierdo I., Delgado-García J.M. Plastic modifications induced by object recognition memory processing. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(6):2652-2657.
15. Dong Z., Gong B., Li H., Bai Y., Wu X., Huang Y., et al. Mechanisms of hippocampal long-term depression are required for memory enhancement by novelty exploration. The Journal of Neuroscience 2012, 32(35):11980-11990.
16. Durmer J.S., Dinges D.F. Neurocognitive consequences of sleep deprivation. Seminars in Neurology 2005, 25(1):117-129.
17. Eckel-Mahan K.L., Phan T., Han S., Wang H., Chan G.C.K., Scheiner Z.S., et al. Circadian oscillation of hippocampal MAPK activity and cAmp: Implications for memory persistence. Nature Neuroscience 2008, 11(9):1074-1082.
18. Florian C., Vecsey C.G., Halassa M.M., Haydon P.G., Abel T. Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. Journal of Neuroscience 2011, 31(19):6956-6962.
19. Franken P., Lopez-Molina L., Marcacci L., Schibler U., Tafti M. The transcription factor DBP affects circadian sleep consolidation and rhythmic EEG activity. Journal of Neuroscience 2000, 20(2):617-625.
20. Graves L.A., Heller E.A., Pack A.I., Abel T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learning & Memory 2003, 10(3):168-176.
21. Grosmark A.D., Mizuseki K., Pastalkova E., Diba K., Buzsáki G. REM sleep reorganizes hippocampal excitability. Neuron 2012, 75(6):1001-1007.
22. Hagewoud R., Havekes R., Novati A., Keijser J.N., Van der Zee E.A., Meerlo P. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. Journal of Sleep Research 2010, 19(2):280-288.
23. Hagewoud R., Havekes R., Tiba P., Novati A., Hogenelst K., Weinreder P., et al. Coping with sleep deprivation: Shifts in regional brain activity and learning strategy. Sleep 2010, 33(11):1465-1473.
24. Hagewoud R., Whitcomb S.N., Heeringa A.N., Havekes R., Koolhaas J.M., Meerlo P. A time for learning and a time for sleep: The effect of sleep deprivation on contextual fear conditioning at different times of the day. Sleep 2010, 33(10):1315-1322.
25. Harrison Y., Horne J. The impact of sleep deprivation on decision making: A review. Journal of Experimental Psychology: Applied 2000, 6(3):236-249.
26. Havekes R., Canton D.A., Park A.J., Huang T., Nie T., Day J.P., et al. Gravin orchestrates protein kinase A and β2-adrenergic receptor signaling critical for synaptic plasticity and memory. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2012, 32(50):18137-18149.
27. Havekes R., Vecsey C.G., Abel T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cellular Signalling 2012, 24(6):1251-1260.
28. Hellman K., Abel T. Fear conditioning increases NREM sleep. Behavioral Neuroscience 2007, 121(2):310-323.
29. Hellman K., Hernandez P., Park A., Abel T. Genetic evidence for a role for protein kinase A in the maintenance of sleep and thalamocortical oscillations. Sleep 2010, 33(1):19-28.
30. Huber R., Deboer T., Tobler I. Topography of EEG dynamics after sleep deprivation in mice. Journal of Neurophysiology 2000, 84(4):1888-1893.
31. Inostroza M., Binder S., Born J. Sleep-dependency of episodic-like memory consolidation in rats. Behavioural Brain Research 2013, 237:15-22.
32. Ishikawa A., Kanayama Y., Matsumura H., Tsuchimochi H., Ishida Y., Nakamura S. Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus. The European Journal of Neuroscience 2006, 24(1):243-248.
33. Kemp A., Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(21):8192-8197.
34. Kopp C., Longordo F., Nicholson J.R., Lüthi A. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. The Journal of Neuroscience 2006, 26(48):12456-12465.
35. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: Effects of behavioral state, experience, and EEG dynamics. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 1999, 19(10):4090-4101.
36. Ledoux L., Sastre J.P., Buda C., Luppi P.H., Jouvet M. Alterations in c-fos expression after different experimental procedures of sleep deprivation in the cat. Brain Research 1996, 735(1):108-118.
37. Li S., Cullen W.K., Anwyl R., Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nature Neuroscience 2003, 6(5):526-531.
38. Luo J., Phan T.X., Yang Y., Garelick M.G., Storm D.R. Increases in cAMP, MAPK activity, and CREB phosphorylation during REM sleep: Implications for REM sleep and memory consolidation. Journal of Neuroscience 2013, 33(15):6460-6468.
39. McDermott C.M., LaHoste G.J., Chen C., Musto A., Bazan N.G., Magee J.C. Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. The Journal of Neuroscience 2003, 23(29):9687-9695.
40. Meerlo P., De Bruin E.A, Strijkstra A.M., Daan S. A social conflict increases EEG slow-wave activity during subsequent sleep. Physiology & Behavior 2001, 73(3):331-335.
41. Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002). Hippocampal damage and exploratory preferences in rats: Memory for objects places and contexts. Learning & Memory 9(2), (pp. 49-57) (Cold Spring Harbor, N.Y.).
42. Oliveira A.M.M., Hawk J.D., Abel T., Havekes R. Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learning & Memory 2010, 215:155-160.
43. Palchykova S., Winsky-Sommerer R., Meerlo P., Dürr R., Tobler I. Sleep deprivation impairs object recognition in mice. Neurobiology of Learning and Memory 2006, 85(3):263-271.
44. Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. Journal of Cognitive Neuroscience 1997, 9(4):534-547.
45. Prince T.-M., Abel T. The impact of sleep loss on hippocampal function. Learning & Memory 2013, 20(10):558-569.
46. Ramadan W., Eschenko O., Sara S.J. Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS One 2009, 4(8):e6697.
47. Rolls A., Colas D., Adamantidis A., Carter M., Lanre-Amos T., Heller H.C., et al. Optogenetic disruption of sleep continuity impairs memory consolidation. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(32):13305-13310.
48. Romcy-Pereira R., Pavlides C. Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. The European Journal of Neuroscience 2004, 20(12):3453-3462.
49. Shrager Y., Bayley P.J., Bontempi B., Hopkins R.O., Squire L.R. Spatial memory and the human hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(8):2961-2966.
50. Smith C. Sleep states and learning: A review of the animal literature. Neuroscience and Biobehavioral Reviews 1985, 9(2):157-168.
51. Smith C., Rose G.M. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiology & Behavior 1996, 59(1):93-97.
52. Smith C., Rose G.M. Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze. Behavioral Neuroscience 1997, 111(6):1197-1204.
53. Spiegel K., Leproult R., Van Cauter E. Early report impact of sleep debt on metabolic and endocrine function 1999, 354:1435-1439.
54. Stern W.C. Acquisition impairments following rapid eye movement sleep deprivation in rats. Physiology & Behavior 1971, 7(3):345-352.
55. Stickgold R., Whidbee D., Schirmer B., Patel V., Hobson J.a Visual discrimination task improvement: A multi-step process occurring during sleep. Journal of Cognitive Neuroscience 2000, 12(2):246-254.
56. Tafti M., Petit B., Chollet D., Neidhart E., De Bilbao F., Kiss J.Z., et al. Deficiency in short-chain fatty acid beta-oxidation affects theta oscillations during sleep. Nature Genetics 2003, 34(3):320-325.
57. Tang X., Liu X., Yang L., Sanford L.D. Rat strain differences in sleep after acute mild stressors and short-term sleep loss. Behavioural Brain Research 2005, 160(1):60-71.
58. Tang X., Xiao J., Liu X., Sanford L.D. Strain differences in the influence of open field exposure on sleep in mice. Behavioural Brain Research 2004, 154(1):137-147.
59. Tang X., Yang L., Sanford L.D. Interactions between brief restraint, novelty and footshock stress on subsequent sleep and EEG power in rats. Brain Research 2007, 1142:110-118.
60. Van der Helm E., Gujar N., Nishida M., Walker M.P. Sleep-dependent facilitation of episodic memory details. PloS One 2011, 6(11):e27421.
61. Van Der Werf Y.D., Altena E., Schoonheim M.M., Sanz-Arigita E.J., Vis J.C., De Rijke W., et al. Sleep benefits subsequent hippocampal functioning. Nature Neuroscience 2009, 12(2):122-123.
62. Veasey S.C., Valladares O., Fenik P., Kapfhamer D., Sanford L., Benington J., et al. An automated system for recording and analysis of sleep in mice. Sleep 2000, 23(8):1025-1040.
63. Vecsey C.G., Baillie G.S., Jaganath D., Havekes R., Daniels A., Wimmer M., et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 2009, 461(7267):1122-1125.
64. Vecsey C.G., Peixoto L., Choi J.H.K., Wimmer M., Jaganath D., Hernandez P.J., et al. Genomic analysis of sleep deprivation reveals translational regulation in the hippocampus. Physiological Genomics 2012, 44(20):981-991.
65. Vecsey C.G., Wimmer M.E.J., Havekes R., Park A.J., Perron I.J., Meerlo P., et al. Daily acclimation handling does not affect hippocampal long-term potentiation or cause chronic sleep deprivation in mice. Sleep 2013, 36(4):601-607.
66. Wamsley E.J., Tucker M.A., Payne J.D., Stickgold R. A brief nap is beneficial for human route-learning: The role of navigation experience and EEG spectral power. Learning & Memory 2010, 17(7):332-336.
67. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: Heterogeneity of function within the temporal lobe. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2004, 24(26):5901-5908.
68. Winters B.D., Saksida L.M., Bussey T.J. Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval. Neuroscience and Biobehavioral Reviews 2008, 32(5):1055-1070.
69. Xu L., Anwyl R., Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 1998, 394(6696):891-894.
70. Youngblood B.D., Zhou J., Smagin G.N., Ryan D.H., Harris R.B. Sleep deprivation by the "flower pot" technique and spatial reference memory. Physiology & Behavior 1997, 61(2):249-256.