Animal studies on the role of sleep in memory: From behavioral performance to molecular mechanisms

Current Topics in Behavioral Neurosciences

Volumn 25, Issue , 2015, Pages 183-206

  Havekes, Robbert ^a   Meerlo, Peter ^b   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

CAMP; CREB; Hippocampus; Learning; Long term potentiation; LTP; Memory; MTOR; PDE; Sleep deprivation; Sleep disturbance

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; OCTOPAMINE; PHOSPHODIESTERASE; ROLIPRAM;

ARTICLE; BEHAVIOR; COGNITIVE DEFECT; DOWN REGULATION; DROSOPHILA; ELECTRIC SHOCK; ELECTROENCEPHALOGRAM; ELECTROMYOGRAM; FEAR; HUMAN; MEMORY CONSOLIDATION; MORRIS WATER MAZE TEST; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SHORT TERM MEMORY; SLEEP; SLEEP DEPRIVATION; ANIMAL; ANIMAL BEHAVIOR; LONG TERM POTENTIATION; MEMORY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; LONG-TERM POTENTIATION; MEMORY; SLEEP; SLEEP DEPRIVATION;

EID: 84929621256     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2015_369     Document Type: Article

References (103)

1. Abel T, Lattal KM (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11:180–187
2. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, 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
3. Abel T, Havekes R, Saletin JM, Walker MP (2013) Sleep, plasticity and memory from molecules to whole-brain networks. Curr Biol 23:R774–R788
4. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA (2010) Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus. Eur J Neurosci 31:1368–1376
5. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA (2011) Sleep deprivation prevents stimulationinduced increases of levels of P-CREB and BDNF: protection by caffeine. Mol Cell Neurosci 46:742–751
6. Anagnostaras SG, Gale GD, Fanselow MS (2001) Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8–17
7. Ballard P (1913) Oblivescence and reminiscence. Br J Psychol Monograph Suppl 1:1–82
8. Basheer R, Strecker RE, Thakkar MM, McCarley RW (2004) Adenosine and sleep-wake regulation. Prog Neurobiol 73:379–396
9. Bergmann BM, Kushida CA, Everson CA, Gilliland MA, Obermeyer W, Rechtschaffen A (1989) Sleep deprivation in the rat: II. Methodology. Sleep 12:5–12
10. Bjorness TE, Riley BT, Tysor MK, Poe GR (2005) REM restriction persistently alters strategy used to solve a spatial task. Learn Mem 12:352–359
11. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER (1998) Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5:365–374
12. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51–61
13. Chen C, Hardy M, Zhang J, LaHoste GJ, Bazan NG (2006) Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments. Biochem Biophys Res Commun 340:435–440
14. Cirelli C, Tononi G (2000) Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J Neurosci 20:9187–9194
15. Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41:35–43
16. Cirelli C, Faraguna U, Tononi G (2006) Changes in brain gene expression after long-term sleep deprivation. J Neurochem 98:1632–1645
17. Coenen AM, van Luijtelaar EL (1985) Stress induced by three procedures of deprivation of paradoxical sleep. Physiol Behav 35:501–504
18. Cohen SJ, Munchow AH, Rios LM, Zhang G, Asgeirsdottir HN, Stackman RW Jr (2013) The rodent hippocampus is essential for nonspatial object memory. Curr Biol 23:1685–1690
19. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiationdependent gene expression in the dentate gyrus in vivo. J Neurosci 20:4563–4572
20. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86
21. Ebbinghaus H (1885) Über das Gedachtnis. Untersuchungen zur experimentellen Psychologie. Duncker & Humblot, Leipzig
22. Eckel-Mahan KL, Phan T, Han S, Wang H, Chan GC, Scheiner ZS, Storm DR (2008) Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat Neurosci 11:1074–1082
23. Esteban JA, Shi S, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136–143
24. Etkin A, Alarcon JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, Kandel ER (2006) A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron 50:127–143
25. Fernandes-Santos L, Patti CL, Zanin KA, Fernandes HA, Tufik S, Andersen ML, Frussa-Filho R (2012) Sleep deprivation impairs emotional memory retrieval in mice: influence of sex. Prog Neuropsychopharmacol Biol Psychiatry 38:216–222
26. Florian C, Vecsey CG, Halassa MM, Haydon PG, Abel T (2011) Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. J Neurosci 31:6956–6962
27. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119–130
28. Graves LA, Heller EA, Pack AI, Abel T (2003) Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem 10:168–176
29. Guan Z, Peng X, Fang J (2004) Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res 1018:38–47
30. Guzman-Marin R, Suntsova N, Bashir T, Nienhuis R, Szymusiak R, McGinty D (2008) Rapid eye movement sleep deprivation contributes to reduction of neurogenesis in the hippocampal dentate gyrus of the adult rat. Sleep 31:167–175
31. Guzmán-Marín R, Ying Z, Suntsova N, Methippara M, Bashir T, Szymusiak R, Gomez-Pinilla F, McGinty D (2006) Suppression of hippocampal plasticity-related gene expression by sleep deprivation in rats. J Physiol 575:807–819
32. Hagewoud R, Whitcomb SN, Heeringa AN, Havekes R, Koolhaas JM, Meerlo P (2010a) 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 33:1315–1322
33. Hagewoud R, Havekes R, Tiba PA, Novati A, Hogenelst K, Weinreder P, Van der Zee EA, Meerlo P (2010b) Coping with sleep deprivation: shifts in regional brain activity and learning strategy. Sleep 33:1465–1473
34. Hagewoud R, Havekes R, Novati A, Keijser JN, Van de Zee EA, Meerlo P (2010c) Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J Sleep Res 19:280–288
35. Hagewoud R, Bultsma LJ, Barf RP, Koolhaas JM, Meerlo P (2011) Sleep deprivation impairs contextual fear conditioning and attenuates subsequent behavioural, endocrine and neuronal responses. J Sleep Res 20:259–266
36. Hairston IS, Little MT, Scanlon MD, Barakat MT, Palmer TD, Sapolsky RM, Heller HC (2005) Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 94:4224–4233
37. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61:213–219
38. Hartley D (1801) Observations on man, his frame, his deity, and his expectations. Scholars Facsimile & Reprint, Gainesville
39. Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37:877–888
40. Havekes R, Vecsey CG, Abel T (2012) The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell Signal 24:1251–1260
41. Havekes R, Bruinenberg VM, Tudor JC, Ferri SL, Baumann A, Meerlo P, Abel T (2014) Transiently Increasing cAMP levels selectively in hippocampal excitatory neurons during sleep deprivation prevents memory deficits caused by sleep loss. J Neurosci 34:15715–15721
42. Houslay MD (2009) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35:91–100
43. Houslay MD, Adams DR (2003) PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370:1–18
44. Huston JP, Haas HL, Boix F, Pfister M, Decking U, Schrader J, Schwarting RK (1996) Extracellular adenosine levels in neostriatum and hippocampus during rest and activity periods of rats. Neuroscience 73:99–107
45. Igaz LM, Vianna MR, Medina JH, Izquierdo I (2002) Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. J Neurosci 22:6781–6789
46. Impey S, Obrietan K, Storm DR (1999) Making new connections: role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 23:11–14
47. Isiegas C, Park A, Kandel ER, Abel T, Lattal KM (2006) Transgenic inhibition of neuronal protein kinase A activity facilitates fear extinction. J Neurosci 26:12700–12707
48. Jenkins JG, Dallenbach KM (1924) Obliviscence during sleep and waking. Am J Psychol 35:605–612
49. Kandel ER (2004) The molecular biology of memory storage: a dialog between genes and synapses. Biosci Rep 24:475–522
50. Kopp C, Longordo F, Nicholson JR, Luthi A (2006) Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J Neurosci 26:12456–12465
51. LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23:155–184
52. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955–959
53. Leenaars CH, Dematteis M, Joosten RN, Eggels L, Sandberg H, Schirris M, Feenstra MG, Van Someren EJ (2011) A new automated method for rat sleep deprivation with minimal confounding effects on corticosterone and locomotor activity. J Neurosci Methods 196:107–117
54. Li S, Tian Y, Ding Y, Jin X, Yan C, Shen X (2009) The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats. Learn Behav 37:246–253
55. Longordo F, Kopp C, Luthi A (2009a) Consequences of sleep deprivation on neurotransmitter receptor expression and function. Eur J Neurosci 29:1810–1819
56. Longordo F, Kopp C, Mishina M, Lujan R, Luthi A (2009b) NR2A at CA1 synapses is obligatory for the susceptibility of hippocampal plasticity to sleep loss. J Neurosci 29:9026–9041
57. Luo J, Phan TX, Yang Y, Garelick MG, Storm DR (2013) Increases in cAMP, MAPK activity, and CREB phosphorylation during REM sleep: implications for REM sleep and memory consolidation. J Neurosci 33:6460–6468
58. Mackiewicz M, Shockley KR, Romer MA, Galante RJ, Zimmerman JE, Naidoo N, Baldwin DA, Jensen ST, Churchill GA, Pack AI (2007) Macromolecule biosynthesis: a key function of sleep. Physiol Genomics 31:441–457
59. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931
60. Mazzucchelli C, Brambilla R (2000) Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell Mol Life Sci 57:604–611
61. McDermott CM, LaHoste GJ, Chen C, Musto A, Bazan NG, Magee JC (2003) Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J Neurosci 23:9687–9695
62. McDermott CM, Hardy MN, Bazan NG, Magee JC (2006) Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J Physiol 570:553–565
63. Mendelson WB, Guthrie RD, Frederick G, Wyatt RJ (1974) The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol Biochem Behav 2:5523–5556
64. Morris RG, Garrud P, Rawlins JN, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683
65. Novati A, Hulshof HJ, Koolhaas JM, Lucassen PJ, Meerlo P (2011) Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience 190:145–155
66. Oliveira AM, Hawk JD, Abel T, Havekes R (2010) Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learn Mem 17:155–160
67. Orban P, Rauchs G, Balteau E, Degueldre C, Luxen A, Maquet P, Peigneux P (2006) Sleep after spatial learning promotes covert reorganization of brain activity. Proc Natl Acad Sci U S A 103:7124–7129
68. Palchykova S, Winsky-Sommerer R, Meerlo P, Durr R, Tobler I (2006) Sleep deprivation impairs object recognition in mice. Neurobiol Learn Mem 85:263–271
69. Park HJ, Kang WS, Paik JW, Kim JW (2012) Effect of valproic acid through regulation of NMDA receptor-ERK signaling in sleep deprivation rats. J Mol Neurosci 47:554–558
70. Pinho N, Moreira KM, Hipolide DC, Sinigaglia-Coimbra R, Ferreira TL, Nobrega JN, Tufik S, Oliveira MG (2013) Sleep deprivation alters phosphorylated CREB levels in the amygdala: relationship with performance in a fear conditioning task. Behav Brain Res 236:221–224
71. Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW (1997) Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 276:1265–1268
72. Porkka-Heiskanen T, Alanko L, Kalinchuk A, Stenberg D (2002) Adenosine and sleep. Sleep Med Rev 6:321–332
73. Prince TM, Wimmer M, Choi J, Havekes R, Aton S, Abel T (2014) Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory. Neurobiol Learn Mem 109:122–130
74. Rauchs G, Orban P, Schmidt C, Albouy G, Balteau E, Degueldre C, Schnackers C, Sterpenich V, Tinguely G, Luxen A, Maquet P, Peigneux P (2008) Sleep modulates the neural substrates of both spatial and contextual memory consolidation. PLoS ONE 3:e2949
75. Ravassard P, Pachoud B, Comte JC, Mejia-Perez C, Scote-Blachon C, Gay N, Claustrat B, Touret M, Luppi PH, Salin PA (2009) Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. Sleep 32:227–240
76. Ribeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, 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
77. Robertson EM (2012) New insights in human memory interference and consolidation. Curr Biol 22:R66–R71
78. Rolls A, Colas D, Adamantidis A, Carter M, Lanre-Amos T, Heller HC, de Lecea L (2011) Optogenetic disruption of sleep continuity impairs memory consolidation. Proc Natl Acad Sci U S A 108:13305–13310
79. Roman V, Walstra I, Luiten PG, Meerlo P (2005) Too little sleep gradually desensitizes the serotonin 1A receptor system. Sleep 28:1505–1510
80. Ruskin DN, LaHoste GJ (2009) Reduced-volume cues effectively support fear conditioning despite sleep deprivation. Physiol Behav 96:64–66
81. Ruskin DN, Liu C, Dunn KE, Bazan NG, LaHoste GJ (2004) Sleep deprivation impairs hippocampus-mediated contextual learning but not amygdala-mediated cued learning in rats. Eur J Neurosci 19:3121–3124
82. Ruskin DN, Dunn KE, Billiot I, Bazan NG, LaHoste GJ (2006) Eliminating the adrenal stress response does not affect sleep deprivation-induced acquisition deficits in the water maze. Life Sci 78:2833–2838
83. Sannino S, Russo F, Torromino G, Pendolino V, Calabresi P, De Leonibus E (2012) Role of the dorsal hippocampus in object memory load. Learn Mem 19:211–218
84. Seibt J, Dumoulin MC, Aton SJ, Coleman T, Watson A, Naidoo N, Frank MG (2012) Protein synthesis during sleep consolidates cortical plasticity in vivo. Curr Biol 22:676–682
85. Smith C, Rose GM (1996) Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol Behav 59:93–97
86. Sportiche N, Suntsova N, Methippara M, Bashir T, Mitrani B, Szymusiak R, McGinty D (2010) Sustained sleep fragmentation results in delayed changes in hippocampal-dependent cognitive function associated with reduced dentate gyrus neurogenesis. Neuroscience 170:247–258
87. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311–317
88. Tiba PA, Oliveira MG, Rossi VC, Tufik S, Suchecki D (2008) Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments. Sleep 31:505–515
89. Tobler I, Jaggi K (1987) Sleep and EEG spectra in the Syrian hamster (Mesocricetus auratus) under baseline conditions and following sleep deprivation. J Comp Physiol A Sens Neural Behav Physiol 161:449–459
90. van der Borght K, Ferrari F, Klauke K, Roman V, Havekes R, Sgoifo A, van der Zee EA, Meerlo P (2006) Hippocampal cell proliferation across the day: increase by running wheel activity, but no effect of sleep and wakefulness. Behav Brain Res 167:36–41
91. Van Der Werf YD, Altena E, Schoonheim MM, Sanz-Arigita EJ, Vis JC, De Rijke W, Van Someren EJ (2009) Sleep benefits subsequent hippocampal functioning. Nat Neurosci 12:122–123
92. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M, Huang T, Brown KM, Li XY, Descalzi G, Kim SS, Chen T, Shang YZ, Zhuo M, Houslay MD, Abel T (2009) Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461:1122–1125
93. Vecsey CG, Peixoto L, Choi JH, Wimmer M, Jaganath D, Hernandez PJ, Blackwell J, Meda K, Park AJ, Hannenhalli S, Abel T (2012) Genomic analysis of sleep deprivation reveals translational regulation in the hippocampus. Physiol Genomics 44:981–991
94. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11:200–208
95. Walsh CM, Booth V, Poe GR (2011) Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following training. Learn Mem 18:422–434
96. Wang GP, Huang LQ, Wu HJ, Zhang L, You ZD, Zhao ZX (2009) Calcineurin contributes to spatial memory impairment induced by rapid eye movement sleep deprivation. Neuroreport 20:1172–1176
97. Watts A, Gritton HJ, Sweigart J, Poe GR (2012) Antidepressant suppression of non-REM sleep spindles and REM sleep impairs hippocampus-dependent learning while augmenting striatumdependent learning. J Neurosci 32:13411–13420
98. Wimmer ME, Rising J, Galante RJ, Wyner A, Pack AI, Abel T (2013) Aging in mice reduces the ability to sustain sleep/wake states. PLoS ONE 8:e81880
99. Winters BD, Bussey TJ (2005) Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25:52–61
100. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) 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. J Neurosci 24:5901–5908
101. Yang RH, Hu SJ, Wang Y, Zhang WB, Luo WJ, Chen JY (2008) Paradoxical sleep deprivation impairs spatial learning and affects membrane excitability and mitochondrial protein in the hippocampus. Brain Res 1230:224–232
102. Yoo SS, Hu PT, Gujar N, Jolesz FA, Walker MP (2007) A deficit in the ability to form new human memories without sleep. Nat Neurosci 10:385–392
103. Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB (1997) Sleep deprivation by the “flower pot” technique and spatial reference memory. Physiol Behav 61:249–256