Multiphasic modification of intrinsic functional connectivity of the rat brain during increasing levels of propofol

NeuroImage

Volumn 83, Issue , 2013, Pages 581-592

  Liu, Xiping ^a   Pillay, Siveshigan ^a   Li, Rupeng ^a   Vizuete, Jeannette A ^a,b   Pechman, Kimberly R ^a   Schmainda, Kathleen M ^a   Hudetz, Anthony G ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Marquette University   (United States)

Author keywords

Consciousness; Functional connectivity; Propofol anesthesia; Resting state; Simultaneous fMRI and EEG

Indexed keywords

PROPOFOL;

ANESTHESIA LEVEL; ANIMAL EXPERIMENT; ARTICLE; BOLD SIGNAL; BRAIN CORTEX; BRAIN FUNCTION; BRAIN FUNCTIONAL CONNECTIVITY; CONNECTOME; DOSE RESPONSE; DRUG DOSE INCREASE; ELECTROENCEPHALOGRAPHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MALE; NEUROANATOMY; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; RAT; RESTING STATE NETWORK; SEDATION; SUBCORTEX;

CONSCIOUSNESS; FUNCTIONAL CONNECTIVITY; PROPOFOL ANESTHESIA; RESTING STATE; SIMULTANEOUS FMRI AND EEG;

ANESTHETICS, INTRAVENOUS; ANIMALS; BRAIN; CLUSTER ANALYSIS; ELECTROENCEPHALOGRAPHY; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PROPOFOL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84881262584     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.07.003     Document Type: Article

References (109)

1. Alkire M.T., Haier R.J., Barker S.J., Shah N.K., Wu J.C., Kao Y.J. Cerebral metabolism during propofol anesthesia in humans studied with positron emission tomography. Anesthesiology 1995, 82:393-403. (discussion 327A).
2. Alkire M.T., Pomfrett C.J., Haier R.J., Gianzero M.V., Chan C.M., Jacobsen B.P., Fallon J.H. Functional brain imaging during anesthesia in humans: effects of halothane on global and regional cerebral glucose metabolism. Anesthesiology 1999, 90:701-709.
3. Alkire M.T., Haier R.J., Fallon J.H. Toward a unified theory of narcosis: brain imaging evidence for a thalamocortical switch as the neurophysiologic basis of anesthetic-induced unconsciousness. Conscious. Cogn. 2000, 9:370-386.
4. Alkire M.T., McReynolds J.R., Hahn E.L., Trivedi A.N. Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat. Anesthesiology 2007, 107:264-272.
5. Alkire M., Hudetz A., Tononi G. Consciousness and anesthesia. Science 2008, 322:876-880.
6. Amzica F. Basic physiology of burst-suppression. Epilepsia 2009, 50(Suppl. 12):38-39.
7. Antognini J.F., Atherley R.J., Dutton R.C., Laster M.J., Eger E.I., Carstens E. The excitatory and inhibitory effects of nitrous oxide on spinal neuronal responses to noxious stimulation. Anesth. Analg. 2007, 104:829-835.
8. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Imaging 1995, 34:537-541.
9. Boly M. Measuring the fading consciousness in the human brain. Curr. Opin. Neurol. 2011, 24:394-400.
10. Boly M., Massimini M., Garrido M.I., Gosseries O., Noirhomme Q., Laureys S., Soddu A. Brain connectivity in disorders of consciousness. Brain Connect. 2012, 2:1-10.
11. 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. 2012, 32:7082-7090.
12. Boveroux P., Vanhaudenhuyse A., Bruno M.A., Noirhomme Q., Lauwick S., Luxen A., Degueldre C., Plenevaux A., Schnakers C., Phillips C., Brichant J.F., Bonhomme V., Maquet P., Greicius M.D., Laureys S., Boly M. Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 2010, 113:1038-1053.
13. Brammer A., West C.D., Allen S.L. A comparison of propofol with other injectable anaesthetics in a rat model for measuring cardiovascular parameters. Lab. Anim. 1993, 27:250-257.
14. Cavazzuti M., Porro C.A., Barbieri A., Galetti A. Brain and spinal cord metabolic activity during propofol anaesthesia. Br. J. Anaesth. 1991, 66:490-495.
15. Chen G., Chen G., Xie C., Ward B.D., Li W., Antuono P., Li S.J. A method to determine the necessity for global signal regression in resting-state fMRI studies. Magn. Reson. Med. 2012, 68:1828-1835.
16. Cimenser A., Purdon P.L., Pierce E.T., Walsh J.L., Salazar-Gomez A.F., Harrell P.G., Tavares-Stoeckel C., Habeeb K., Brown E.N. Tracking brain states under general anesthesia by using global coherence analysis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8832-8837.
17. Dam M., Ori C., Pizzolato G., Ricchieri G.L., Pellegrini A., Giron G.P., Battistin L. The effects of propofol anesthesia on local cerebral glucose utilization in the rat. Anesthesiology 1990, 73:499-505.
18. Dawson D.A., Cha K., Lewis L.B., Mendola J.D., Shmuel A. Evaluation and calibration of functional network modeling methods based on known anatomical connections. NeuroImage 2012.
19. Dean P. Sensory cortex: visual perceptual functions. The Cerebral Cortex of the Rat 1990, 275-307. MIT Press, Cambridge. B. Kolb, R.C. Tees (Eds.).
20. Devor M., Zalkind V. Reversible analgesia, atonia, and loss of consciousness on bilateral intracerebral microinjection of pentobarbital. Pain 2001, 94:101-112.
21. Duyn J. Spontaneous fMRI activity during resting wakefulness and sleep. Prog. Brain Res. 2011, 193:295-305.
22. Erchova I.A., Lebedev M.A., Diamond M.E. Somatosensory cortical neuronal population activity across states of anaesthesia. Eur. J. Neurosci. 2002, 15:744-752.
23. Ferrarelli F., Massimini M., Sarasso S., Casali A., Riedner B.A., Angelini G., Tononi G., Pearce R.A. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2681-2686.
24. Fiset P., Paus T., Daloze T., Plourde G., Meuret P., Bonhomme V., Hajj-Ali N., Backman S.B., Evans A.C. Brain mechanisms of propofol-induced loss of consciousness in humans: a positron emission tomographic study. J. Neurosci. 1999, 19:5506-5513.
25. Fiset P., Plourde G., Backman S.B. Brain imaging in research on anesthetic mechanisms: studies with propofol. Prog. Brain Res. 2005, 150:245-250.
26. Franceschini M.A., Radhakrishnan H., Thakur K., Wu W., Ruvinskaya S., Carp S., Boas D.A. The effect of different anesthetics on neurovascular coupling. NeuroImage 2010, 51:1367-1377.
27. Franks N.P. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci. 2008, 9:370-386.
28. Gusnard D.A., Raichle M.E. Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2001, 2:685-694.
29. Heine L., Soddu A., Gomez F., Vanhaudenhuyse A., Tshibanda L., Thonnard M., Charland-Verville V., Kirsch M., Laureys S., Demertzi A. Resting state networks and consciousness: alterations of multiple resting state network connectivity in physiological, pharmacological, and pathological consciousness states. Front. Psychol. 2012, 3:295.
30. Hill N.J., Gupta D., Brunner P., Gunduz A., Adamo M.A., Ritaccio A., Schalk G. Recording human electrocorticographic (ECoG) signals for neuroscientific research and real-time functional cortical mapping. J. Vis. Exp. 2012.
31. Hudetz A.G. Feedback suppression in anesthesia. Is it reversible?. Conscious. Cogn. 2009, 18:1079-1081.
32. Hudetz A.G. General anesthesia and human brain connectivity. Brain Connect. 2012.
33. Hudetz A.G., Imas O.A. Burst activation of the cerebral cortex by flash stimuli during isoflurane anesthesia in rats. Anesthesiology 2007, 107:983-991.
34. Suppressing the Mind: Anesthetic Modulation of Memory and Consciousness 2009, Humana Press, New York. 1st ed. A.G. Hudetz, R.A. Pearce (Eds.).
35. Hudetz A.G., Vizuete J.A., Imas O.A. Desflurane selectively suppresses long-latency cortical neuronal response to flash in the rat. Anesthesiology 2009, 111:231-239.
36. Hutchison R.M., Mirsattari S.M., Jones C.K., Gati J.S., Leung L.S. Functional networks in the anesthetized rat brain revealed by independent component analysis of resting-state FMRI. J. Neurophysiol. 2010, 103:3398-3406.
37. Imas O.A., Ropella K.M., Ward B.D., Wood J.D., Hudetz A.G. Volatile anesthetics enhance flash-induced gamma oscillations in rat visual cortex. Anesthesiology 2005, 102:937-947.
38. Jones B. Arousal systems. Front. Biosci. 2003, 8:s438-s451.
39. Jugovac I., Imas O., Hudetz A.G. Supraspinal anesthesia: behavioral and electroencephalographic effects of intracerebroventricularly infused pentobarbital, propofol, fentanyl, and midazolam. Anesthesiology 2006, 105:764-778.
40. Kaisti K.K., Langsjo J.W., Aalto S., Oikonen V., Sipila H., Teras M., Hinkka S., Metsahonkala L., Scheinin H. Effects of sevoflurane, propofol, and adjunct nitrous oxide on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 2003, 99:603-613.
41. Kalthoff D., Seehafer J.U., Po C., Wiedermann D., Hoehn M. Functional connectivity in the rat at 11.7T: impact of physiological noise in resting state fMRI. NeuroImage 2011, 54:2828-2839.
42. Kannurpatti S.S., Biswal B.B., Kim Y.R., Rosen B.R. Spatio-temporal characteristics of low-frequency BOLD signal fluctuations in isoflurane-anesthetized rat brain. NeuroImage 2008, 40:1738-1747.
43. Keilholz S., Magnuson M.E., Pan W.J., Willis M., Thompson G. Dynamic properties of functional connectivity in the rodent. Brain Connect. 2012.
44. Kolb B. Posterior parietal and temporal association. The Cerbral Cortex of the Rat 1990, 459-471. MIT Press, Cambridge. B. Kolb, R.C. Tees (Eds.).
45. Kroeger D., Amzica F. Hypersensitivity of the anesthesia-induced comatose brain. J. Neurosci. 2007, 27:10597-10607.
46. Kuizenga K., Wierda J.M., Kalkman C.J. Biphasic EEG changes in relation to loss of consciousness during induction with thiopental, propofol, etomidate, midazolam or sevoflurane. Br. J. Anaesth. 2001, 86:354-360.
47. Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 2005, 9:556-559.
48. Lee J.G., Hudetz A.G., Smith J.J., Hillard C.J., Bosnjak Z.J., Kampine J.P. The effects of halothane and isoflurane on cerebrocortical microcirculation and autoregulation as assessed by laser-Doppler flowmetry. Anesth. Analg. 1994, 79:58-65.
49. Lee U., Kim S., Noh G.J., Choi B.M., Hwang E., Mashour G.A. The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans. Conscious. Cogn. 2009, 18:1069-1078.
50. Lee U., Mashour G.A., Kim S., Noh G.J., Choi B.M. Propofol induction reduces the capacity for neural information integration: implications for the mechanism of consciousness and general anesthesia. Conscious. Cogn. 2009, 18:56-64.
51. Liang Z., King J., Zhang N. Uncovering intrinsic connectional architecture of functional networks in awake rat brain. J. Neurosci. 2011, 31:3776-3783.
52. Liu X., Zhu X.H., Zhang Y., Chen W. Neural origin of spontaneous hemodynamic fluctuations in rats under burst-suppression anesthesia condition. Cereb. Cortex 2011, 21:374-384.
53. Liu X., Lauer K.K., Ward B.D., Rao S.M., Li S.J., Hudetz A.G. Propofol disrupts functional interactions between sensory and high-order processing of auditory verbal memory. Hum. Brain Mapp. 2012, 33:2487-2498.
54. Liu X., Zhu X.H., Zhang Y., Chen W. The change of functional connectivity specificity in rats under various anesthesia levels and its neural origin. Brain Topogr. 2012.
55. Liu J.V., Hirano Y., Nascimento G.C., Stefanovic B., Leopold D.A., Silva A.C. fMRI in the awake marmoset: somatosensory-evoked responses, functional connectivity, and comparison with propofol anesthesia. NeuroImage 2013.
56. Lu H., Zuo Y., Gu H., Waltz J.A., Zhan W., Scholl C.A., Rea W., Yang Y., Stein E.A. Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18265-18269.
57. Lu J., Nelson L.E., Franks N., Maze M., Chamberlin N.L., Saper C.B. Role of endogenous sleep-wake and analgesic systems in anesthesia. J. Comp. Neurol. 2008, 508:648-662.
58. Lu H., Zou Q., Gu H., Raichle M.E., Stein E.A., Yang Y. Rat brains also have a default mode network. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3979-3984.
59. Ma J., Shen B., Stewart L.S., Herrick I.A., Leung L.S. The septohippocampal system participates in general anesthesia. J. Neurosci. 2002, 22:RC200.
60. Majeed W., Magnuson M., Hasenkamp W., Schwarb H., Schumacher E.H., Barsalou L., Keilholz S.D. Spatiotemporal dynamics of low frequency BOLD fluctuations in rats and humans. NeuroImage 2011, 54:1140-1150.
61. Mankinen K., Long X.Y., Paakki J.J., Harila M., Rytky S., Tervonen O., Nikkinen J., Starck T., Remes J., Rantala H., Zang Y.F., Kiviniemi V. Alterations in regional homogeneity of baseline brain activity in pediatric temporal lobe epilepsy. Brain Res. 2011, 1373:221-229.
62. Mantini D., Gerits A., Nelissen K., Durand J.B., Joly O., Simone L., Sawamura H., Wardak C., Orban G.A., Buckner R.L., Vanduffel W. Default mode of brain function in monkeys. J. Neurosci. 2011, 31:12954-12962.
63. Martuzzi R., Ramani R., Qiu M., Rajeevan N., Constable R.T. Functional connectivity and alterations in baseline brain state in humans. NeuroImage 2010, 49:823-834.
64. Masamoto K., Kanno I. Anesthesia and the quantitative evaluation of neurovascular coupling. J. Cereb. Blood Flow Metab. 2012, 32:1233-1247.
65. Mhuircheartaigh R.N., Rosenorn-Lanng D., Wise R., Jbabdi S., Rogers R., Tracey I. Cortical and subcortical connectivity changes during decreasing levels of consciousness in humans: a functional magnetic resonance imaging study using propofol. J. Neurosci. 2010, 30:9095-9102.
66. Mishra A.M., Ellens D.J., Schridde U., Motelow J.E., Purcaro M.J., DeSalvo M.N., Enev M., Sanganahalli B.G., Hyder F., Blumenfeld H. Where fMRI and electrophysiology agree to disagree: corticothalamic and striatal activity patterns in the WAG/Rij rat. J. Neurosci. 2011, 31:15053-15064.
67. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. NeuroImage 2009, 44:893-905.
68. Nallasamy N., Tsao D.Y. Functional connectivity in the brain: effects of anesthesia. Neuroscientist 2011, 17:94-106.
69. Ogawa S., Lee T.M., Stepnoski R., Chen W., Zhu X.H., Ugurbil K. An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11026-11031.
70. Ogawa K., Uema T., Motohashi N., Nishikawa M., Takano H., Hiroki M., Imabayashi E., Ohnishi T., Inoue T., Takayama Y., Takeda M., Matsuda H., Andoh T., Yamada Y. Neural mechanism of propofol anesthesia in severe depression: a positron emission tomographic study. Anesthesiology 2003, 98:1101-1111.
71. Pan W.J., Thompson G., Magnuson M., Majeed W., Jaeger D., Keilholz S. Broadband local field potentials correlate with spontaneous fluctuations in functional magnetic resonance imaging signals in the rat somatosensory cortex under isoflurane anesthesia. Brain Connect. 2011, 1:119-131.
72. Pawela C.P., Biswal B.B., Cho Y.R., Kao D.S., Li R., Jones S.R., Schulte M.L., Matloub H.S., Hudetz A.G., Hyde J.S. Resting-state functional connectivity of the rat brain. Magn. Reson. Med. 2008, 59:1021-1029.
73. Pawela C.P., Biswal B.B., Hudetz A.G., Schulte M.L., Li R., Jones S.R., Cho Y.R., Matloub H.S., Hyde J.S. A protocol for use of medetomidine anesthesia in rats for extended studies using task-induced BOLD contrast and resting-state functional connectivity. NeuroImage 2009, 46:1137-1147.
74. Pillay S., Vizuete J.A., McCallum J.B., Hudetz A.G. Norepinephrine infusion into nucleus basalis elicits microarousal in desflurane-anesthetized rats. Anesthesiology 2011, 115:733-742.
75. Pincus S.M., Mulligan T., Iranmanesh A., Gheorghiu S., Godschalk M., Veldhuis J.D. Older males secrete luteinizing hormone and testosterone more irregularly, and jointly more asynchronously, than younger males. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14100-14105.
76. Power J.D., Cohen A.L., Nelson S.M., Wig G.S., Barnes K.A., Church J.A., Vogel A.C., Laumann T.O., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional network organization of the human brain. Neuron 2011, 72:665-678.
77. Prielipp R.C., Wall M.H., Tobin J.R., Groban L., Cannon M.A., Fahey F.H., Gage H.D., Stump D.A., James R.L., Bennett J., Butterworth J. Dexmedetomidine-induced sedation in volunteers decreases regional and global cerebral blood flow. Anesth. Analg. 2002, 95:1052-1059. (table of contents).
78. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:676-682.
79. Rampil I.J., King B.S. Volatile anesthetics depress spinal motor neurons. Anesthesiology 1996, 85:129-134.
80. Reiner K., Sukhotinsky I., Devor M. Mesopontine tegmental anesthesia area projects independently to the rostromedial medulla and to the spinal cord. Neuroscience 2007, 146:1355-1370.
81. Saad Z.S., Gotts S.J., Murphy K., Chen G., Jo H.J., Martin A., Cox R.W. Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2012, 2:25-32.
82. Scheeringa R., Petersson K.M., Kleinschmidt A., Jensen O., Bastiaansen M.C. EEG alpha power modulation of FMRI resting-state connectivity. Brain Connect. 2012, 2:254-264.
83. Schiff N.D. Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann. N. Y. Acad. Sci. 2008, 1129:105-118.
84. Schiff N.D., Plum F. The role of arousal and "gating" systems in the neurology of impaired consciousness. J. Clin. Neurophysiol. 2000, 17:438-452.
85. 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.
86. Schroter M.S., Spoormaker V.I., Schorer A., Wohlschlager A., Czisch M., Kochs E.F., Zimmer C., Hemmer B., Schneider G., Jordan D., Ilg R. Spatiotemporal reconfiguration of large-scale brain functional networks during propofol-induced loss of consciousness. J. Neurosci. 2012, 32:12832-12840.
87. Schrouff J., Perlbarg V., Boly M., Marrelec G., Boveroux P., Vanhaudenhuyse A., Bruno M.A., Laureys S., Phillips C., Pelegrini-Issac M., Maquet P., Benali H. Brain functional integration decreases during propofol-induced loss of consciousness. NeuroImage 2011, 57:198-205.
88. Shmuel A., Leopold D.A. Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum. Brain Mapp. 2008, 29:751-761.
89. Silva A., Cardoso-Cruz H., Silva F., Galhardo V., Antunes L. Comparison of anesthetic depth indexes based on thalamocortical local field potentials in rats. Anesthesiology 2010, 112:355-363.
90. Stamatakis E.A., Adapa R.M., Absalom A.R., Menon D.K. Changes in resting neural connectivity during propofol sedation. PLoS One 2010, 5:e14224.
91. Steyn-Ross D.A., Steyn-Ross M.L., Wilcocks L.C., Sleigh J.W. Toward a theory of the general-anesthetic-induced phase transition of the cerebral cortex. II. Numerical simulations, spectral entropy, and correlation times. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2001, 64:011918.
92. Steyn-Ross M.L., Steyn-Ross D.A., Sleigh J.W., Whiting D.R. Theoretical predictions for spatial covariance of the electroencephalographic signal during the anesthetic-induced phase transition: increased correlation length and emergence of spatial self-organization. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2003, 68:021902.
93. Sumiyoshi A., Suzuki H., Ogawa T., Riera J.J., Shimokawa H., Kawashima R. Coupling between gamma oscillation and fMRI signal in the rat somatosensory cortex: its dependence on systemic physiological parameters. NeuroImage 2012, 60:738-746.
94. Tononi G. An information integration theory of consciousness. BMC Neurosci. 2004, 5:42.
95. Tononi G. Information integration: its relevance to brain function and consciousness. Arch. Ital. Biol. 2010, 148:299-322.
96. Tu Y., Yu T., Fu X.Y., Xie P., Lu S., Huang X.Q., Gong Q.Y. Altered thalamocortical functional connectivity by propofol anesthesia in rats. Pharmacology 2011, 88:322-326.
97. Tung A., Szafran M.J., Bluhm B., Mendelson W.B. Sleep deprivation potentiates the onset and duration of loss of righting reflex induced by propofol and isoflurane. Anesthesiology 2002, 97:906-911.
98. Upadhyay J., Baker S.J., Chandran P., Miller L., Lee Y., Marek G.J., Sakoglu U., Chin C.L., Luo F., Fox G.B., Day M. Default-mode-like network activation in awake rodents. PLoS One 2011, 6:e27839.
99. Veselis R.A. Anesthesia-a descent or a jump into the depths?. Conscious. Cogn. 2001, 10:230-235. (discussion 246-258).
100. Veselis R.A., Reinsel R.A., Feshchenko V.A., Wronski M. The comparative amnestic effects of midazolam, propofol, thiopental, and fentanyl at equisedative concentrations. Anesthesiology 1997, 87:749-764.
101. Veselis R.A., Reinsel R.A., Feshchenko V.A. Drug-induced amnesia is a separate phenomenon from sedation: electrophysiologic evidence. Anesthesiology 2001, 95:896-907.
102. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447:83-86.
103. Vincent J.L., Kahn I., Snyder A.Z., Raichle M.E., Buckner R.L. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J. Neurophysiol. 2008, 100:3328-3342.
104. Wang K., van Meer M.P., van der Marel K., van der Toorn A., Xu L., Liu Y., Viergever M.A., Jiang T., Dijkhuizen R.M. Temporal scaling properties and spatial synchronization of spontaneous blood oxygenation level-dependent (BOLD) signal fluctuations in rat sensorimotor network at different levels of isoflurane anesthesia. NMR Biomed. 2011, 24:61-67.
105. Williams K.A., Magnuson M., Majeed W., LaConte S.M., Peltier S.J., Hu X., Keilholz S.D. Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat. Magn. Reson. Imaging 2010, 28:995-1003.
106. Zecharia A., Franks N.P. General anesthesia and ascending arousal pathways. Anesthesiology 2009, 111:695-696.
107. Zhang N., Rane P., Huang W., Liang Z., Kennedy D., Frazier J.A., King J. Mapping resting-state brain networks in conscious animals. J. Neurosci. Methods 2010, 189:186-196.
108. Zhao F., Zhao T., Zhou L., Wu Q., Hu X. BOLD study of stimulation-induced neural activity and resting-state connectivity in medetomidine-sedated rat. NeuroImage 2008, 39:248-260.
109. Zhou Y., Shu N., Liu Y., Song M., Hao Y., Liu H., Yu C., Liu Z., Jiang T. Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr. Res. 2008, 100:120-132.