Anesthesia and the Thalamocortical System

Chapter
Part of the Contemporary Clinical Neuroscience book series (CCNE)

Abstract

Neuroimaging the effect of anesthesia in the human brain reveals that anesthesia suppresses the functioning of the brain both in a global- and regional-specific manner. The suppression of activity generally has a global component to it (i.e., the entire brain seems to shut down), but on top of that a few select regions appear to be more suppressed than the rest of the brain (i.e., some areas appear to be more sensitive to the suppression effects of anesthesia). These regionally sensitive areas include the parietal and frontal cortical regions along with a consistently observed effect that shows a suppression of thalamic activity. It remains unknown as to which of these effects caused by anesthesia are the most important for producing a loss of consciousness. This chapter will discuss some recent findings from anesthesia research that serve to implicate a role for the thalamocortical system in mediating consciousness.

Keywords

Anesthesia arousal awareness central medial thalamus desflurane sevoflurane thalamocortical unconsciousness 

References

  1. Abulafia, R., V. Zalkind, and M. Devor. 2009. Cerebral activity during the anesthesia-like state induced by mesopontine microinjection of pentobarbital. J Neurosci 29(11):7053–7064.CrossRefPubMedGoogle Scholar
  2. Alkire, M. T. 1998. Quantitative EEG correlations with brain glucose metabolic rate during anesthesia in volunteers. Anesthesiology 89(2):323–333.CrossRefPubMedGoogle Scholar
  3. Alkire, M. T., and R. J. Haier. 2001. Correlating in vivo anaesthetic effects with ex vivo receptor density data supports a GABAergic mechanism of action for propofol, but not for isoflurane. Br J Anaesth 86(5):618–626.CrossRefPubMedGoogle Scholar
  4. Alkire, M. T., and J. Miller. 2005. General anesthesia and the neural correlates of consciousness. Prog Brain Res 150:229–244.CrossRefPubMedGoogle Scholar
  5. Alkire, M. T., and S. V. Nathan. 2005. Does the amygdala mediate anesthetic-induced amnesia? Basolateral amygdala lesions block sevoflurane-induced amnesia. Anesthesiology 102(4):754–760.CrossRefPubMedGoogle Scholar
  6. Alkire, M. T., R. J. Haier, and J. H. Fallon. 2000. Toward a unified theory of narcosis: brain imaging evidence for a thalamocortical switch as the neurophysiologic basis of anesthetic-induced unconsciousness. Conscious Cogn 9(3):370–386.CrossRefPubMedGoogle Scholar
  7. Alkire, M. T., A. G. Hudetz, and G. Tononi. 2008. Consciousness and anesthesia. Science 322(5903):876–880.CrossRefPubMedGoogle Scholar
  8. Alkire, M. T., R. J. Haier, S. J. Barker, N. K. Shah, J. C. Wu, and Y. J. Kao. 1995. Cerebral metabolism during propofol anesthesia in humans studied with positron emission tomography. Anesthesiology 82(2):393–403.CrossRefPubMedGoogle Scholar
  9. Alkire, M. T., R. J. Haier, M. V. Gianzero, C. M. Chan, L. M. Smalling, B. P. Jacobsen, and C. T. Anderson. 1997. A positron emission tomography study of human cerebral metabolism during halothane anesthesia. Anesthesiology 87(3):A175.CrossRefGoogle Scholar
  10. Alkire, M. T., R. J. Haier, N. K. Shah, and C. T. Anderson. 1997. Positron emission tomography study of regional cerebral metabolism in humans during isoflurane anesthesia. Anesthesiology 86(3):549–557.CrossRefPubMedGoogle Scholar
  11. Alkire, M. T., J. R. McReynolds, E. L. Hahn, and A. N. Trivedi. 2007. Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat Anesthesiology 107:264–272.CrossRefPubMedGoogle Scholar
  12. Alkire, M. T., R. Gruver, J. Miller, J. R. McReynolds, E. L. Hahn, and L. Cahill. 2008. Neuroimaging analysis of an anesthetic gas that blocks human emotional memory. Proc Natl Acad Sci USA 105(5):1722–1727.CrossRefPubMedGoogle Scholar
  13. Alkire, M. T., C. D. Asher, A. M. Franciscus, and E. L. Hahn. 2009. Thalamic microinfusion of antibody to a voltage-gated potassium channel restores consciousness during anesthesia. Anesthesiology 110(4):766–773.CrossRefPubMedGoogle Scholar
  14. Angel, A. 1991. The G. L. Brown lecture. Adventures in anaesthesia. Exp Physiol 76(1):1–38.PubMedGoogle Scholar
  15. Antkowiak, B. 1999. Different actions of general anesthetics on the firing patterns of neocortical neurons mediated by the GABA(A) receptor. Anesthesiology 91(2):500–511.CrossRefPubMedGoogle Scholar
  16. Arhem, P., G. Klement, and J. Nilsson. 2003. Mechanisms of anesthesia: towards integrating network, cellular, and molecular level modeling. Neuropsychopharmacology 28(Suppl 1):S40–S47.CrossRefPubMedGoogle Scholar
  17. Bogen, J. E. 1997. Some neurophysiologic aspects of consciousness. Semin Neurol 17(2):95–103.CrossRefPubMedGoogle Scholar
  18. Buchsbaum, M. S., J. C. Gillin, J. Wu, E. Hazlett, N. Sicotte, R. M. Dupont, and W. E. Bunney, Jr. 1989. Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sci 45(15):1349–1356.CrossRefPubMedGoogle Scholar
  19. Cirelli, C., D. Bushey, S. Hill, R. Huber, R. Kreber, B. Ganetzky, and G. Tononi. 2005. Reduced sleep in Drosophila Shaker mutants. Nature 434(7037):1087–1092.CrossRefPubMedGoogle Scholar
  20. Desmurget, M., K. T. Reilly, N. Richard, A. Szathmari, C. Mottolese, and A. Sirigu. 2009. Movement intention after parietal cortex stimulation in humans. Science 324(5928):811–813.CrossRefPubMedGoogle Scholar
  21. Detsch, O., C. Vahle-Hinz, E. Kochs, M. Siemers, and B. Bromm. 1999. Isoflurane induces dose-dependent changes of thalamic somatosensory information transfer. Brain Res 829(1–2):77-89.CrossRefPubMedGoogle Scholar
  22. Dong, H. L., S. Fukuda, E. Murata, and T. Higuchi. 2006. Excitatory and inhibitory actions of isoflurane on the cholinergic ascending arousal system of the rat. Anesthesiology 104(1):122–133.CrossRefPubMedGoogle Scholar
  23. Dringenberg, H. C., and M. C. Olmstead. 2003. Integrated contributions of basal forebrain and thalamus to neocortical activation elicited by pedunculopontine tegmental stimulation in urethane-anesthetized rats. Neuroscience 119(3):839–853.CrossRefPubMedGoogle Scholar
  24. Dringenberg, H. C., A. J. Saber, and L. Cahill. 2001. Enhanced frontal cortex activation in rats by convergent amygdaloid and noxious sensory signals. Neuroreport 12(11):2395–2398.CrossRefPubMedGoogle Scholar
  25. Drummond, J. C., and P. Patel. 2000. Cerebral blood flow and metabolism. In Anesthesia, edited by R. D. Miller. New York: Churchill-Livingstone.Google Scholar
  26. Eger, E. I., II, D. M. Fisher, J. P. Dilger, J. M. Sonner, A. Evers, N. P. Franks, R. A. Harris, J. J. Kendig, W. R. Lieb, and T. Yamakura. 2001. Relevant concentrations of inhaled anesthetics for in vitro studies of anesthetic mechanisms. Anesthesiology 94(5):915–921.CrossRefPubMedGoogle Scholar
  27. Fan, J., B. D. McCandliss, J. Fossella, J. I. Flombaum, and M. I. Posner. 2005. The activation of attentional networks. Neuroimage 26(2):471–479.CrossRefPubMedGoogle Scholar
  28. Flood, P., J. Ramirez-Latorre, and L. Role. 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(4):859–865.CrossRefPubMedGoogle Scholar
  29. Franks, N. P. 2008. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9(5):370–386.CrossRefPubMedGoogle Scholar
  30. French, J. D., R. B. Livingston, and R. Hernandez-Peon. 1953. Cortical influences upon the arousal mechanism. Trans Am Neurol Assoc 3(78th Meeting):57–58.PubMedGoogle Scholar
  31. French, J. D., M. Verzeano, and H. W. Magoun. 1953. A neural basis of the anesthetic state. Arch Neurol Psychiatry 69(4):519–529.PubMedGoogle Scholar
  32. Gallezot, J. D., M. Bottlaender, M. C. Gregoire, D. Roumenov, J. R. Deverre, C. Coulon, M. Ottaviani, F. Dolle, A. Syrota, and H. Valette. 2005. In vivo imaging of human cerebral nicotinic acetylcholine receptors with 2-18F-fluoro-A-85380 and PET. J Nucl Med 46(2):240–247.PubMedGoogle Scholar
  33. Hentschke, H., C. Schwarz, and B. Antkowiak. 2005. Neocortex is the major target of sedative concentrations of volatile anaesthetics: strong depression of firing rates and increase of GABAA receptor-mediated inhibition. Eur J Neurosci 21(1):93–102.CrossRefPubMedGoogle Scholar
  34. Hudetz, A.G. 2006. Suppressing consciousness: mechanisms of general anesthesia. Semin Anesthesia Perioperative Med Pain 25:196–204.CrossRefGoogle Scholar
  35. John, E. R., and L. S. Prichep. 2005. The anesthetic cascade: a theory of how anesthesia suppresses consciousness. Anesthesiology 102(2):447–471.CrossRefPubMedGoogle Scholar
  36. Jones, B. E. 2003. Arousal systems. Front Biosci 8:s438–s451.CrossRefPubMedGoogle Scholar
  37. Jung, R. E., and R. J. Haier. 2007. The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30(2):135–154.CrossRefPubMedGoogle Scholar
  38. Keifer, J. C., H. A. Baghdoyan, L. Becker, and R. Lydic. 1994. Halothane decreases pontine acetylcholine release and increases EEG spindles. Neuroreport 5(5):577–580.CrossRefPubMedGoogle Scholar
  39. Kelz, M. B., Y. Sun, J. Chen, Q. Cheng Meng, J. T. Moore, S. C. Veasey, S. Dixon, M. Thornton, H. Funato, and M. Yanagisawa. 2008. An essential role for orexins in emergence from general anesthesia. Proc Natl Acad Sci USA 105(4):1309–1314.CrossRefPubMedGoogle Scholar
  40. Kodaka, M., J. W. Johansen, and P. S. Sebel. 2005. The influence of gender on loss of consciousness with sevoflurane or propofol. Anesth Analg 101(2):377–381.CrossRefPubMedGoogle Scholar
  41. Langsjo, J. W., E. Salmi, K. K. Kaisti, S. Aalto, S. Hinkka, R. Aantaa, V. Oikonen, T. Viljanen, T. Kurki, M. Silvanto, and H. Scheinin. 2004. Effects of subanesthetic ketamine on regional cerebral glucose metabolism in humans. Anesthesiology 100(5):1065–1071.CrossRefPubMedGoogle Scholar
  42. Laureys, S. 2005. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 9(12):556–559.CrossRefPubMedGoogle Scholar
  43. Llinas, R. R., and M. Steriade. 2006. Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95(6):3297–3308.CrossRefPubMedGoogle Scholar
  44. Lydic, R., and H. A. Baghdoyan. 2005. Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103(6):1268–1295.CrossRefPubMedGoogle Scholar
  45. Mashour, G. A. 2004. Consciousness unbound: toward a paradigm of general anesthesia. Anesthesiology 100(2):428–433.CrossRefPubMedGoogle Scholar
  46. Michenfelder, J.D. 1988. Anesthesia and the brain. New York: Churchill-Livingstone.Google Scholar
  47. Miller, J. W., and J. A. Ferrendelli. 1990. Characterization of GABAergic seizure regulation in the midline thalamus. Neuropharmacology 29(7):649–655.CrossRefPubMedGoogle Scholar
  48. Miller, J. W., C. M. Hall, K. D. Holland, and J. A. Ferrendelli. 1989. Identification of a median thalamic system regulating seizures and arousal. Epilepsia 30(4):493–500.CrossRefPubMedGoogle Scholar
  49. Nicoll, R. A., and D. V. Madison. 1982. General anesthetics hyperpolarize neurons in the vertebrate central nervous system. Science 217(4564):1055–1057.CrossRefPubMedGoogle Scholar
  50. Nofzinger, E. A., D. J. Buysse, J. M. Miewald, C. C. Meltzer, J. C. Price, R. C. Sembrat, H. Ombao, C. F. Reynolds, T. H. Monk, M. Hall, D. J. Kupfer, and R. Y. Moore. 2002. Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain 125(Pt 5):1105–1115.CrossRefPubMedGoogle Scholar
  51. Penfield, W. 1958. Centrencephalic integrating system. Brain 81(2):231–234.CrossRefPubMedGoogle Scholar
  52. Ries, C. R., and E. Puil. 1999a. Ionic mechanism of isoflurane's actions on thalamocortical neurons. J Neurophysiol 81(4):1802–1809.PubMedGoogle Scholar
  53. Ries, C. R., and E. Puil. 1999b. Mechanism of anesthesia revealed by shunting actions of isoflurane on thalamocortical neurons. J Neurophysiol 81(4):1795–1801.PubMedGoogle Scholar
  54. Schreckenberger, M., C. Lange-Asschenfeld, M. Lochmann, K. Mann, T. Siessmeier, H. G. Buchholz, P. Bartenstein, and G. Grunder. 2004. The thalamus as the generator and modulator of EEG alpha rhythm: a combined PET/EEG study with lorazepam challenge in humans. Neuroimage 22(2):637–644.CrossRefPubMedGoogle Scholar
  55. Steriade, M. 1994. Sleep oscillations and their blockage by activating systems. J Psychiatry Neurosci 19(5):354–358.PubMedGoogle Scholar
  56. Steriade, M., I. Timofeev, and F. Grenier. 2001. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85(5):1969–1985.PubMedGoogle Scholar
  57. Sugiyama, K., T. Muteki, and K. Shimoji. 1992. Halothane-induced hyperpolarization and depression of postsynaptic potentials of guinea pig thalamic neurons in vitro. Brain Res 576(1):97–103.CrossRefPubMedGoogle Scholar
  58. Tinklenberg, J. A., I. S. Segal, T. Z. Guo, and M. Maze. 1991. Analysis of anesthetic action on the potassium channels of the Shaker mutant of Drosophila. Ann N Y Acad Sci 625: 532–539.CrossRefPubMedGoogle Scholar
  59. Trout, W. E., and W. D. Kaplan. 1970. A relation between longevity, metabolic rate, and activity in shaker mutants of Drosophila melanogaster. Exp Gerontol 5(1):83–92.CrossRefPubMedGoogle Scholar
  60. Vahle-Hinz, C., O. Detsch, M. Siemers, E. Kochs, and B. Bromm. 2001. Local GABA(A) receptor blockade reverses isoflurane's suppressive effects on thalamic neurons in vivo.Google Scholar
  61. Vahle-Hinz, C., O. Detsch, M. Siemers, and E. Kochs. 2007. Contributions of GABAergic and glutamatergic mechanisms to isoflurane-induced suppression of thalamic somatosensory information transfer. Exp Brain Res 176(1):159–172.CrossRefPubMedGoogle Scholar
  62. Velly, L. J., M. F. Rey, N. J. Bruder, F. A. Gouvitsos, T. Witjas, J. M. Regis, J. C. Peragut, and F. M. Gouin. 2007. Differential dynamic of action on cortical and subcortical structures of anesthetic agents during induction of anesthesia. Anesthesiology 107(2):202–212.CrossRefPubMedGoogle Scholar
  63. Vincent, J. L., G. H. Patel, M. D. Fox, A. Z. Snyder, J. T. Baker, D. C. Van Essen, J. M. Zempel, L. H. Snyder, M. Corbetta, and M. E. Raichle. 2007. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447(7140):83–86.CrossRefPubMedGoogle Scholar
  64. Violet, J. M., D. L. Downie, R. C. Nakisa, W. R. Lieb, and N. P. Franks. 1997. Differential sensitivities of mammalian neuronal and muscle nicotinic acetylcholine receptors to general anesthetics. Anesthesiology 86(4):866–874.CrossRefPubMedGoogle Scholar
  65. Vogt, B. A., and S. Laureys. 2005. Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog Brain Res 150:205–217.CrossRefPubMedGoogle Scholar
  66. Volkow, N. D., G. J. Wang, R. Hitzemann, J. S. Fowler, N. Pappas, P. Lowrimore, G. Burr, K. Pascani, J. Overall, and A. P. Wolf. 1995. Depression of thalamic metabolism by lorazepam is associated with sleepiness. Neuropsychopharmacology 12(2):123–132.CrossRefPubMedGoogle Scholar
  67. Wang, H., H. Shi, L. Zhang, M. Pourrier, B. Yang, S. Nattel, and Z. Wang. 2000. Nicotine is a potent blocker of the cardiac A-type K(+) channels. Effects on cloned Kv4.3 channels and native transient outward current. Circulation 102(10):1165–1171.PubMedGoogle Scholar
  68. Weber, B., C. Schaper, D. Bushey, M. Rohlfs, M. Steinfath, G. Tononi, C. Cirelli, J. Scholz, and B. Bein. 2009. Increased volatile anesthetic requirement in short-sleeping Drosophila mutants. Anesthesiology 110(2):313–316.CrossRefPubMedGoogle Scholar
  69. White, N.S., and M.T. Alkire. 2002. Network activity changes during general anesthesia provide support for neurobiological theories of conscious awareness. American Society of Anesthesiologists annual meeting, Orlando, Fl, A-796.Google Scholar
  70. White, N. S., and M. T. Alkire. 2003. Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness. Neuroimage 19(2 Pt 1):402–411.CrossRefPubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.UCIMC, Department of Anesthesiology and Perioperative CareOrangeUSA

Personalised recommendations