Cellular and neurochemical basis of sleep stages in the thalamocortical network

eLife

Volumn 5, Issue November 2016, 2016, Pages

  Krishnan, Giri P ^a   Chauvette, Sylvain ^b   Shamie, Isaac ^c   Soltani, Sara ^b   Timofeev, Igor ^b   Cash, Sydney S ^d   Halgren, Eric ^c   Bazhenov, Maxim ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BRAIN MONOAMINE; HISTAMINE; PROPOFOL;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL AMPLITUDE; ADULT; ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAT; CELL FUNCTION; CLUSTER ANALYSIS; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DECAY TIME CONSTANT; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAPHY; HUMAN; INHIBITORY POSTSYNAPTIC POTENTIAL; MICRODIALYSIS; MODEL; MOUSE; NERVE CELL NETWORK; NERVE POTENTIAL; NERVE STIMULATION; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; NONREM SLEEP; POTASSIUM CURRENT; REM SLEEP; SLEEP PATTERN; SLEEP STAGE; SLEEP WAKING CYCLE; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; ULTRADIAN RHYTHM; WAKEFULNESS; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; METABOLISM; PHYSIOLOGY; SPECIES DIFFERENCE; THALAMUS;

ACETYLCHOLINE; ANIMALS; CATS; CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; GAMMA-AMINOBUTYRIC ACID; HISTAMINE; HUMANS; MICE; NERVE NET; SLEEP STAGES; SPECIES SPECIFICITY; THALAMUS; WAKEFULNESS;

EID: 84997173338     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.18607     Document Type: Article

References (94)

1. Achermann P, Borbély AA. 1997. Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81:213-222. doi: 10.1016/S0306-4522(97)00186-3, PMID: 9300413
2. Aeschbach D, Borbély AA. 1993. All-night dynamics of the human sleep EEG. Journal of Sleep Research 2:70-81. doi: 10.1111/j.1365-2869.1993.tb00065.x, PMID: 10607074
3. Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723. doi: 10.1109/TAC.1974.1100705
4. Amzica F, Steriade M. 1997. The K-complex: its slow (<1-Hz) rhythmicity and relation to delta waves. Neurology 49:952-959. doi: 10.1212/wnl.49.4.952, PMID: 9339673
5. Amzica F, Steriade M. 1998. Electrophysiological correlates of sleep delta waves. Electroencephalography and Clinical Neurophysiology 107:69-83. doi: 10.1016/S0013-4694(98)00051-0, PMID: 9751278
6. Aston-Jones G, Bloom FE. 1981. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. Journal of Neuroscience 1:876-886. PMID: 7346592
7. Baghdoyan HA, Lydic R. 2012. Chapter 57-The neurochemistry of sleep and wakefulness. In: Basic Neurochemistry, 8th edn. New York: Academic Press. p 982-999.
8. Bazhenov M, Timofeev I, Steriade M, Sejnowski T. 2000. Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. Journal of Neurophysiology 84:1076-1087. PMID: 10938329
9. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. 1998. Computational models of thalamocortical augmenting responses. Journal of Neuroscience 18:6444-6465. PMID: 9698334
10. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. 1999. Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nature Neuroscience 2:168-174. doi: 10.1038/5729, PMID: 10195202
11. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. 2002. Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. Journal of Neuroscience 22:8691-8704. PMID: 12351744
12. Bendor D, Wilson MA. 2012. Biasing the content of hippocampal replay during sleep. Nature Neuroscience 15: 1439-1444. doi: 10.1038/nn.3203, PMID: 22941111
13. Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M. 2011. Corticothalamic feedback controls sleep spindle duration in vivo. Journal of Neuroscience 31:9124-9134. doi: 10.1523/JNEUROSCI.0077-11.2011, PMID: 21697364
14. Bruno RM, Sakmann B. 2006. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627. doi: 10.1126/science.1124593, PMID: 16778049
15. Cantero JL, Atienza M. 2000. Alpha burst activity during human REM sleep: descriptive study and functional hypotheses. Clinical Neurophysiology 111:909-915. doi: 10.1016/S1388-2457(99)00318-1, PMID: 10802463
16. Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C, Devinsky O, Kuzniecky R, Doyle W, Madsen JR, Bromfield E, Eross L, Halász P, Karmos G, Csercsa R, Wittner L, Ulbert I. 2009. The human K-complex represents an isolated cortical down-state. Science 324:1084-1087. doi: 10.1126/science.1169626, PMID: 1 9461004
17. Chauvette S, Seigneur J, Timofeev I. 2012. Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 75:1105-1113. doi: 10.1016/j.neuron.2012.08.034, PMID: 22998877
18. Chen JY, Chauvette S, Skorheim S, Timofeev I, Bazhenov M. 2012. Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. The Journal of Physiology 590:3987-4010. doi: 10.1113/jphysiol.2012.227462, PMID: 22641778
19. Ching S, Cimenser A, Purdon PL, Brown EN, Kopell NJ. 2010. Thalamocortical model for a propofol-induced-rhythm associated with loss of consciousness. PNAS 107:22665-22670. doi: 10.1073/pnas.1017069108
20. Clemens Z, Molle M, Eross L, Barsi P, Halász P, Born J. 2007. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130:2868-2878. doi: 10.1093/brain/awm146, PMID: 17615093
21. Compte A, Sanchez-Vives MV, McCormick DA, Wang X-J. 2003. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. Journal of Neurophysiology 89: 2707-2725. doi: 10.1152/jn.00845.2002
22. Constanti A, Galvan M. 1983. M-current in voltage-clamped olfactory cortex neurones. Neuroscience Letters 39: 65-70. doi: 10.1016/0304-3940(83)90166-0, PMID: 6314193
23. Contreras D, Steriade M. 1995. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. Journal of Neuroscience 15:604-622. PMID: 7823167
24. Contreras D, Steriade M. 1996. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. The Journal of Physiology 490:159-179. doi: 10.1113/jphysiol.1996.sp021133, PMID: 87452 85
25. Crowley K, Trinder J, Kim Y, Carrington M, Colrain IM. 2002. The effects of normal aging on sleep spindle and K-complex production. Clinical Neurophysiology 113:1615-1622. doi: 10.1016/S1388-2457(02)00237-7, PMID: 12350438
26. Destexhe A, Bal T, McCormick DA, Sejnowski TJ. 1996. Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. Journal of Neurophysiology 76:2049-2070. PMID: 8890314
27. Destexhe A, Mainen ZF, Sejnowski TJ. 1994. An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Computation 6:14-18. doi: 10.1162/neco.1994.6.1.14
28. Euston DR, Tatsuno M, McNaughton BL. 2007. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318:1147-1150. doi: 10.1126/science.1148979, PMID: 18006749
29. Feinberg I, Floyd TC. 1979. Systematic trends across the night in human sleep cycles. Psychophysiology 16:283-291. doi: 10.1111/j.1469-8986.1979.tb02991.x, PMID: 220659
30. Flood P, Ramirez-Latorre J, Role L. 1997. Alpha 4 beta 2 neuronal nicotinic acetylcholine receptors in the central nervous system are inhibited by isoflurane and propofol, but alpha 7-type nicotinic acetylcholine receptors are unaffected. Anesthesiology 86:859-865. doi: 10.1097/00000542-199704000-00016, PMID: 9105230
31. Gil Z, Connors BW, Amitai Y. 1997. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686. doi: 10.1016/S0896-6273(00)80380-3, PMID: 9331357
32. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. Journal of Neuroscience 26:4535-4545. doi: 10.1523/JNEUROSCI.5297-05.2006, PMID: 16641233
33. Hengen KB, Torrado Pacheco A, McGregor JN, Van Hooser SD, Turrigiano GG. 2016. Neuronal fring rate homeostasis is inhibited by sleep and promoted by wake. Cell 165:180-191. doi: 10.1016/j.cell.2016.01.046, PMID: 26997481
34. Hill S, Tononi G. 2005. Modeling sleep and wakefulness in the thalamocortical system. Journal of Neurophysiology 93:1671-1698. doi: 10.1152/jn.00915.2004, PMID: 15537811
35. Hsieh CY, Cruikshank SJ, Metherate R. 2000. Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Research 880:51-64. doi: 10.1016/S0006-8993(00)02766-9, PMID: 11032989
36. Iber C, Aaos M. 2007. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications: American Academy of Sleep Medicine.
37. Kikuchi T, Wang Y, Sato K, Okumura F. 1998. In vivo effects of propofol on acetylcholine release from the frontal cortex, hippocampus and striatum studied by intracerebral microdialysis in freely moving rats. British Journal of Anaesthesia 80:644-648. doi: 10.1093/bja/80.5.644, PMID: 9691870
38. Kimura F, Fukuda M, Tsumoto T. 1999. Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input. European Journal of Neuroscience 11:3597-3609. doi: 10.1046/j.1460-9568.1999.00779.x, PMID: 10564367
39. Kitamura A, Marszalec W, Yeh JZ, Narahashi T. 2003. Effects of halothane and propofol on excitatory and inhibitory synaptic transmission in rat cortical neurons. Journal of Pharmacology and Experimental Therapeutics 304:162-171. doi: 10.1124/jpet.102.043273, PMID: 12490587
40. Lemieux M, Chen JY, Lonjers P, Bazhenov M, Timofeev I. 2014. The impact of cortical deafferentation on the neocortical slow oscillation. Journal of Neuroscience 34:5689-5703. doi: 10.1523/JNEUROSCI.1156-13.2014, PMID: 24741059
41. Liu YW, Zuo W, Ye JH. 2013. Propofol stimulates noradrenalin-inhibited neurons in the ventrolateral preoptic nucleus by reducing GABAergic inhibition. Anesthesia & Analgesia 117:358-363. doi: 10.1213/ANE.0b013e318297366e, PMID: 23780420
42. Loomis AL, Harvey EN, Hobart GA. 1937. Cerebral states during sleep, as studied by human brain potentials. Journal of Experimental Psychology 21:127-144. doi: 10.1037/h0057431
43. 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. Journal of Neuroscience Research 81:891-899. doi: 10.1002/jnr.20602, PMID: 16041801
44. Marrosu F, Portas C, Mascia MS, Casu MA, Fà 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 Research 671:329-332. doi: 10.1016/0006-8993(94)01399-3, PMID: 7743225
45. McCarley RW, Hobson JA. 1975. Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189:58-60. doi: 10.1126/science.1135627, PMID: 1135627
46. McCormick DA, Bal T. 1997. Sleep and arousal: thalamocortical mechanisms. Annual Review of Neuroscience 20: 185-215. doi: 10.1146/annurev.neuro.20.1.185, PMID: 9056712
47. McCormick DA, Williamson A. 1989. Convergence and divergence of neurotransmitter action in human cerebral cortex. PNAS 86:8098-8102. doi: 10.1073/pnas.86.20.8098, PMID: 2573061
48. McCormick DA, Williamson A. 1991. Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: possible cellular mechanisms of histaminergic control of arousal. Journal of Neuroscience 11:3188-3199. PMID: 1658246
49. McCormick DA. 1992. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Progress in Neurobiology 39:337-388. doi: 10.1016/0301-0082(92)90012-4, PMID: 1354387
50. Mena-Segovia J, Sims HM, Magill PJ, Bolam JP. 2008. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. The Journal of Physiology 586:2947-2960. doi: 10.1113/jphysiol.2008.153874, PMID: 18440991
51. Meuret P, Backman SB, Bonhomme V, Plourde G, Fiset P. 2000. Physostigmine reverses propofol-induced unconsciousness and attenuation of the auditory steady state response and bispectral index in human volunteers. Anesthesiology 93:708-717. doi: 10.1097/00000542-200009000-00020, PMID: 10969304
52. Mittmann T, Alzheimer C. 1998. Muscarinic inhibition of persistent Na+ current in rat neocortical pyramidal neurons. Journal of Neurophysiology 79:1579-1582. PMID: 9497434
53. Murasaki O, Kaibara M, Nagase Y, Mitarai S, Doi Y, Sumikawa K, Taniyama K. 2003. Site of action of the general anesthetic propofol in muscarinic M1 receptor-mediated signal transduction. Journal of Pharmacology and Experimental Therapeutics 307:995-1000. doi: 10.1124/jpet.103.055772, PMID: 14534362
54. Murphy M, Bruno MA, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant JF, Phillips C, Massimini M, Laureys S, Tononi G, Boly M. 2011. Propofol anesthesia and sleep: a high-density EEG study. Sleep 34:283-291. doi: 10.3410/f.11117956.12356054, PMID: 21358845
55. Molle M, Marshall L, Gais S, Born J. 2002. Grouping of spindle activity during slow oscillations in human nonrapid eye movement sleep. Journal of Neuroscience 22:10941-10947. PMID: 12486189
56. Muller B, Gabelein WD, Schulz H. 2006. A taxonomic analysis of sleep stages. Sleep 29:967-974. PMID: 16 895265
57. Nelson LE, Guo TZ, Lu J, Saper CB, Franks NP, Maze M. 2002. The sedative component of anesthesia is mediated by GABA(A) receptors in an endogenous sleep pathway. Nature Neuroscience 5:979-984. doi: 10.1038/nn913, PMID: 12195434
58. Niedermeyer E, da Silva FL. 2005. Electroencephalography: Basic Principles, Clinical Applications, and Related Fields. Lippincott Williams & Wilkins.
59. Niknazar M, Krishnan GP, Bazhenov M, Mednick SC. 2015. Coupling of thalamocortical sleep oscillations are important for memory consolidation in humans. PLoS One 10:e0144720. doi: 10.1371/journal.pone.0144720, PMID: 26671283
60. Nádasdy Z, Hirase H, Czurkó A, Csicsvari J, Buzsáki G. 1999. Replay and time compression of recurring spike sequences in the hippocampus. Journal of Neuroscience 19:9497-9507. PMID: 10531452
61. Parrino L, Terzano MG. 1996. Polysomnographic effects of hypnotic drugs. A review. Psychopharmacology 126: 1-16. doi: 10.1007/BF02246405, PMID: 8853211
62. Pennartz CM, 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. Journal of Neuroscience 24:6446-6456. doi: 10.1523/JNEUROSCI.0575-04.2004, PMID: 15269254
63. Popa D, Duvarci S, Popescu AT, Lena C, Pare D. 2010. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. PNAS 107:6516-6519. doi: 10.1073/pnas.0913016107
64. Prell GD, Khandelwal JK, Burns RS, LeWitt PA, Green JP. 1988. Elevated levels of histamine metabolites in cerebrospinal fluid of aging, healthy humans. Comprehensive Gerontology. Section A, Clinical and Laboratory Sciences 2:114-119. PMID: 2906817
65. Purdon PL, Pierce ET, Mukamel EA, Prerau MJ, Walsh JL, Wong KFK, Salazar-Gomez AF, Harrell PG, Sampson AL, Cimenser A, Ching S, Kopell NJ, Tavares-Stoeckel C, Habeeb K, Merhar R, Brown EN. 2013. Electroencephalogram signatures of loss and recovery of consciousness from propofol. PNAS 110:E1142-E1151. doi: 10.1073/pnas.1221180110
66. Rechtschaffen A, Kales A. 1968. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. Bethesda, Md: U. S. National Institute of Neurological Diseases and Blindness, Neurological Information Network.
67. Robinson PA, Phillips AJK, Fulcher BD, Puckeridge M, Roberts JA. 2011. Quantitative modelling of sleep dynamics. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 369:3840-3854. doi: 10.1098/rsta.2011.0120
68. Rudolph M, Pospischil M, Timofeev I, Destexhe A. 2007. Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. Journal of Neuroscience 27:5280-5370. doi: 10.1523/JNEUROSCI.4652-06.2007, PMID: 17507551
69. Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nature Neuroscience 3:1027-1034. doi: 10.1038/79848, PMID: 11017176
70. Saunders A, Granger AJ, Sabatini BL. 2015. Corelease of acetylcholine and GABA from cholinergic forebrain neurons. eLife 4:e06412. doi: 10.7554/eLife.06412, PMID: 25723967
71. Schellenberger Costa M, Weigenand A, Ngo HV, Marshall L, Born J, Martinetz T, Claussen JC. 2016. A thalamocortical neural mass model of the EEG during NREM sleep and Its response to auditory stimulation. PLOS Computational Biology 12:e1005022. doi: 10.1371/journal.pcbi.1005022, PMID: 27584827
72. Sheroziya M, Timofeev I. 2014. Global intracellular slow-wave dynamics of the thalamocortical system. Journal of Neuroscience 34:8875-8893. doi: 10.1523/JNEUROSCI.4460-13.2014, PMID: 24966387
73. Silber MH, Ancoli-Israel S, Bonnet MH, Chokroverty S, Grigg-Damberger MM, Hirshkowitz M, Kapen S, Keenan SA, Kryger MH, Penzel T, Pressman MR, Iber C. 2007. The visual scoring of sleep in adults. Journal of Clinical Sleep Medicine 3:121-131. PMID: 17557422
74. Sivagnanam S, Majumdar A, Yoshimoto K, Astakhov V, Bandrowski A, Martone ME, Carnevale NT. 2013. Introducing the Neuroscience Gateway. IWSG.
75. Steriade M, Deschénes M. 1984. The thalamus as a neuronal oscillator. Brain Research Reviews 8:1-63. doi: 10.1016/0165-0173(84)90017-1
76. Steriade M, Deschênes M, Domich L, Mulle C. 1985. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. Journal of Neurophysiology 54:1473-1497. PMID: 4087044
77. Steriade M, Dossi RC, Nuñez A. 1991. Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. Journal of Neuroscience 11:3200-3217. PMID: 1941080
78. Steriade M, Jones EG, Llinas R. 1990. Thalmic Oscillations and Signaling. New York: John Wiley & Sons.
79. Steriade M, Llinás RR. 1988. The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68:649-742. PMID: 2839857
80. Steriade M, McCormick D, Sejnowski T. 1993a. Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685. doi: 10.1126/science.8235588
81. Steriade M, Nuñez A, Amzica F. 1993b. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. Journal of Neuroscience 13:3266-3283
82. Steriade M, Timofeev I, Grenier F. 2001. Natural waking and sleep states: a view from inside neocortical neurons. Journal of Neurophysiology 85:1969-1985. PMID: 11353014
83. Szymusiak R, Alam N, McGinty D. 2000. Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep. Behavioural Brain Research 115:171-253. doi: 10.1016/S0166-4328(00)00257-6, PMID: 11000419
84. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M. 2000. Origin of slow cortical oscillations in deafferented cortical slabs. Cerebral Cortex 10:1185-1199. doi: 10.1093/cercor/10.12.1185, PMID: 11073868
85. Timofeev I, Grenier F, Steriade M. 2001. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. PNAS 98:1924-1929. doi: 10.1073/pnas.041430398, PMID: 11172052
86. Timofeev I, Steriade M. 1996. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. Journal of Neurophysiology 76:4152-4168. PMID: 8985908
87. Vanini G, Lydic R, Baghdoyan HA. 2012. GABA-to-ACh ratio in basal forebrain and cerebral cortex varies significantly during sleep. Sleep 35:1325-1334. doi: 10.5665/sleep.2106, PMID: 23024430
88. Vanini G, Wathen BL, Lydic R, Baghdoyan HA. 2011. Endogenous GABA levels in the pontine reticular formation are greater during wakefulness than during rapid eye movement sleep. Journal of Neuroscience 31:2649-2656. doi: 10.1523/JNEUROSCI.5674-10.2011, PMID: 21325533
89. Vazquez J, Baghdoyan HA. 2001. Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 280: R598-601. PMID: 11208592
90. von Krosigk M, Bal T, McCormick DA. 1993. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261:361-364. doi: 10.1126/science.8392750, PMID: 8392750
91. Wei Y, Krishnan GP, Bazhenov M. 2016. Synaptic mechanisms of memory consolidation during sleep slow oscillations. Journal of Neuroscience 36:4231-4247. doi: 10.1523/JNEUROSCI.3648-15.2016, PMID: 27076422
92. Werth E, Achermann P, Borbély AA. 1996. Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. Neuroreport 8:123-127. doi: 10.1097/00001756-199612200-00025, PMID: 9051765
93. Wulff K, Gatti S, Wettstein JG, Foster RG. 2010. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nature Reviews Neuroscience 11:589-599. doi: 10.1038/nrn2868, PMID: 20631712
94. Yu X, Ye Z, Houston CM, Zecharia AY, Ma Y, Zhang Z, Uygun DS, Parker S, Vyssotski AL, Yustos R, Franks NP, Brickley SG, Wisden W, Ma Y ZZ. 2015. Wakefulness Is governed by GABA and histamine cotransmission. Neuron 87:164-178. doi: 10.1016/j.neuron.2015.06.003, PMID: 26094607