Sleep and Synaptic Plasticity in the Developing and Adult Brain

  • Marcos G. FrankEmail author
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 25)


Sleep is hypothesized to play an integral role in brain plasticity. This has traditionally been investigated using behavioral assays. In the last 10–15 years, studies combining sleep measurements with in vitro and in vivo models of synaptic plasticity have provided exciting new insights into how sleep alters synaptic strength. In addition, new theories have been proposed that integrate older ideas about sleep function and recent discoveries in the field of synaptic plasticity. There remain, however, important challenges and unanswered questions. For example, sleep does not appear to have a single effect on synaptic strength. An unbiased review of the literature indicates that the effects of sleep vary widely depending on ontogenetic stage, the type of waking experience (or stimulation protocols) that precede sleep and the type of neuronal synapse under examination. In this review, I discuss these key findings in the context of current theories that posit different roles for sleep in synaptic plasticity.


Hebbian Synaptic scaling Homeostasis Function Ontogeny Synaptic remodeling 


  1. Aghajanian GK, Bloom FE (1967) The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 6:716–727PubMedGoogle Scholar
  2. Albensi BC, Oliver DR, Toupin J, Odero G (2007) Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: are they effective or relevant? Exp Neurol 204:1–13PubMedGoogle Scholar
  3. Alfoldi P, Tobler I, Borbely AA (1990) Sleep regulation in rats during early development. Am J Physiol 258:R634–R644PubMedGoogle Scholar
  4. Arrigoni E, Lu J, Vetrivelan R, Saper CB (2009) Long-term synaptic plasticity is impaired in rats with lesions of the ventrolateral preoptic nucleus. Eur J Neurosci 30:2112–2120PubMedCentralPubMedGoogle Scholar
  5. Aton SJ, Broussard C, Dumoulin M, Seibt J, Watson A, Coleman T, Frank MG (2013) Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons. Proc Natl Acad Sci USA 110:3101–3106PubMedCentralPubMedGoogle Scholar
  6. Aton SJ, Seibt J, Dumoulin M, Jha SK, Steinmetz N, Coleman T, Naidoo N, Frank MG (2009) Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61:454–466PubMedCentralPubMedGoogle Scholar
  7. Aton SJ, Suresh A, Broussard C, Frank MG (2014) Sleep promotes cortical response potentiation following visual experience. Sleep (in press)Google Scholar
  8. Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem 11:697–704PubMedCentralPubMedGoogle Scholar
  9. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389–399PubMedGoogle Scholar
  10. Bendor D, Wilson MA (2012) Biasing the content of hippocampal replay during sleep. Nat Neurosci 15:1439–1444PubMedCentralPubMedGoogle Scholar
  11. Benington JH, Frank MG (2003) Cellular and molecular connections between sleep and synaptic plasticity. Prog Neurobiol 69:77–101Google Scholar
  12. Benington JH, Heller HC (1994) Does the function of REM sleep concern non-REM sleep or waking? Prog Neurobiol 44:433–449PubMedGoogle Scholar
  13. Bittar P, Muller D (1993) Time-dependent reversal of long-term potentiation by brief cooling shocks in rat hippocampal slices. Brain Res 620:181–188PubMedGoogle Scholar
  14. Buisseret P, Imbert M (1976) Visual cortical cells: their developmental properties in normal and dark reared kittens. J Physiol 255:511–525PubMedCentralPubMedGoogle Scholar
  15. Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92PubMedGoogle Scholar
  16. Campbell IG, Guinan MJ, Horowitz JM (2002) Sleep deprivation impairs long-term potentiation in the rat hippocampal slices. J Neurophysiol 88:1073–1076PubMedGoogle Scholar
  17. Chauvette S, Seigneur J, Timofeev I (2012) Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 75:1105–1113PubMedCentralPubMedGoogle Scholar
  18. 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 340:435–440PubMedGoogle Scholar
  19. Conboy L, Sandi C (2009) Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action. Neuropsychopharmacology 35:674–685PubMedCentralPubMedGoogle Scholar
  20. Cooke SF, Bear MF (2010) Visual experience induces long-term potentiation in the primary visual cortex. J Neurosci 30:16304–16313PubMedCentralPubMedGoogle Scholar
  21. Crair MC, Ruthazer ES, Gillespie DC, Stryker MP (1997) Relationship between the ocular dominance and orientation maps in visual cortex of monocularly deprived cats. Neuron 19:307–318PubMedGoogle Scholar
  22. Crick F, Mitchison G (1983) The function of dream sleep. Nature 304:111–114PubMedGoogle Scholar
  23. Crick F, Mitchison G (1995) REM sleep and neural nets. Behav Brain Res 69:147–155PubMedGoogle Scholar
  24. Dadvand L, Stryker MP, Frank MG (2006) Sleep does not enhance the recovery of deprived eye responses in developing visual cortex. Neuroscience 143:815–826PubMedCentralPubMedGoogle Scholar
  25. Daftary SS, Panksepp J, Dong Y, Saal DB (2009) Stress-induced, glucocorticoid-dependent strengthening of glutamatergic synaptic transmission in midbrain dopamine neurons. Neurosci Lett 452:273–276PubMedCentralPubMedGoogle Scholar
  26. Dave AS, Margoliash D (2000) Song replay during sleep and computational rules of sensorimotor vocal learning. Science 290:812–816PubMedGoogle Scholar
  27. Davis CJ, Harding JW, Wright JW (2003) REM sleep deprivation-induced deficits in the latency-to-peak induction and maintenance of long-term potentiation within the CA1 region of the hippocampus. Brain Res 973:293–297PubMedGoogle Scholar
  28. Davis CJ, Meighan PC, Taishi P, Krueger JM, Harding JW, Wright JW (2006) REM sleep deprivation attenuates actin-binding protein cortactin: a link between sleep and hippocampal plasticity. Neurosci Lett 400:191–196PubMedGoogle Scholar
  29. Daw NW, Sato H, Fox K, Carmichael T, Gingerich R (1991) Cortisol reduces plasticity in the kitten visual cortex. J Neurobiol 22:158–168PubMedGoogle Scholar
  30. de Villers-Sidani E, Merzenich MM (2011) Chapter 8—Lifelong plasticity in the rat auditory cortex: basic mechanisms and role of sensory experience. In: Chapman CE, Kalaska JF, Green AM, Franco L (eds) Progress in brain research, Elsevier, pp 119–131Google Scholar
  31. Deuker L, Olligs J, Fell J, Kranz TA, Mormann F, Montag C, Reuter M, Elger CE, Axmacher N (2013) Memory consolidation by replay of stimulus-specific neural activity. J Neurosci 33:19373–19383PubMedGoogle Scholar
  32. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126PubMedGoogle Scholar
  33. Donlea JM, Thimgan MS, Suzuki Y, Gottschalk L, Shaw PJ (2011) Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332:1571–1576PubMedCentralPubMedGoogle Scholar
  34. Dumoulin MC, Aton S, Watson A, Coleman T, Frank MG (2013) ERK activity during sleep is necessary for the consolidation of cortical plasticity. Cerebral cortex (in press)Google Scholar
  35. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1–10PubMedCentralPubMedGoogle Scholar
  36. Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75:230–249PubMedCentralPubMedGoogle Scholar
  37. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34:709–720PubMedGoogle Scholar
  38. Faraguna U, Nelson A, Vyazovskiy VV, Cirelli C, Tononi G (2010) Unilateral cortical spreading depression affects sleep need and induces molecular and electrophysiological signs of synaptic potentiation in vivo. Cereb Cortex 20:2939–2947PubMedCentralPubMedGoogle Scholar
  39. Faraguna U, Vyazovskiy VV, Nelson AB, Tononi G, Cirelli C (2008) A causal role for brain-derived neurotrophic factor in the homeostatic regulation of sleep. J Neurosci 28:4088–4095PubMedGoogle Scholar
  40. Florian CD, 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 31:6956–6962Google Scholar
  41. Foeller E, Feldman DE (2004) Synaptic basis for developmental plasticity in somatosensory cortex. Curr Opin Neurobiol 14:89–95PubMedGoogle Scholar
  42. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683PubMedGoogle Scholar
  43. Frank MG (2007) Hippocampal dreams, cortical wishes: a closer look at neuronal replay and the hippocampal-neocortical dialogue during sleep. Cell Sci Rev 3:161–171Google Scholar
  44. Frank MG (2011) Sleep and developmental brain plasticity: not just for kids. Prog Brain Res 193:221–232PubMedGoogle Scholar
  45. Frank MG (2012) Erasing synapses in sleep: is it time to be SHY? Neural Plasticity 2012:264–378Google Scholar
  46. Frank MG (2013) Why I’m not SHY: a reply to Tononi and Cirelli. Neural plasticity 2013:394–946Google Scholar
  47. Frank MG, Benington J (2006) The role of sleep in brain plasticity: dream or reality? Neurosci 12:477–488Google Scholar
  48. Frank MG, Heller HC (1997) Development of REM and slow wave sleep in the rat. Am J Physiol 272:R1792–R1799PubMedGoogle Scholar
  49. Frank MG, Issa NP, Stryker MP (2001) Sleep enhances plasticity in the developing visual cortex. Neuron 30:275–287PubMedGoogle Scholar
  50. Frank MG, Jha SK, Coleman T (2006) Blockade of postsynaptic activity in sleep inhibits developmental plasticity in visual cortex. NeuroReport 17:1459–1463PubMedGoogle Scholar
  51. Frank MG, Morrissette R, Heller HC (1998) Effects of sleep deprivation in neonatal rats. Am J Physiol 275:R148–R157PubMedGoogle Scholar
  52. Franken P, Dijk DJ, Tobler I, Borbely AA (1991) Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol 261:R198–R208PubMedGoogle Scholar
  53. Franken P, Tobler I, Borbely AA (1993) Effects of 12-h sleep deprivation and of 12-h cold exposure on sleep regulation and cortical temperature in the rat. Physiolo Behav 54:885–894Google Scholar
  54. Genzel L, Kroes MCW, Dresler M, Battaglia FP (2014) Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci 37:10–19PubMedGoogle Scholar
  55. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223PubMedGoogle Scholar
  56. Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin Neurobiol 252:452–459Google Scholar
  57. Giuditta A (1995) The sequential hypothesis of the function of sleep. Behav Brain Res 69:157–166PubMedGoogle Scholar
  58. Glotzbach SF, Heller HC (2000) Temperature regulation. In: Roth C, Kryger M, Dement WC (eds) Principles and practice of sleep medicine. Saunders, Philadelphia, pp 289–304Google Scholar
  59. Graves L, Pack A, Abel T (2001) Sleep and memory: a molecular perspective. Trends Neurosci 24:237–243PubMedGoogle Scholar
  60. Groc L, Choquet D, Chaouloff F (2008) The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 11:868–870PubMedGoogle Scholar
  61. Guzman-Marin 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. J Physiol (Lond) 575:807–819Google Scholar
  62. Hanlon EC, Vyazovskiy VV, Faraguna U, Tononi G, Cirelli C (2011) Synaptic potentiation and sleep need: clues from molecular and electrophysiological studies. Curr Top Med Chem 11:2472–2482PubMedGoogle Scholar
  63. Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351–359PubMedGoogle Scholar
  64. Heinrich B (1974) Thermoregulation in endothermic insects. Science 185:747–756PubMedGoogle Scholar
  65. Hengen KB, Lambo ME, Van Hooser SD, Katz DB, Turrigiano GG (2013) Firing rate homeostasis in visual cortex of freely behaving rodents. Neuron 80:335–342PubMedGoogle Scholar
  66. Hennevin E, Huetz C, Edeline J-M (2007) Neural representations during sleep: from sensory processing to memory traces. Neurobiol Learn Mem 87:416–440PubMedGoogle Scholar
  67. Hoffman KL, McNaughton BL (2002) Coordinated reactivation of distributed memory traces in primate cortex. Science 297:2070–2073PubMedGoogle Scholar
  68. Holscher C (1999) Synaptic plasticity and learning and memory: LTP and beyond. J Neurosci Res 58:62–75PubMedGoogle Scholar
  69. Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419–436PubMedCentralPubMedGoogle Scholar
  70. Huber R (2007) TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS ONE 2:e276PubMedCentralPubMedGoogle Scholar
  71. Ishikawa A, Kanayama Y, Matsumura H, Tsuchimochi H, Ishida Y, Nakamura S (2006) Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus. Eur J Neurosci 24:243–248PubMedGoogle Scholar
  72. Jha SK, Jones BE, Coleman T, Steinmetz N, Law C, Griffin G, Hawk J, Frank MG (2005) Sleep-dependent plasticity requires cortical activity. J Neurosci 25:9266–9274PubMedGoogle Scholar
  73. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100–106PubMedGoogle Scholar
  74. Joels M, Krugers H, Karst H (2008) Stress-induced changes in hippocampal function. Prog Brain Res 167:3–15PubMedGoogle Scholar
  75. Jouvet-Mounier D, Astic L, Lacote D (1970) Ontogenesis of the states of sleep in rat, cat and guinea pig during the first postnatal month. Dev Psychobiol 2:216–239PubMedGoogle Scholar
  76. Karst H, Joels M (2005) Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol 94:3479–3486PubMedGoogle Scholar
  77. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758–761PubMedGoogle Scholar
  78. Kim E, Mahmoud GS, Grover LM (2005) REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus. Neurosci Lett 388:163–167PubMedGoogle Scholar
  79. Kirkwood A, Lee HK, Bear MF (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex. Nature 375:328–331PubMedGoogle Scholar
  80. Komatsuzaki Y, Hatanaka Y, Murakami G, Mukai H, Hojo Y, Saito M, Kimoto T, Kawato S (2012) Corticosterone induces rapid spinogenesis via synaptic glucocorticoid receptors and kinase networks in hippocampus. PLoS ONE 7:e34124PubMedCentralPubMedGoogle Scholar
  81. Kopp C, Longordo F, Nicholson JR, Luthi A (2006) Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. J Neurosci 26:12456–12465PubMedGoogle Scholar
  82. Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience and EEG dynamics. J Neurosci 19:4090–4101PubMedGoogle Scholar
  83. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183–1194PubMedGoogle Scholar
  84. Liston C, Cichon JM, Jeanneteau F, Jia Z, Chao MV, Gan W-B (2013) Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nat Neurosci 16:698–705PubMedCentralPubMedGoogle Scholar
  85. Liu W, Yuen EY, Yan Z (2010) The stress hormone corticosterone increases synaptic amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors via serum- and glucocorticoid-inducible kinase (SGK) regulation of the GDI-Rab4 complex. J Biol Chem 285:6101–6108Google Scholar
  86. Longordo F, Kopp C, Mishina M, Lujan R, Luthi A (2009) NR2A at CA1 synapses is obligatory for the susceptibility of hippocampal plasticity to sleep loss. J Neurosci 29:9026–9041PubMedCentralPubMedGoogle Scholar
  87. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156PubMedGoogle Scholar
  88. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21PubMedGoogle Scholar
  89. Maquet P, Laureys S, Peigneux P, Fuchs S, Petiau C, Phillips C, Aerts J, Del Fiore G, Degueldre C, Meulemans T, Luxen A, Franck G, Van Der Linden M, Smith C, Cleeremans A (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3:831–836PubMedGoogle Scholar
  90. Maret S, Faraguna U, Nelson AB, Cirelli C, Tononi G (2011) Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat Neurosci (advance online publication)Google Scholar
  91. Markram H, Gerstner W, Sjostrom PJ (2011) A history of spike-timing-dependent plasticity. Front Synaptic Neurosci 3:1–24Google Scholar
  92. Marks CA, Wayner MJ (2005) Effects of sleep disruption on rat dentate granule cell LTP in vivo. Brain Res Bull 66:114–119PubMedGoogle Scholar
  93. McDermott CM, Hardy MN, Bazan NG, Magee JC (2005) Sleep-deprivation induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus J Physiol (Lond). doi:  10.1113/jphysiol.2005.093781
  94. 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 (Lond) 570:553–565Google Scholar
  95. 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 23:9687–9695PubMedGoogle Scholar
  96. Mioche L, Singer W (1989) Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties. J Neurophysiol 62:185–197PubMedGoogle Scholar
  97. Miyamoto H, Katagiri H, Hensch T (2003) Experience-dependent slow-wave sleep development. Nat Neurosci 6:553–554PubMedGoogle Scholar
  98. Mongrain V, Hernandez SA, Pradervand S, Dorsaz S, Curie T, Hagiwara G, Gip P, Heller HC, Franken P (2010) Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis. Sleep 33:1147–1157PubMedCentralPubMedGoogle Scholar
  99. Moser E, Mathiesen I, Andersen P (1993) Association between brain temperature and dentate field potentials in exploring and swimming rats. Science 259:1324–1326PubMedGoogle Scholar
  100. 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 49:143–155PubMedGoogle Scholar
  101. Olijslagers JE, de Kloet ER, Elgersma Y, van Woerden GM, Joels M, Karst H (2008) Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 27:2542–2550PubMedGoogle Scholar
  102. Olson C, Freeman RD (1975) Progressive changes in kitten striate cortex during monocular deprivation. J Neurophysiol 38:26–32PubMedGoogle Scholar
  103. Olson C, Freeman RD (1980) Profile of the sensitive period for monocular deprivation in kittens. Exp Brain Res 39:17–21PubMedGoogle Scholar
  104. Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep. J Neurosci 9:2907–2918PubMedGoogle Scholar
  105. Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Phillips C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44:535–545PubMedGoogle Scholar
  106. Peng IF, Berke BA, Zhu Y, Lee W-H, Chen W, Wu C-F (2007) Temperature-dependent developmental plasticity of drosophila neurons: cell-autonomous roles of membrane excitability, Ca2+ influx, and cAMP signaling. J Neurosci 27:12611–12622PubMedGoogle Scholar
  107. Pennartz CMA, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL (2004) The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci 24:6446–6456PubMedGoogle Scholar
  108. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12:919–926PubMedGoogle Scholar
  109. Poe GR, Nitz DA, McNaughton BL, Barnes CA (2000) Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855:176–180PubMedGoogle Scholar
  110. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337–351PubMedCentralPubMedGoogle Scholar
  111. Qin YL, McNaughton BL, Skaggs WE, Barnes CA (1997) Memory reprocessing in cortiocortical and hippocampalcortical neuronal ensembles. Philos Trans R Soc Lond B Biol Sci 352:1525–1533PubMedCentralPubMedGoogle Scholar
  112. Ravassard P, Pachoud B, Comte J, Gay N, Touret M, Luppi P, Salin PA (2006) Paradoxical sleep amount modulates neuronal plasticity in adult rat hippocampus. J Sleep Res 15:191Google Scholar
  113. 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 32:227–240PubMedCentralPubMedGoogle Scholar
  114. Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H, Morris RGM (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981–4989PubMedGoogle Scholar
  115. Ribeiro S (2004) Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2:e24PubMedCentralPubMedGoogle Scholar
  116. Ribeiro S (2007) Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus. Front Neurosci 1:43–55PubMedCentralPubMedGoogle Scholar
  117. Ribeiro S (2011) Sleep and plasticity. Pflugers Archiv Eur J Physiol 1–10Google Scholar
  118. Roelandse M, Matus A (2004) Hypothermia-associated loss of dendritic spines. J Neurosci 24:7843–7847PubMedGoogle Scholar
  119. Roffwarg HP, Muzio JN, Dement WC (1966) Ontogenetic development of the human sleep-dream cycle. Science 152:604–619PubMedGoogle Scholar
  120. Romcy-Pereira R, Pavlides C (2004) Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur J Neurosci 20:3453–3462PubMedGoogle Scholar
  121. Sato M, Stryker MP (2008) Distinctive features of adult ocular dominance plasticity. J Neurosci 28:10278–10286PubMedCentralPubMedGoogle Scholar
  122. Satoh E, Shimeki S (2010) Acute restraint stress enhances calcium mobilization and glutamate exocytosis in cerebrocortical synaptosomes from mice. Neurochem Res 35:693–701PubMedGoogle Scholar
  123. Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF (2003) NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38:977–985PubMedGoogle Scholar
  124. Schönauer M, Geisler T, Gais S (2013) Strengthening procedural memories by reactivation in sleep. J Cogn Neurosci 26:143–153PubMedGoogle Scholar
  125. Schwindel DC, McNaughton B (2011) Hippocampal-cortical interactions and the dynamics of memory trace activation. Prog Brain Res 193:163–177PubMedGoogle Scholar
  126. Seibt J, Dumoulin M, Aton SJ, Naidoo J, Watson A, Coleman T, Frank MG (2012) Protein synthesis during sleep consolidates cortical plasticity in vivo. Curr Biol 22:676–682PubMedCentralPubMedGoogle Scholar
  127. Seibt J, Frank MG (2012) Translation regulation in sleep: making experience last. Communicative and integrative biology (in Press)Google Scholar
  128. Sengpiel F, Godecke I, Stawinski P, Hubener M, Lowel S, Bonhoffer T (1998) Intrinsic and environmental factors in the development of functional maps in cat visual cortex. Neuropharmacology 37:607–621PubMedGoogle Scholar
  129. Shaffery JP, Lopez J, Bissette G, Roffwarg HP (2005) Rapid eye movement sleep deprivation revives a form of developmentally regulated synaptic plasticity in the visual cortex of post-critical period rats. Neurosci Lett 391:131–135Google Scholar
  130. Shaffery JP, Lopez J, Roffwarg HP (2012) Brain-derived neurotrophic factor (BDNF) reverses the effects of rapid eye movement sleep deprivation (REMSD) on developmentally regulated, long-term potentiation (LTP) in visual cortex slices. Neurosci Lett 513:84–88PubMedCentralPubMedGoogle Scholar
  131. Shaffery JP, Roffwarg HP (2003) Rapid eye-movement sleep deprivation does not ‘rescue’ developmentally regulated long-term potentiation in visual cortex of mature rats. Neurosci Lett 342:196–200PubMedGoogle Scholar
  132. Shaffery JP, Sinton CM, Bissette G, Roffwarg HP, Marks GA (2002) Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 110:431–443PubMedGoogle Scholar
  133. Siapas AG, Wilson MA (1998) Coordinated interations between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128PubMedGoogle Scholar
  134. Simkus CRL, Stricker C (2002) Properties of mEPSCs recorded in layer II neurones of rat barrel cortex. J Physiol 545:509–520PubMedCentralPubMedGoogle Scholar
  135. Singer W (1979) Neuronal mechanisms in experience dependent modification of visual cortex function. In: Cuenod M, Kreutzberg GW, Bloom FE (eds) Development and chemical sensitivity of neurons. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 457–477Google Scholar
  136. Sirota A, Csicsvari J, Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rodents. PNAS 100:2065–2069PubMedCentralPubMedGoogle Scholar
  137. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870–1873PubMedGoogle Scholar
  138. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563–576PubMedGoogle Scholar
  139. Stevenson RD (1985) Body size and limits to the daily range of body temperature in terrestrial ectotherms. Am Nat 125:102–117Google Scholar
  140. Sur M, Leamey CA (2001) Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2:251–262PubMedGoogle Scholar
  141. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, McCarley RW, Brown RE, Strecker RE (2006) Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 23:2739–2748PubMedCentralPubMedGoogle Scholar
  142. Tatsuno M, Lipa P, McNaughton BL (2006) Methodological considerations on the use of template matching to study long-lasting memory trace replay. J Neurosci 26:10727–10742PubMedGoogle Scholar
  143. Thurber A, Jha SK, Coleman T, Frank MG (2008) A preliminary study of sleep ontogenesis in the ferret (Mustela putorius furo). Behav Brain Res 189:41–51PubMedCentralPubMedGoogle Scholar
  144. Tiriac A, Uitermarkt BD, Fanning AS, Sokoloff G, Blumberg MS (2012) Rapid whisker movements in sleeping newborn rats. Curr Biol 22:2075–2080PubMedCentralPubMedGoogle Scholar
  145. Tononi G (2009) Slow wave homeostasis and synaptic plasticity. J Clin Sleep Med 5:S16–S19PubMedCentralPubMedGoogle Scholar
  146. Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143–150PubMedGoogle Scholar
  147. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62PubMedGoogle Scholar
  148. Tononi G, Cirelli C (2012) Time to be SHY? some comments on sleep and synaptic homeostasis. Neural plasticity (in press)Google Scholar
  149. Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81:12–34PubMedCentralPubMedGoogle Scholar
  150. Tropea D, Van Wart A, Sur M (2009) Molecular mechanisms of experience-dependent plasticity in visual cortex. Philos Trans R Soc B Biol Sci 364:341–355Google Scholar
  151. Tsanov M, Manahan-Vaughan D (2007) The adult visual cortex expresses dynamic synaptic plasticity that is driven by the light/dark cycle. J Neurosci 27:8414–8421PubMedGoogle Scholar
  152. Tse YC, Bagot RC, Wong TP (2012) Dynamic regulation of NMDAR function in the adult brain by the stress hormone corticosterone. Front Cell Neurosci 6:9PubMedCentralPubMedGoogle Scholar
  153. Turrigiano G (2007) Homeostatic signaling: the positive side of negative feedback. In: Cull-Candy S, Klein R (eds) Curr Opin Neurobiol Signal mech 17:318–324Google Scholar
  154. Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227PubMedGoogle Scholar
  155. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422–435PubMedCentralPubMedGoogle Scholar
  156. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892–896PubMedGoogle Scholar
  157. Turrigiano GG, Nelson SB (2000) Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10:358–364PubMedGoogle Scholar
  158. Van Cauter E (2005) Endocrine physiology. In: Kryger M, Roth T, Dement WC (eds) Principles and practice of sleep medicine. Elsevier, Philadelphia, pp 266–282Google Scholar
  159. Vanin S, Bhutani S, Montelli S, Menegazzi P, Green EW, Pegoraro M, Sandrelli F, Costa R, Kyriacou CP (2012) Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 484:371–375PubMedGoogle Scholar
  160. Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M, Huang T, Brown KM, Li X-Y, Descalzi G, Kim SS, Chen T, Shang Y-Z, Zhuo M, Houslay MD, Abel T (2009) Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461:1122–1125PubMedCentralPubMedGoogle Scholar
  161. 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 11:200–208PubMedGoogle Scholar
  162. Wiesel TN, Hubel DH (1963) Single cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 28:1029–1040Google Scholar
  163. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–682PubMedGoogle Scholar
  164. Yang G, Gan W.-B (2011) Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex. Dev Neurobiol 72:1391–1398Google Scholar
  165. Yuen EY, Liu W, Karatsoreos IN, Ren Y, Feng J, McEwen BS, Yan Z (2011) Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry 16:156–170PubMedCentralPubMedGoogle Scholar
  166. Zhong Y, Wu C-F (2004) Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci 24:1439–1445PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Neuroscience, School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Department of NeuroscienceUniversity of PennsylvaniaPhiladelphiaUSA

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