Arousal transitions in sleep, wakefulness, and anesthesia are characterized by an orderly sequence of cortical events

NeuroImage

Volumn 116, Issue , 2015, Pages 222-231

  Liu, Xiao ^a   Yanagawa, Toru ^b   Leopold, David A ^c   Chang, Catie ^a   Ishida, Hiroaki ^d   Fujii, Naotaka ^b   Duyn, Jeff H ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Alpha inhibitory gating; Consciousness; Feedback process; Propofol anesthesia; Resting state global signal; Sleep

Indexed keywords

PROPOFOL; INTRAVENOUS ANESTHETIC AGENT;

ADULT; ANESTHESIA; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; EVOKED CORTICAL RESPONSE; FEEDBACK SYSTEM; FREQUENCY MODULATION; MACACA; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SLEEP; UNCONSCIOUSNESS; WAKEFULNESS; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; ELECTROENCEPHALOGRAM; PHYSIOLOGY; RHESUS MONKEY;

ANESTHETICS, INTRAVENOUS; ANIMALS; AROUSAL; BRAIN WAVES; CEREBRAL CORTEX; ELECTROCORTICOGRAPHY; MACACA MULATTA; PROPOFOL; SLEEP; WAKEFULNESS;

EID: 84954197529     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.04.003     Document Type: Article

References (76)

1. Aeschbach D., Borbely A.A. All-night dynamics of the human sleep EEG. J. Sleep Res. 1993, 2:70-81.
2. Alkire M.T., Hudetz A.G., Tononi G. Consciousness and anesthesia. Science 2008, 322:876-880.
3. Bastos A.M., Usrey W.M., Adams R.A., Mangun G.R., Fries P., Friston K.J. Canonical microcircuits for predictive coding. Neuron 2012, 76:695-711.
4. Beltramo R., D'Urso G., Dal Maschio M., Farisello P., Bovetti S., Clovis Y., Lassi G., Tucci V., De Pietri Tonelli D., Fellin T. Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat. Neurosci. 2013, 16:227-234.
5. Bianciardi M., Fukunaga M., van Gelderen P., Horovitz S.G., de Zwart J.A., Duyn J.H. Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. NeuroImage 2009, 45:160-168.
6. Boly M., Moran R., Murphy M., Boveroux P., Bruno M.A., Noirhomme Q., Ledoux D., Bonhomme V., Brichant J.F., Tononi G., Laureys S., Friston K. Connectivity changes underlying spectral EEG changes during propofol-induced loss of consciousness. J. Neurosci. Off. J. Soc. Neurosci. 2012, 32:7082-7090.
7. Buffalo E.A., Fries P., Landman R., Buschman T.J., Desimone R. Laminar differences in gamma and alpha coherence in the ventral stream. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11262-11267.
8. Buschman T.J., Miller E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 2007, 315:1860-1862.
9. Chauvette S., Volgushev M., Timofeev I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 2010, 20:2660-2674.
10. Davis H., Davis P.A., Loomis A.L., Harvey E.N., Hobart G. Changes in human brain potentials during the onset of sleep. Science 1937, 86:448-450.
11. Detari L., Juhasz G., Kukorelli T. Firing properties of cat basal forebrain neurones during sleep-wakefulness cycle. Electroencephalogr. Clin. Neurophysiol. 1984, 58:362-368.
12. Dijk D.J., Hayes B., Czeisler C.A. Dynamics of electroencephalographic sleep spindles and slow wave activity in men: effect of sleep deprivation. Brain Res. 1993, 626:190-199.
13. Engel A.K., Fries P. Beta-band oscillations-signalling the status quo?. Curr. Opin. Neurobiol. 2010, 20:156-165.
14. Fukunaga M., Horovitz S.G., van Gelderen P., de Zwart J.A., Jansma J.M., Ikonomidou V.N., Chu R., Deckers R.H., Leopold D.A., Duyn J.H. Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. Magn. Reson. Imaging 2006, 24:979-992.
15. Greicius M.D., Kiviniemi V., Tervonen O., Vainionpaa V., Alahuhta S., Reiss A.L., Menon V. Persistent default-mode network connectivity during light sedation. Hum. Brain Mapp. 2008, 29:839-847.
16. Halasz P., Terzano M., Parrino L., Bodizs R. The nature of arousal in sleep. J. Sleep Res. 2004, 13:1-23.
17. Horovitz S.G., Fukunaga M., de Zwart J.A., van Gelderen P., Fulton S.C., Balkin T.J., Duyn J.H. Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum. Brain Mapp. 2008, 29:671-682.
18. Imas O.A., Ropella K.M., Ward B.D., Wood J.D., Hudetz A.G. Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat. Neurosci. Lett. 2005, 387:145-150.
19. Jao T., Vertes P.E., Alexander-Bloch A.F., Tang I.N., Yu Y.C., Chen J.H., Bullmore E.T. Volitional eyes opening perturbs brain dynamics and functional connectivity regardless of light input. NeuroImage 2013, 69:21-34.
20. Jensen O., Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci. 2010, 4:186.
21. Jerbi K., Freyermuth S., Dalal S., Kahane P., Bertrand O., Berthoz A., Lachaux J.P. Saccade related gamma-band activity in intracerebral EEG: dissociating neural from ocular muscle activity. Brain Topogr. 2009, 22:18-23.
22. Jordan D., Ilg R., Riedl V., Schorer A., Grimberg S., Neufang S., Omerovic A., Berger S., Untergehrer G., Preibisch C., Schulz E., Schuster T., Schroter M., Spoormaker V., Zimmer C., Hemmer B., Wohlschlager A., Kochs E.F., Schneider G. Simultaneous electroencephalographic and functional magnetic resonance imaging indicate impaired cortical top-down processing in association with anesthetic-induced unconsciousness. Anesthesiology 2013, 119:1031-1042.
23. Kiviniemi V.J., Haanpaa H., Kantola J.H., Jauhiainen J., Vainionpaa V., Alahuhta S., Tervonen O. Midazolam sedation increases fluctuation and synchrony of the resting brain BOLD signal. Magn. Reson. Imaging 2005, 23:531-537.
24. Klimesch W., Sauseng P., Hanslmayr S. EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res. Rev. 2007, 53:63-88.
25. Ku S.W., Lee U., Noh G.J., Jun I.G., Mashour G.A. Preferential inhibition of frontal-to-parietal feedback connectivity is a neurophysiologic correlate of general anesthesia in surgical patients. PLoS ONE 2011, 6. (e25155).
26. Larson-Prior L.J., Zempel J.M., Nolan T.S., Prior F.W., Snyder A.Z., Raichle M.E. Cortical network functional connectivity in the descent to sleep. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4489-4494.
27. Lee M.G., Hassani O.K., Alonso A., Jones B.E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. Off. J. Soc. Neurosci. 2005, 25:4365-4369.
28. Lee U., Ku S., Noh G., Baek S., Choi B., Mashour G.A. Disruption of frontal-parietal communication by ketamine, propofol, and sevoflurane. Anesthesiology 2013, 118:1264-1275.
29. Lewis L.D., Weiner V.S., Mukamel E.A., Donoghue J.A., Eskandar E.N., Madsen J.R., Anderson W.S., Hochberg L.R., Cash S.S., Brown E.N., Purdon P.L. Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E3377-E3386.
30. Licata S.C., Nickerson L.D., Lowen S.B., Trksak G.H., Maclean R.R., Lukas S.E. The hypnotic zolpidem increases the synchrony of BOLD signal fluctuations in widespread brain networks during a resting paradigm. NeuroImage 2013, 70:211-222.
31. Liu X., Duyn J.H. Time-varying functional network information extracted from brief instances of spontaneous brain activity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4392-4397.
32. Liu X., Duyn J.H. Resting-state fMRI signal anti-correlation exists in absence of global signal regression. Proceedings of 21st ISMRM Annual Meeting, Salt Lake City, Utah, USA 2013, 2251.
33. Liu X., Chang C., Duyn J.H. Decomposition of spontaneous brain activity into distinct fMRI co-activation patterns. Front. Syst. Neurosci. 2013, 7.
34. Liu X., Yanagawa T., Leopold D.A., Fujii N., Duyn J.H. Robust long-range coordination of spontaneous neural activity in waking, sleep and anesthesia. Cereb. Cortex 2014, [Epub ahead of print].
35. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
36. Magoun H.W. An ascending reticular activating system in the brain stem. A.M.A. Arch. Neurol. Psychiatry 1952, 67:145-154.
37. Maier A., Wilke M., Aura C., Zhu C., Ye F.Q., Leopold D.A. Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat. Neurosci. 2008, 11:1193-1200.
38. Maier A., Adams G.K., Aura C., Leopold D.A. Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front. Syst. Neurosci. 2010, 4.
39. Mann K., Backer P., Roschke J. Dynamical properties of the sleep EEG in different frequency bands. Int. J. Neurosci. 1993, 73:161-169.
40. Massimini M., Ferrarelli F., Esser S.K., Riedner B.A., Huber R., Murphy M., Peterson M.J., Tononi G. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8496-8501.
41. Meeren H.K., Van Luijtelaar E.L., Coenen A.M. Cortical and thalamic visual evoked potentials during sleep-wake states and spike-wave discharges in the rat. Electroencephalogr. Clin. Neurophysiol. 1998, 108:306-319.
42. Merica H., Fortune R.D., Gaillard J.M. Hemispheric temporal organization during the onset of sleep in normal subjects. Phasic events and dynamic organization of sleep 1991, 7:73-84. Raven Press, New York.
43. Merker B. Cortical gamma oscillations: the functional key is activation, not cognition. Neurosci. Biobehav. Rev. 2013, 37:401-417.
44. Mitra P., Bokil H. Observed Brain Dynamics 2008, Oxford University Press, New York.
45. Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1949, 1:455-473.
46. Murphy M., Bruno M.A., Riedner B.A., Boveroux P., Noirhomme Q., Landsness E.C., Brichant J.F., Phillips C., Massimini M., Laureys S., Tononi G., Boly M. Propofol anesthesia and sleep: a high-density EEG study. Sleep 2011, 34:283A-291A.
47. Nagasaka Y., Shimoda K., Fujii N. Multidimensional recording (MDR) and data sharing: an ecological open research and educational platform for neuroscience. PLoS ONE 2011, 6. (e22561).
48. Olbrich S., Mulert C., Karch S., Trenner M., Leicht G., Pogarell O., Hegerl U. EEG-vigilance and BOLD effect during simultaneous EEG/fMRI measurement. NeuroImage 2009, 45:319-332.
49. Ornitz E.M., Ritvo E.R., Carr E.M., La Franchi S., Walter R.D. The effect of sleep onset on the auditory averaged evoked response. Electroencephalogr. Clin. Neurophysiol. 1967, 23:335-341.
50. Oswal A., Brown P., Litvak V. Movement related dynamics of subthalmo-cortical alpha connectivity in Parkinson's disease. NeuroImage 2013, 70:132-142.
51. Palva S., Palva J.M. New vistas for alpha-frequency band oscillations. Trends Neurosci. 2007, 30:150-158.
52. Petridou N., Gaudes C.C., Dryden I.L., Francis S.T., Gowland P.A. Periods of rest in fMRI contain individual spontaneous events which are related to slowly fluctuating spontaneous activity. Hum. Brain Mapp. 2013, 34:1319-1329.
53. Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 1999, 110:1842-1857.
54. Sanchez-Vives M.V., McCormick D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 2000, 3:1027-1034.
55. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437:1257-1263.
56. Saper C.B., Fuller P.M., Pedersen N.P., Lu J., Scammell T.E. Sleep state switching. Neuron 2010, 68:1023-1042.
57. Scholvinck M.L., Maier A., Ye F.Q., Duyn J.H., Leopold D.A. Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10238-10243.
58. Sedley W., Cunningham M.O. Do cortical gamma oscillations promote or suppress perception? An under-asked question with an over-assumed answer. Front. Hum. Neurosci. 2013, 7:595.
59. Sherin J.E., Shiromani P.J., McCarley R.W., Saper C.B. Activation of ventrolateral preoptic neurons during sleep. Science 1996, 271:216-219.
60. Steenland H.W. Staying awake: top-down systems control of sleep. OA Neurosci. 2014, 2:1-14.
61. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006, 137:1087-1106.
62. Szymusiak R., McGinty D. Sleep-related neuronal discharge in the basal forebrain of cats. Brain Res. 1986, 370:82-92.
63. Tagliazucchi E., Balenzuela P., Fraiman D., Chialvo D.R. Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. Front. Physiol. 2012, 3:15.
64. Takahashi K., Lin J.S., Sakai K. Characterization and mapping of sleep-waking specific neurons in the basal forebrain and preoptic hypothalamus in mice. Neuroscience 2009, 161:269-292.
65. Takahashi K., Kayama Y., Lin J.S., Sakai K. Locus coeruleus neuronal activity during the sleep-waking cycle in mice. Neuroscience 2010, 169:1115-1126.
66. Terzano M.G., Parrino L. Origin and significance of the cyclic alternating pattern (CAP). Review article. Sleep Med. Rev. 2000, 4:101-123.
67. Thomson D.J. Spectrum estimation and harmonic analysis. Proc. IEEE 1982, 70:1055-1096.
68. Tinker J.H., Sharbrough F.W., Michenfelder J.D. Anterior shift of the dominant EEG rhytham during anesthesia in the Java monkey: correlation with anesthetic potency. Anesthesiology 1977, 46:252-259.
69. Uchida S., Maloney T., March J.D., Azari R., Feinberg I. Sigma (12-15Hz) and delta (0.3-3Hz) EEG oscillate reciprocally within NREM sleep. Brain Res. Bull. 1991, 27:93-96.
70. Uchida S., Maloney T., Feinberg I. Beta (20-28Hz) and delta (0.3-3Hz) EEGs oscillate reciprocally across NREM and REM sleep. Sleep 1992, 15:352-358.
71. van Kerkoerle T., Self M.W., Dagnino B., Gariel-Mathis M.A., Poort J., van der Togt C., Roelfsema P.R. Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:14332-14341.
72. Vassalli A., Dellepiane J.M., Emmenegger Y., Jimenez S., Vandi S., Plazzi G., Franken P., Tafti M. Electroencephalogram paroxysmal theta characterizes cataplexy in mice and children. Brain J. Neurol. 2013, 136:1592-1608.
73. Vijayan S., Ching S., Purdon P.L., Brown E.N., Kopell N.J. Thalamocortical mechanisms for the anteriorization of alpha rhythms during propofol-induced unconsciousness. J. Neurosci. 2013, 33:11070-11075.
74. von Stein A., Chiang C., Konig P. Top-down processing mediated by interareal synchronization. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14748-14753.
75. Wong C.W., Olafsson V., Tal O., Liu T.T. The amplitude of the resting-state fMRI global signal is related to EEG vigilance measures. NeuroImage 2013, 83:983-990.
76. Yanagawa T., Chao Z.C., Hasegawa N., Fujii N. Large-scale information flow in conscious and unconscious states: an ECoG study in monkeys. PLoS ONE 2013, 8. (e80845).