Sleep is for forgetting

Journal of Neuroscience

Volumn 37, Issue 3, 2017, Pages 464-473

  Poe, Gina R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Depotentiation; Development; Mental health; Noradrenaline; REM sleep; Spindles; Theta; TR sleep

Indexed keywords

BETA ADRENERGIC RECEPTOR; LEVODOPA; NORADRENALIN; SEROTONIN; SEROTONIN RECEPTOR;

ARTICLE; AUTISM; DORSAL STRIATUM; DYSKINESIA; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HUMAN; HYPERPOLARIZATION; MEMORY DISORDER; NONHUMAN; PARKINSON DISEASE; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRIORITY JOURNAL; REM SLEEP; SCHIZOPHRENIA; SLEEP SPINDLE; SLOW WAVE SLEEP; SYNAPSE; ANIMAL; BRAIN; ELECTROENCEPHALOGRAM; MEMORY CONSOLIDATION; PHYSIOLOGY; SLEEP;

ANIMALS; BRAIN; BRAIN WAVES; HUMANS; MEMORY CONSOLIDATION; SLEEP; SLEEP, REM;

EID: 85010379899     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0820-16.2017     Document Type: Article

References (104)

1. Akindele MO, Evans JI, Oswald I (1970) Mono-amine oxidase inhibitors, sleep and mood. Electroencephalogr Clin Neurophysiol 29:47-56.
2. Almaguer-Melian W, Rojas-Reyes Y, Alvare A, Rosillo JC, Frey JU, Bergado JA (2005) Long-term potentiation in the dentate gyrus in freely moving rats is reinforced by intraventricular application of norepinephrine, but not oxotremorine. Neurobiol Learn Mem 83:72-78.
3. Aston-Jones G, Bloom FE (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1:876-886.
4. Ball WA, Morrison AR, Ross RJ (1989) The effects of tones onPGOwaves in slow wave sleep and paradoxical sleep. Exp Neurol 104:251-256.
5. Basheer R, Sherin JE, Saper CB, Morgan JI, McCarley RW, Shiromani PJ (1997) Effects of sleep on wake-induced c-fos expression. J Neurosci 17:9746-9750.
6. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
7. Blake DT, Merzenich MM (2002) Effects of REM sleep on behaviorally induced changes in neuronal state: Neuronal replay during sleep? Seattle: Association of Professional Sleep Societies.
8. Blake DT, Strata F, Kempter R, Merzenich MM (2005) Experiencedependent plasticity in S1 caused by noncoincident inputs. J Neurophysiol 94:2239-2250.
9. Blitzer RD, Iyengar R, Landau EM (2005) Postsynaptic signaling networks: cellular cogwheels underlying long-term plasticity. Biol Psychiatry 57: 113-119.
10. Bock J, Braun K (1998) Differential emotional experience leads to pruning of dendritic spines in the forebrain of domestic chicks. Neural Plast 6:17-27.
11. Bondareff W, Mountjoy CQ, Roth M (1982) Loss of neurons of origin of the adrenergic projection to cerebral cortex (nucleus locus ceruleus) in senile dementia. Neurology 32:164-168.
12. Booth V, Poe GR (2006) Input source and strength influences overall firing phase of model hippocampal CA1 pyramidal cells during theta: relevance to REM sleep reactivation and memory consolidation. Hippocampus 16: 161-173.
13. Bramham CR, Srebro B (1989) Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res 493:74-86.
14. Braunewell KH, Manahan-Vaughan D (2001) Long-term depression: a cellular basis for learning? Rev Neurosci 12:121-140.
15. Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139-171.
16. Cirelli C, Tononi G (2000a) Gene expression in the brain across the sleepwaking cycle. Brain Res 885:303-321.
17. Cirelli C, Tononi G (2000b) Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J Neurosci 20:9187-9194.
18. Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41:35-43.
19. Cousins JN, El-Deredy W, Parkes LM, Hennies N, Lewis PA (2014) Cued memory reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence. J Neurosci 34:15870-15876.
20. Cowdin N, Kobayashi I, Mellman TA (2014) Theta frequency activity during rapid eye movement (REM) sleep is greater in people with resilience versus PTSD. Exp Brain Res 232:1479-1485.
21. Crick F, Mitchison G (1983) The function of dream sleep. Nature 304:111-114.
22. Datta S, Mavanji V, Ulloor J, Patterson EH (2004) Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivationinduced learning impairment in the rat: a mechanism for sleepdependent plasticity. J Neurosci 24:1416-1427.
23. Dave AS, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290:812-816.
24. Deregnaucourt S, Mitra PP, Feher O, Pytte C, Tchernichovski O (2005) How sleep affects the developmental learning of bird song. Nature 433: 710-716.
25. Eschenko O, Magri C, Panzeri S, Sara SJ (2012) Noradrenergic neurons of the locus coeruleus are phase-lockedto cortical up-down states during sleep. Cereb Cortex 22:426-435.
26. Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G (2006) A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res Bull 69:86-94.
27. Ferrarelli F, Huber R, Peterson MJ, Massimini M, Murphy M, Riedner BA, Watson A, Bria P, Tononi G (2007) Reduced sleep spindle activity in schizophrenia patients. J Psychiatry 164:483-492.
28. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683.
29. Fox SE, Wolfson S, Ranck JB Jr (1986) Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495-508.
30. Gardner RJ, Hughes SW, Jones MW (2013) Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles. J Neurosci 33:18469-18480.
31. Gasparini S, DiFrancesco D (1999) Action of serotonin on the hyperpolarization-activated cation current (Ih) in rat CA1 hippocampal neurons. Eur J Neurosci 11:3093-3100.
32. Givens B (1996) Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport 8:159-163.
33. Grosmark AD, Mizuseki K, Pastalkova E, Diba K, Buzsáki G (2012) REM sleep reorganizes hippocampal excitability. Neuron 75:1001-1007.
34. Hanlon EC, Faraguna U, Vyazovskiy VV, Tononi G, Cirelli C (2009) Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep 32:719-729.
35. Harder R, Malow BA, Goodpaster RL, Iqbal F, Halbower A, Goldman SE, Fawkes DB, Wang L, Shi Y, Baudenbacher F, Diedrich A (2016) Heart rate variability during sleep in children with autism spectrum disorder. Clin Auton Res 26:423-432.
36. Hassani OK, Lee MG, Henny P, Jones BE (2009) Discharge profiles of identified GABAergic in comparisonto cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. J Neurosci 29: 11828-11840.
37. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neurosci 16:218-222.
38. Hoedlmoser K, Birklbauer J, Schabus M, Eibenberger P, Rigler S, Mueller E (2015) The impact of diurnal sleep on the consolidation of a complex gross motor adaptation task. J Sleep Res 24:100-109.
39. Huerta PT, Lisman JE (1995) Bidirectional synaptic c plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15:1053-1063.
40. Jackson C, McCabe BJ, Nicol AU, Grout AS, Brown MW, Horn G (2008) Dynamics of a memory trace: effects of sleep on consolidation. Curr Biol 18:393-400.
41. Jenkins JG, Dallenbach KM (1924) Obliviscence during sleep and waking. J Psychol 35:605-612.
42. Jones BE, Halaris AE, McIlhany M, Moore RY (1977) Ascending projections of the locus coeruleus in the rat: I. Axonal transport in central noradrenaline neurons. Brain Res 127:1-21.
43. Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12:913-918.
44. Katsuki H, Izumi Y, Zorumski CF (1997) Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 77:3013-3020.
45. Kemp A, Manahan-Vaughan D (2004a) Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A 101:8192-8197.
46. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
47. Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19:4090-4101.
48. Lashley KS (1950) In search of the engram. Cambridge: Cambridge University. Lee KH, McCormick DA (1996) Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17:309-321.
49. Léna I, Parrot S, Deschaux O, Muffat-Joly S, Sauvinet V, Renaud B, Suaud-Chagny MF, Gottesmann C (2005) Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep-wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J Neurosci Res 81:891-899.
50. Liberzon I, King AP, Ressler KJ, Almli LM, Zhang P, Ma ST, Cohen GH, Tamburrino MB, Calabrese JR, Galea S. (2014) Interaction of the ADRB2 gene polymorphism with childhood trauma in predicting adult symptoms of posttraumatic stress disorder. JAMA Psychiatry 71:1174-1182.
51. Limoges E, Mottron L, Bolduc C, Berthiaume C, Godbout R (2005) Atypical sleep architecture and the autism phenotype. Brain 128:1049-1061.
52. Manahan-Vaughan D, Braunewell KH (1999) Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A 96:8739-8744.
53. Mann DM, Lincoln J, Yates PO, Stamp JE, Toper S (1980) Changes in the monoamine containing neurones of the human CNS in senile dementia. Br J Psychiatry 136:533-541.
54. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M, Imperato A, Gessa GL (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671:329-332.
55. Mavanji V, Ulloor J, Saha S, Datta S (2004) Neurotoxic lesions of phasic pontine-wave generator cells impair retention of 2-way active avoidance memory. Sleep 27:1282-1292.
56. McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457.
57. McGinty DJ, Harper RM (1976) Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101:569-575.
58. Mellman TA, Kumar A, Kulick-Bell R, Kumar M, Nolan B (1995) Nocturnal/daytime urine noradrenergic measures and sleep in combat-related PTSD. Biol Psychiatry 38:174-179.
59. Melton AW, Irwin JM (1940) The influence of degree of interpolated learn-ing on retroactive inhibition and the overt transfer of specific responses. Am J Psychol 53:175-203.
60. Meneses A, Hong E (1997) Effects of 5-HT4 receptor agonists and antagonists in learning. Pharmacol Biochem Behav 56:347-351.
61. Migliore M, Messineo L, Ferrante M (2004) Dendritic Ih selectively blocks temporal summation of unsynchronized distal inputs in CA1 pyramidal neurons. J Comput Neurosci 16:5-13.
62. Mizumori SJ, Perez GM, Alvarado MC, Barnes CA, McNaughton BL (1990) Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res 528:12-20.
63. Nakao K, Ikegaya Y, Yamada MK, Nishiyama N, Matsuki N (2002) Hippocampal long-term depression as an index of spatial working memory. Eur J Neurosci 16:970-974.
64. Nielsen TA (2000) A review of mentation in REM and NREM sleep: “covert” REM sleep as a possible reconciliation of two opposing models. Behav Brain Sci 23:851-866; discussion 904-1121.
65. Nitz D, Siegel JM (1997) GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience 78:795-801.
66. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsáki G, Siegelbaum SA, Kandel ER, Morozov A (2004) A behavioral role for dendritic integration HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119:719-732.
67. O’Dell TJ, Connor SA, Guglietta R, Nguyen PV (2015) _-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus. Learn Mem 22:461-471.
68. Park SP, Lopez-Rodriguez F, Wilson CL, Maidment N, Matsumoto Y, Engel J Jr (1999) In vivo microdialysis measures of extracellular serotonin in the rat hippocampus during sleep-wakefulness. Brain Res 833:291-296.
69. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387.
70. Poe GR, Nitz DA, McNaughton BL, Barnes CA (2000) Experiencedependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855:176-180.
71. Rashidy-Pour A, Motamedi F, Motahed-Larijani Z (1996a) Effects of reversible inactivations of the medial septal area on reference and working memory versions of the Morris water maze. Brain Res 709:131-140.
72. Rashidy-Pour A, Motamedi F, Semnanian S, Zarrindast MR, Fatollahi Y, Behzadi G (1996b) Effects of reversible inactivation of the medial septal area on long-term potentiation and recurrent inhibition of hippocampal population spikes in rats. Brain Res 734:43-48.
73. Rausch G, Scheich H (1982) Dendritic spine loss and enlargement during maturation of the speech control system in the mynah bird (Gracula religiosa). Neurosci Lett 29:129-133.
74. Ribeiro S, Nicolelis MA (2004) Reverberation, storage, and postsynaptic propagation of memories during sleep. LearnMem11:686-696.
75. Ribeiro S, Goyal V, Mello CV, Pavlides C (1999) Brain gene expression during REM sleep depends on prior waking experience. Learn Mem 6:500-508.
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 rapideye-movement sleep. J Neurosci 22:10914-10923.
77. Roffwarg HP, Muzio JN, Dement WC (1966) Ontogenetic development of the human sleep-dream cycle. Science 152:604-619.
78. Romcy-Pereira R, Pavlides C (2004) Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur J Neurosci 20:3453-3462.
79. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10:211-223.
80. Shank SS, Margoliash D (2009) Sleep and sensorimotor integration during early vocal learning in a songbird. Nature 458:73-77.
81. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123-1128.
82. Solodkin M, Cardona A, Corsi-Cabrera M (1985) Paradoxical sleep augmentation after imprinting in the domestic chick. Physiol Behav 35:343-348.
83. Steriade M (2004) Acetylcholine systems and rhythmic activities during the waking-sleep cycle. Prog Brain Res 145:179-196.
84. Suarez LM, Solis O, Aguado C, Lujan R, Moratalla R (2016) L-DOPA oppositely regulates synaptic strength and spine morphology in D1 and D2 striatal projection neurons in dyskinesia. Cereb Cortex. Advance online publication. Retrieved Sept. 9, 2016. doi: 10.1093/cercor/bhw263.
85. Thomas MJ, Moody TD, Makhinson M, O’Dell TJ (1996) Activity dependent _-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17:475-482.
86. Tomlinson BE, Irving D, Blessed G (1981) Cell loss in the locus coeruleus in senile dementia of Alzheimer type. J Neurol Sci 49:419-428.
87. Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143-150.
88. van Liempt S, Arends J, Cluitmans PJ, Westenberg HG, Kahn RS, Vermetten E (2013) Sympathetic activity and hypothalamo-pituitary-adrenal axis activity during sleep in post-traumatic stress disorder: a study assessing polysomnography with simultaneous blood sampling. Psychoneuroendocrinology 38:155-165.
89. Vanderheyden WM, Poe GR, Liberzon I (2014) Trauma exposure and sleep: using a rodent model to understand sleep function in PTSD. Exp Brain Res 232:1575-1584.
90. Vanderheyden WM, George SA, Urpa L, Kehoe M, Liberzon I, Poe GR (2015) Sleep alterations following exposure to stress predict fearassociated memory impairments in a rodent model of PTSD. Exp Brain Res 233:2335-2346.
91. Veatch OJ, Maxwell-Horn AC, Malow BA (2015) Sleep in autism spectrum disorders. Curr Sleep Med Rep 1:131-140.
92. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578-598.
93. Vyazovskiy V, Borbély AA, Tobler I (2000) Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J Sleep Res 9:367-371.
94. Wallhäusser-Franke E, Nixdorf-Bergweiler BE, DeVoogd TJ (1995) Song isolation is associated with maintaining high spine frequencies on zebra finch 1MAN neurons. Neurobiol Learn Mem 64:25-35.
95. Wamsley EJ, Tucker MA, Payne JD, Stickgold R (2010) A brief nap is beneficial for human route-learning: the role of navigation experience and EEG spectral power. Learn Mem 17:332-336.
96. Wamsley EJ, Tucker MA, Shinn AK, Ono KE, McKinley SK, Ely AV, Goff DC, Stickgold R, Manoach DS (2012) Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry 71:154-161.
97. Wamsley EJ, Shinn AK, Tucker MA, Ono KE, McKinley S, Ely AV, Goff DC, Stickgold R, Manoach DS (2013) The effects of eszopiclone on sleep spindless and memory consolidation in schizophrenia: a double-blind randomized trial. Sleep 36:1369-1376.
98. Watts A, Gritton HJ, Sweigart J, Poe GR (2012) Antidepressant suppression of non-REM sleep spindles and REM sleep impairs hippocampusdependent learning while augmenting striatum-dependent learning. J Neurosci 32:13411-13420.
99. Wierzynski CM, Lubenov EV, Gu M, Siapas AG (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61:587-596.
100. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679.
101. Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160-163.
102. Winson J (1990) The meaning of dreams. Sci Am 263:86-88.
103. Xu L, Anwyl R, Rowan MJ (1998) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394:891-894.
104. Yang HW, Lin YW, Yen CD, Min MY (2002) Change in bi-directional plasticity at CA1 synapses in hippocampal slices taken from 6-hydroxydopamine-treated rats: the role of endogenous norepinephrine. Eur J Neurosci 16:1117-1128.