Sevoflurane Induces Coherent Slow-Delta Oscillations in Rats
Jennifer A Guidera, Norman E Taylor, Justin T Lee, Ksenia Y Vlasov, JunZhu Pei, Emily P Stephen, J Patrick Mayo, Emery N Brown, Ken Solt, Jennifer A Guidera, Norman E Taylor, Justin T Lee, Ksenia Y Vlasov, JunZhu Pei, Emily P Stephen, J Patrick Mayo, Emery N Brown, Ken Solt
Abstract
Although general anesthetics are routinely administered to surgical patients to induce loss of consciousness, the mechanisms underlying anesthetic-induced unconsciousness are not fully understood. In rats, we characterized changes in the extradural EEG and intracranial local field potentials (LFPs) within the prefrontal cortex (PFC), parietal cortex (PC), and central thalamus (CT) in response to progressively higher doses of the inhaled anesthetic sevoflurane. During induction with a low dose of sevoflurane, beta/low gamma (12-40 Hz) power increased in the frontal EEG and PFC, PC and CT LFPs, and PFC-CT and PFC-PFC LFP beta/low gamma coherence increased. Loss of movement (LOM) coincided with an abrupt decrease in beta/low gamma PFC-CT LFP coherence. Following LOM, cortically coherent slow-delta (0.1-4 Hz) oscillations were observed in the frontal EEG and PFC, PC and CT LFPs. At higher doses of sevoflurane sufficient to induce loss of the righting reflex, coherent slow-delta oscillations were dominant in the frontal EEG and PFC, PC and CT LFPs. Dynamics similar to those observed during induction were observed as animals emerged from sevoflurane anesthesia. We conclude that the rat is a useful animal model for sevoflurane-induced EEG oscillations in humans, and that coherent slow-delta oscillations are a correlate of sevoflurane-induced behavioral arrest and loss of righting in rats.
Keywords: EEG; anesthesia; coherence; rat; sevoflurane.
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References
- Akeju O., Westover M. B., Pavone K. J., Sampson A. L., Hartnack K. E., Brown E. N., et al. (2014). Effects of sevoflurane and propofol on frontal electroencephalogram power and coherence. Anesthesiology 121 990–998. 10.1097/ALN.0000000000000436
- Alkire M. T., Asher C. D., Franciscus A. M., Hahn E. L. (2009). Thalamic microinfusion of antibody to a voltage-gated potassium channel restores consciousness during anesthesia. Anesthesiology 110 766–773. 10.1097/ALN.0b013e31819c461c
- Alonso L. M., Proekt A., Schwartz T. H., Pryor K. O., Cecchi G. A., Magnasco M. O. (2014). Dynamical criticality during induction of anesthesia in human ECoG recordings. Front. Neural Circuits 8:20 10.3389/fncir.2014.00020
- Baker R., Gent T. C., Yang Q., Parker S., Vyssotski A. L., Wisden W., et al. (2014). Altered activity in the central medial thalamus precedes changes in the neocortex during transitions into both sleep and propofol anesthesia. J. Neurosci. 34 13326–13335. 10.1523/JNEUROSCI.1519-14.2014
- Blain-Moraes S., Tarnal V., Vanini G., Alexander A., Rosen D., Shortal B., et al. (2015). Neurophysiological correlates of sevoflurane-induced unconsciousness. Anesthesiology 122 307–316. 10.1097/ALN.0000000000000482
- Brown E. N., Lydic R., Schiff N. D. (2010). General anesthesia, sleep, and coma. N. Engl. J. Med. 363 2638–2650. 10.1056/NEJMra0808281
- Brown E. N., Purdon P. L., Van Dort C. J. (2011). General anesthesia and altered states of arousal: a systems neuroscience analysis. Annu. Rev. Neurosci. 34 601–628. 10.1146/annurev-neuro-060909-153200
- Chander D., García P. S., MacColl J. N., Illing S., Sleigh J. W. (2014). Electroencephalographic variation during end maintenance and emergence from surgical anesthesia. PLoS ONE 9:e106291 10.1371/journal.pone.0106291
- Chauvette S., Crochet S., Volgushev M., Timofeev I. (2011). Properties of slow oscillation during slow-wave sleep and anesthesia in cats. J. Neurosci. 31 14998–15008. 10.1523/JNEUROSCI.2339-11.2011
- Ching S., Cimenser A., Purdon P. L., Brown E. N., Kopell N. J. (2010). Thalamocortical model for a propofol-induced α-rhythm associated with loss of consciousness. Proc. Natl. Acad. Sci. U.S.A. 107 22665–22670. 10.1073/pnas.1017069108
- Cohen M. X. (2014). Analyzing Neural Time Series Data: Theory and Practice (Issues in Clinical and Cognitive Neuropsychology). Cambridge, MA: MIT Press.
- Eckenhoff R. G. (2001). Promiscuous ligands and attractive cavities: how do the inhaled anesthetics work? Mol. Interv. 1 258–268.
- Eger E. I., II, Koblin D. D., Harris R. A., Kendig J. J., Pohorille A., Halsey M. J., et al. (1997). Hypothesis: inhaled anesthetics produce immobility and amnesia by different mechanisms at different sites. Anesth. Analg. 84 915–918.
- Franks N. P. (2006). Molecular targets underlying general anaesthesia. Br. J. Pharmacol. 147(Suppl. 1) S72–S81.
- Franks N. P. (2008). General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci. 9 370–386. 10.1038/nrn2372
- Friedman E. B., Sun Y., Moore J. T., Hung H. T., Meng Q. C., Perera P., et al. (2010). A conserved behavioral state barrier impedes transitions between anesthetic-induced unconsciousness and wakefulness: evidence for neural inertia. PLoS ONE 5:e11903 10.1371/journal.pone.0011903
- Grasshoff C., Rudolph U., Antkowiak B. (2005). Molecular and systemic mechanisms of general anaesthesia: the ‘multi-site and multiple mechanisms’ concept. Curr. Opin. Anaesthesiol. 18 386–391.
- Gugino L. D., Chabot R. J., Prichep L. S., John E. R., Formanek V., Aglio L. S. (2001). Quantitative EEG changes associated with loss and return of consciousness in healthy adult volunteers anaesthetized with propofol or sevoflurane. Br. J. Anaesth. 87 421–428. 10.1093/bja/87.3.421
- Hemmings H. C., Jr., Akabas M. H., Goldstein P. A., Trudell J. R., Orser B. A., Harrison N. L. (2005). Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol. Sci. 26 503–510.
- Hight D. F., Dadok V. M., Szeri A. J., García P. S., Voss L., Sleigh J. W. (2014). Emergence from general anesthesia and the sleep-manifold. Front. Syst. Neurosci. 8:146 10.3389/fnsys.2014.00146
- Hudson A. E., Calderon D. P., Pfaff D. W., Proekt A. (2014). Recovery of consciousness is mediated by a network of discrete metastable activity states. Proc. Natl. Acad. Sci. U.S.A. 111 9283–9288. 10.1073/pnas.1408296111
- Ishizawa Y., Ahmed O. J., Patel S. R., Gale J. T., Sierra-Mercado D., Brown E. N., et al. (2016). Dynamics of propofol-induced loss of consciousness across primate neocortex. J. Neurosci. 36 7718–7726. 10.1523/JNEUROSCI.4577-15.2016
- Joiner W. J., Friedman E. B., Hung H.-T., Koh K., Sowcik M., Sehgal A., et al. (2013). Genetic and anatomical basis of the barrier separating wakefulness and anesthetic-induced unresponsiveness. PLoS Genet. 9:e1003605 10.1371/journal.pgen.1003605
- Kafashan M., Ching S., Palanca B. J. A. (2016). Sevoflurane alters spatiotemporal functional connectivity motifs that link resting-state networks during wakefulness. Front. Neural Circuits 10:107 10.3389/fncir.2016.00107
- Kajikawa Y., Schroeder C. E. (2011). How local is the local field potential? Neuron 72 847–858. 10.1016/j.neuron.2011.09.029
- Kashimoto S., Furuya A., Nonaka A., Oguchi T., Koshimizu M., Kumazawa T. (2006). The minimum alveolar concentration of sevoflurane in rats. Eur. J. Anaesthesiol. 14 359–361. 10.1046/j.1365-2346.1997.00092.x
- Kenny J., Chemali J., Cotten J., Md P., Van Dort C., Kim S.-E., et al. (2016). Physostigmine and methylphenidate induce distinct arousal states during isoflurane general anesthesia in rats. Anesth. Analg. 123 1210–1219.
- Ku S.-W., Lee U., Noh G.-J., Jun I.-G., Mashour G. A. (2011). Preferential inhibition of frontal-to-parietal feedback connectivity is a neurophysiologic correlate of general anesthesia in surgical patients. PLoS ONE 6:e25155 10.1371/journal.pone.0025155
- Lewis L. D., Weiner V. S., Mukamel E. A., Donoghue J. A., Eskandar E. N., Madsen J. R., et al. (2012). Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proc. Natl. Acad. Sci. U.S.A. 109 E3377–E3386. 10.1073/pnas.1210907109
- Lindén H., Tetzlaff T., Potjans C. T., Klas Pettersen H., Grün S., Diesmann M., et al. (2011). Modeling the spatial reach of the LFP. Neuron 72 859–872. 10.1016/j.neuron.2011.11.006
- Lioudyno M. I., Birch A. M., Tanaka B. S., Sokolov Y., Goldin A. L., Chandy K. G., et al. (2013). Shaker-related potassium channels in the central medial nucleus of the thalamus are important molecular targets for arousal suppression by volatile general anesthetics. J. Neurosci. 33 16310–16322. 10.1523/JNEUROSCI.0344-13.2013
- Mashour G. A., Alkire M. T. (2013). Consciousness, anesthesia, and the thalamocortical system. Anesthesiology 118 13–15. 10.1097/ALN.0b013e318277a9c6
- McCarthy M. M., Brown E. N., Kopell N. (2008). Potential network mechanisms mediating electroencephalographic beta rhythm changes during propofol-induced paradoxical excitation. J. Neurosci. 28 13488–13504. 10.1523/JNEUROSCI.3536-08.2008
- Mitra P., Bokil H. (2008). Observed Brain Dynamics. New York, NY: Oxford University Press.
- Palanca B. J. A., Mitra A., Larson-Prior L., Snyder A. Z., Avidan M. S., Raichle M. E. (2015). Resting-state functional magnetic resonance imaging correlates of sevoflurane-induced unconsciousness. Anesthesiology 123 346–356. 10.1097/ALN.0000000000000731
- Paxinos G., Watson C. (2005). The Rat Brain in Stereotaxic Coordinates. Amsterdam: Elsevier Academic Press.
- Pilge S., Jordan D., Kreuzer M., Kochs E. F., Schneider G. (2014). Burst suppression-MAC and burst suppression-CP50 as measures of cerebral effects of anaesthetics. Br. J. Anaesth. 112 1067–1074. 10.1093/bja/aeu016
- Purdon P. L., Pierce E. T., Mukamel E. A., Prerau M. J., Walsh J. L., Wong K. F. K., et al. (2013). Electroencephalogram signatures of loss and recovery of consciousness from propofol. Proc. Natl. Acad. Sci. U.S.A. 110 E1142–E1151. 10.1073/pnas.1221180110
- Purdon P. L., Sampson A., Pavone K. J., Brown E. N. (2015). Clinical electroencephalography for anesthesiologists: part I: background and basic signatures. Anesthesiology 123 937–960. 10.1097/ALN.0000000000000841
- Rudolph U., Antkowiak B. (2004). Molecular and neuronal substrates for general anaesthetics. Nat. Rev. Neurosci. 5 709–720. 10.1038/nrn1496
- Schiff N. D. (2008). Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann. N. Y. Acad. Sci. 1129 105–118. 10.1196/annals.1417.029
- Silva A., Cardoso-Cruz H., Silva F., Galhardo V., Antunes L. (2010). Comparison of anesthetic depth indexes based on thalamocortical local field potentials in rats. Anesthesiology 112 355–363. 10.1097/ALN.0b013e3181ca3196
- Steriade M., McCormick D. A., Sejnowski T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science 262 679–685.
- Tononi G. (2008). Consciousness as integrated information: a provisional manifesto. Biol. Bull. 215 216–242. 10.2307/25470707
- Vanderwolf C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26 407–418. 10.1016/0013-4694(69)90092-3
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