Modulation of the Hippocampal θ-Rhythm as a Mechanism for Anesthetic-Induced Amnesia

  • Misha Perouansky
  • Robert Pearce
Part of the Contemporary Clinical Neuroscience book series (CCNE)


Understanding the mechanisms of anesthetic interference with memory and consciousness is of scientific value and clinical importance. For the clinician, the ability to precisely monitor the effect of anesthetics on the brain, the organ where anesthetic drugs exert their core effects (effects on all other organs, no matter how profound, are side effects), would be practice changing.

The last decades have witnessed a momentous increase in the interest of the (neuro) scientific community in synchronized neuronal activity, the “rhythms of the brain” (Buzsaki. 2006. Rhythms of the Brain. 1 ed. New York: Oxford University Press). As their links to higher cognitive function become unraveled, mechanistically grounded approaches to understanding, measuring, and predicting drug effects on the mind become fathomable. This chapter will review the evidence suggesting that the ability of the brain to form explicit memories is dependent on the precise timing of synchronized neuronal activity in the hippocampus that presents as the θ-rhythm. Based on experiments in our lab, we will then develop the argument that anesthetic-induced amnesia is, at some point, reflected by the θ-rhythm and hence can be measured and quantified.


Anesthesia hippocampus θ-rhythm gamma oscillations 40 Hz rhythms amnesia learning memory 



Supported by National Institutes of Health (Bethesda, MD, USA) GM47818 (to M. Perouansky and R. Pearce) and NS056411 (to R. Pearce) and the Department of Anesthesiology, University of Wisconsin, Madison, WI, USA


  1. Avidan, M. S., L. Zhang, B. A. Burnside, K. J. Finkel, A. C. Searleman, J. A. Selvidge, L. Saager, M. S. Turner, S. Rao, M. Bottros, C. Hantler, E. Jacobsohn, and A. S. Evers. 2008. Anesthesia awareness and the bispectral index. N Engl J Med 358(11):1097–1108.CrossRefPubMedGoogle Scholar
  2. Banks, M. I., and R. A. Pearce. 1999. Dual actions of volatile anesthetics on GABA(A) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology 90(1):120–134.CrossRefPubMedGoogle Scholar
  3. Behrens, C. J., L. P. van den Boom, L. de Hoz, A. Friedman, and U. Heinemann. 2005. Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8(11):1560–1567.CrossRefPubMedGoogle Scholar
  4. Berg-Johnsen, J., and I. A. Langmoen. 1986. The effect of isoflurane on unmyelinated and myelinated fibres in the rat brain. Acta Physiol Scand 127(1):87–93.CrossRefPubMedGoogle Scholar
  5. Berg-Johnsen, J., and I. A. Langmoen. 1992. The effect of isoflurane on excitatory synaptic transmission in the rat hippocampus. Acta Anaesthesiol Scand 36(4):350–355.CrossRefPubMedGoogle Scholar
  6. Berry, S. D., and R. F. Thompson. 1978. Prediction of learning rate from the hippocampal electroencephalogram. Science 200(4347):1298–1300.CrossRefPubMedGoogle Scholar
  7. Bird, C. M., and N. Burgess. 2008. The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9(3):182–194.CrossRefPubMedGoogle Scholar
  8. Bland, B. H. 1986. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26(1):1–54.CrossRefPubMedGoogle Scholar
  9. Bland, B. H., C. E. Bland, L. V. Colom, S. H. Roth, S. DeClerk, A. Dypvik, J. Bird, and A. Deliyannides. 2003. Effect of halothane on type 2 immobility-related hippocampal theta field activity and theta-on/theta-off cell discharges. Hippocampus 13(1):38–47.CrossRefPubMedGoogle Scholar
  10. Bland, B. H., J. Jackson, D. Derrie-Gillespie, T. Azad, A. Rickhi, and J. Abriam. 2006. Amplitude, frequency, and phase analysis of hippocampal theta during sensorimotor processing in a jump avoidance task. Hippocampus 16(8):673–681.CrossRefPubMedGoogle Scholar
  11. Bland, B. H., and S. D. Oddie. 2001. Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav Brain Res 127(1–2):119–136.CrossRefPubMedGoogle Scholar
  12. Buzsaki, G. 1989. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31(3):551–570.CrossRefPubMedGoogle Scholar
  13. Buzsaki, G. 2002. Theta oscillations in the hippocampus. Neuron 33(3):325–340.CrossRefPubMedGoogle Scholar
  14. Buzsaki, G. 2005. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15(7):827–840.CrossRefPubMedGoogle Scholar
  15. Buzsaki, G. 2006. Rhythms of the Brain. 1 ed. New York: Oxford University Press.CrossRefGoogle Scholar
  16. Caraiscos, V. B., J. G. Newell, K. E. You-Ten, E. M. Elliott, T. W. Rosahl, K. A. Wafford, J. F. MacDonald, and B. A. Orser. 2004. Selective enhancement of tonic GABAergic inhibition in murine hippocampal neurons by low concentrations of the volatile anesthetic isoflurane. J Neurosci 24(39):8454–8458.CrossRefPubMedGoogle Scholar
  17. Chrobak, J. J., and G. Buzsaki. 1996. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16(9):3056–3066.PubMedGoogle Scholar
  18. DeCoteau, W. E., C. Thorn, D. J. Gibson, R. Courtemanche, P. Mitra, Y. Kubota, and A. M. Graybiel. 2007. Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci USA 104(13):5644–5649.CrossRefPubMedGoogle Scholar
  19. Dutton, R. C., A. J. Maurer, J. M. Sonner, M. S. Fanselow, M. J. Laster, and E. I. Eger, II. 2001. The concentration of isoflurane required to suppress learning depends on the type of learning. Anesthesiology 94(3):514–519.CrossRefPubMedGoogle Scholar
  20. Dutton, R. C., A. J. Maurer, J. M. Sonner, M. S. Fanselow, M. J. Laster, and E. I. Eger, II. 2002. Short-term memory resists the depressant effect of the nonimmobilizer 1-2-dichlorohexafluorocyclobutane (2 N) more than long-term memory. Anesth Analg 94(3):631–639; table of contents.CrossRefPubMedGoogle Scholar
  21. Edelman, G. 2001. Consciousness: the remembered present. Ann N Y Acad Sci 929:111–122.CrossRefPubMedGoogle Scholar
  22. Eichenbaum, H. 2004. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44(1):109–120.CrossRefPubMedGoogle Scholar
  23. Faulkner, H. J., R. D. Traub, and M. A. Whittington. 1998. Disruption of synchronous gamma oscillations in the rat hippocampal slice: a common mechanism of anaesthetic drug action. Br J Pharmacol 125(3):483–492.CrossRefPubMedGoogle Scholar
  24. Faulkner, H. J., R. D. Traub, and M. A. Whittington. 1999. Anaesthetic/amnesic agents disrupt beta frequency oscillations associated with potentiation of excitatory synaptic potentials in the rat hippocampal slice. Br J Pharmacol 128(8):1813–1825.CrossRefPubMedGoogle Scholar
  25. Franks, N. P., and W. R. Lieb. 1999. Background K+ channels: an important target for volatile anesthetics? Nat Neurosci 2(5):395–396.CrossRefPubMedGoogle Scholar
  26. Gonsowski, C. T., B. S. Chortkoff, E. I. Eger, II, H. L. Bennett, and R. B. Weiskopf. 1995. Subanesthetic concentrations of desflurane and isoflurane suppress explicit and implicit learning. Anesth Analg 80(3):568–572.CrossRefPubMedGoogle Scholar
  27. Gonsowski, C. T., and E. I. Eger, II. 1994. Nitrous oxide minimum alveolar anesthetic concentration in rats is greater than previously reported. Anesth Analg 79(4):710–712.CrossRefPubMedGoogle Scholar
  28. Gray, C. M., P. Konig, A. K. Engel, and W. Singer. 1989. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338(6213):334–337.CrossRefPubMedGoogle Scholar
  29. Griffin, A. L., Y. Asaka, R. D. Darling, and S. D. Berry. 2004. Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav Neurosci 118(2):403–411.CrossRefPubMedGoogle Scholar
  30. Hemmings, H. C. 2009. Molecular targets of general anesthetics in the nervous system. In Suppressing the mind: anesthetic modulation of memory and consciousness, edited by A. G. Hudetz and R. A. Pearce. New York City: Springer.Google Scholar
  31. Hu, H., K. Vervaeke, and J. F. Storm. 2002. Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J Physiol 545(Pt 3):783–805.CrossRefPubMedGoogle Scholar
  32. Hudetz, A. G. 2009. Cortical disintegration mechanism of anesthetic-induced unconsciousness. In Suppressing the mind: anesthetic modulation of memory and consciousness, edited by A. G. Hudetz and R. A. Pearce. New York City: Springer.Google Scholar
  33. Huerta, P. T., and J. E. Lisman. 1995. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15 (5):1053-63.CrossRefPubMedGoogle Scholar
  34. Huxter, J. R., T. J. Senior, K. Allen, and J. Csicsvari. 2008. Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci 11(5):587–594.CrossRefPubMedGoogle Scholar
  35. Jensen, O. 2005. Reading the hippocampal code by theta phase-locking. Trends Cogn Sci 9(12):551–553.CrossRefPubMedGoogle Scholar
  36. Jensen, O., and J. E. Lisman. 2005. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci 28(2):67–72.CrossRefPubMedGoogle Scholar
  37. Jones, M. V., P. A. Brooks, and N. L. Harrison. 1992. Enhancement of gamma-aminobutyric acid-activated Cl-currents in cultured rat hippocampal neurones by three volatile anaesthetics. J Physiol 449:279–293.PubMedGoogle Scholar
  38. Jones, M. W., and M. A. Wilson. 2005. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3(12):e402.CrossRefPubMedGoogle Scholar
  39. Jouvet, M. 1969. Biogenic amines and the states of sleep. Science 163(862):32–41.CrossRefPubMedGoogle Scholar
  40. Kahana, M. J., R. Sekuler, J. B. Caplan, M. Kirschen, and J. R. Madsen. 1999. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399(6738):781–784.CrossRefPubMedGoogle Scholar
  41. Kim, J. J., and M. S. Fanselow. 1992. Modality-specific retrograde amnesia of fear. Science 256(5057):675–677.CrossRefPubMedGoogle Scholar
  42. Kirson, E. D., Y. Yaari, and M. Perouansky. 1998. Presynaptic and postsynaptic actions of halothane at glutamatergic synapses in the mouse hippocampus. Br J Pharmacol 124(8):1607–1614.CrossRefPubMedGoogle Scholar
  43. Koblin, D. D., B. S. Chortkoff, M. J. Laster, E. I. Eger, II, M. J. Halsey, and P. Ionescu. 1994. Polyhalogenated and perfluorinated compounds that disobey the Meyer-Overton hypothesis. Anesth Analg 79(6):1043–1048.CrossRefPubMedGoogle Scholar
  44. Kramis, R., C. H. Vanderwolf, and B. H. Bland. 1975. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 49(1 Pt 1):58–85.CrossRefPubMedGoogle Scholar
  45. Larson, J., D. Wong, and G. Lynch. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368(2):347–350.CrossRefPubMedGoogle Scholar
  46. Leung, L. S. 1980. Behavior-dependent evoked potentials in the hippocampal CA1 region of the rat. I. Correlation with behavior and EEG. Brain Res 198(1):95–117.CrossRefPubMedGoogle Scholar
  47. Leung, L. S. 1984. Theta rhythm during REM sleep and waking: correlations between power, phase and frequency. Electroencephalogr Clin Neurophysiol 58(6):553–564.CrossRefPubMedGoogle Scholar
  48. Leung, L. S., and H. W. Yu. 1998. Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J Neurophysiol 79(3):1592–1596.PubMedGoogle Scholar
  49. Lukatch, H. S., V. A. Doze, and M. B. MacIver. 1996. Halothane prolongs GABA(A) fast and slow inhibitory currents. Anesthesiology 85:A673.Google Scholar
  50. Lukatch, H. S., and M. B. MacIver. 1997. Voltage-clamp analysis of halothane effects on GABA(A fast) and GABA(A slow) inhibitory currents. Brain Res 765(1):108–112.CrossRefPubMedGoogle Scholar
  51. MacIver, M. B. 1997. General anesthetic actions on transmission at glutamate and GABA synapses. In Anesthesia: biologic foundations, edited by T. L. e. a. Yaksh. Philadelphia: Lippincott-Raven.Google Scholar
  52. MacIver, M. B. 2009. Loss of recall and the hippocampal circuit effects produced by anesthetics. In Suppressing the mind: anesthetic modulation of memory and consciousness, edited by A. G. Hudetz and R. A. Pearce. New York City: Springer.Google Scholar
  53. MacIver, M. B., J. W. Mandema, D. R. Stanski, and B. H. Bland. 1996. Thiopental uncouples hippocampal and cortical synchronized electroencephalographic activity. Anesthesiology 84(6):1411–1424.CrossRefPubMedGoogle Scholar
  54. MacIver, M. B., A. A. Mikulec, S. M. Amagasu, and F. A. Monroe. 1996. Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 85(4):823–834.CrossRefGoogle Scholar
  55. Matus-Amat, P., E. A. Higgins, R. M. Barrientos, and J. W. Rudy. 2004. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 24(10):2431–2439.CrossRefPubMedGoogle Scholar
  56. McCartney, H., A. D. Johnson, Z. M. Weil, and B. Givens. 2004. Theta reset produces optimal conditions for long-term potentiation. Hippocampus 14(6):684–687.CrossRefPubMedGoogle Scholar
  57. McEchron, M. D., and J. F. Disterhoft. 1999. Hippocampal encoding of non-spatial trace conditioning. Hippocampus 9(4):385–396.CrossRefPubMedGoogle Scholar
  58. McHugh, T. J., M. W. Jones, J. J. Quinn, N. Balthasar, R. Coppari, J. K. Elmquist, B. B. Lowell, M. S. Fanselow, M. A. Wilson, and S. Tonegawa. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317(5834):94–99.CrossRefPubMedGoogle Scholar
  59. McNaughton, N., M. Ruan, and M. A. Woodnorth. 2006. Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16(12):1102–1110.CrossRefPubMedGoogle Scholar
  60. Mennerick, S., V. Jevtovic-Todorovic, S. M. Todorovic, W. Shen, J. W. Olney, and C. F. Zorumski. 1998. Effect of nitrous oxide on excitatory and inhibitory synaptic transmission in hippocampal cultures. J Neurosci 18(23):9716–9726.PubMedGoogle Scholar
  61. Mikulec, A. A., S. Pittson, S. M. Amagasu, F. A. Monroe, and M. B. MacIver. 1998. Halothane depresses action potential conduction in hippocampal axons. Brain Res 796(1–2):231–238.CrossRefPubMedGoogle Scholar
  62. Morris, R. G., E. Anderson, G. S. Lynch, and M. Baudry. 1986. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319(6056):774–776.CrossRefPubMedGoogle Scholar
  63. Morris, R. G., and U. Frey. 1997. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B Biol Sci 352(1360):1489–1503.CrossRefPubMedGoogle Scholar
  64. Myles, P. S., K. Leslie, J. McNeil, A. Forbes, and M. T. Chan. 2004. Bispectral index monitoring to prevent awareness during anaesthesia: the B-Aware randomised controlled trial. Lancet 363(9423):1757–1763.CrossRefPubMedGoogle Scholar
  65. Nakashiba, T., J. Z. Young, T. J. McHugh, D. L. Buhl, and S. Tonegawa. 2008. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 319(5867):1260–1264.CrossRefPubMedGoogle Scholar
  66. Nakazawa, K., M. C. Quirk, R. A. Chitwood, M. Watanabe, M. F. Yeckel, L. D. Sun, A. Kato, C. A. Carr, D. Johnston, M. A. Wilson, and S. Tonegawa. 2002. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297(5579):211–218.CrossRefPubMedGoogle Scholar
  67. Nishikawa, K., and M. B. MacIver. 2000a. Excitatory synaptic transmission mediated by NMDA receptors is more sensitive to isoflurane than are non-NMDA receptor-mediated responses. Anesthesiology 92(1):228–236.CrossRefPubMedGoogle Scholar
  68. Nishikawa, K., and M. B. MacIver. 2000b. Membrane and synaptic actions of halothane on rat hippocampal pyramidal neurons and inhibitory interneurons. J Neurosci 20(16):5915–5923.PubMedGoogle Scholar
  69. Nishikawa, K., and M. B. MacIver. 2001. Agent-selective effects of volatile anesthetics on GABAA receptor-mediated synaptic inhibition in hippocampal interneurons. Anesthesiology 94(2):340–347.CrossRefPubMedGoogle Scholar
  70. O’Keefe, J., and M. L. Recce. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3(3):317–330.CrossRefPubMedGoogle Scholar
  71. Orr, G., G. Rao, F. P. Houston, B. L. McNaughton, and C. A. Barnes. 2001. Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11(6):647–654.CrossRefPubMedGoogle Scholar
  72. Pan, W. X., and N. McNaughton. 1997. The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764(1–2):101–108.CrossRefPubMedGoogle Scholar
  73. Pearce, R. A., S. D. Grunder, and L. D. Faucher. 1995. Different mechanisms for use-dependent depression of two GABAA-mediated IPSCs in rat hippocampus. J Physiol 484(Pt 2):425–435.PubMedGoogle Scholar
  74. Pearce, R. A., J. L. Stringer, and E. W. Lothman. 1989. Effect of volatile anesthetics on synaptic transmission in the rat hippocampus. Anesthesiology 71(4):591–598.CrossRefPubMedGoogle Scholar
  75. Perouansky, M. 2008. Modern Anesthetics. Handb Exp Pharmacol (182):209–223.Google Scholar
  76. Perouansky, M., D. Baranov, M. Salman, and Y. Yaari. 1995. Effects of halothane on glutamate receptor-mediated excitatory postsynaptic currents. A patch-clamp study in adult mouse hippocampal slices. Anesthesiology 83(1):109–119.CrossRefPubMedGoogle Scholar
  77. Perouansky, M., H. Hentschke, M. Perkins, and R. A. Pearce. 2007. Amnesic concentrations of the nonimmobilizer 1,2-dichlorohexafluorocyclobutane (F6, 2 N) and isoflurane alter hippocampal theta oscillations in vivo. Anesthesiology 106(6):1168–1176.CrossRefPubMedGoogle Scholar
  78. Perouansky, M., E. D. Kirson, and Y. Yaari. 1996. Halothane blocks synaptic excitation of inhibitory interneurons. Anesthesiology 85(6):1431–1438; discussion 29A.CrossRefPubMedGoogle Scholar
  79. Perouansky, M., Perkins, M. G., Ford, T. M., Pearce, R. A. 2007. A comparison of the effects of halothane and nitrous oxide on hippocampal network activity. Soc Neurosci Annual Meeting Abstract # 937.1/AAA8.Google Scholar
  80. Perouansky, M., Perkins, M. G., Pearce, R. A. 2007. Isoflurane and F6 differentially affect hippocampal γ-oscillations. Am Soc Anesth Annual Meeting Abstract # A1217.Google Scholar
  81. Perouansky, M., Zurn, J., Perkins, M. G., Pearce, R. A. 2007. Nitrous oxide alters hippocampal theta and gamma oscillations in rats. Am Soc Anesth Annual Meeting Abstract # A1217.Google Scholar
  82. Raghavachari, S., M. J. Kahana, D. S. Rizzuto, J. B. Caplan, M. P. Kirschen, B. Bourgeois, J. R. Madsen, and J. E. Lisman. 2001. Gating of human theta oscillations by a working memory task. J Neurosci 21(9):3175–3183.PubMedGoogle Scholar
  83. Robbe, D., S. M. Montgomery, A. Thome, P. E. Rueda-Orozco, B. L. McNaughton, and G. Buzsaki. 2006. Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9(12):1526–1533.CrossRefPubMedGoogle Scholar
  84. Sato, N., and Y. Yamaguchi. 2007. Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18(5):419–424.CrossRefPubMedGoogle Scholar
  85. Seager, M. A., L. D. Johnson, E. S. Chabot, Y. Asaka, and S. D. Berry. 2002. Oscillatory brain states and learning: impact of hippocampal theta-contingent training. Proc Natl Acad Sci USA 99(3):1616–1620.CrossRefPubMedGoogle Scholar
  86. Sederberg, P. B., M. J. Kahana, M. W. Howard, E. J. Donner, and J. R. Madsen. 2003. Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23(34):10809–10814.PubMedGoogle Scholar
  87. Sederberg, P. B., A. Schulze-Bonhage, J. R. Madsen, E. B. Bromfield, D. C. McCarthy, A. Brandt, M. S. Tully, and M. J. Kahana. 2007. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17(5):1190–1196.CrossRefPubMedGoogle Scholar
  88. Shin, J., D. Kim, R. Bianchi, R. K. Wong, and H. S. Shin. 2005. Genetic dissection of theta rhythm heterogeneity in mice. Proc Natl Acad Sci USA 102(50):18165–18170.CrossRefPubMedGoogle Scholar
  89. Siapas, A. G., E. V. Lubenov, and M. A. Wilson. 2005. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46(1):141–151.CrossRefPubMedGoogle Scholar
  90. Singer, W. 1993. Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349–374.CrossRefPubMedGoogle Scholar
  91. Squire, L. R., C. E. Stark, and R. E. Clark. 2004. The medial temporal lobe. Annu Rev Neurosci 27:279–306.CrossRefPubMedGoogle Scholar
  92. Steriade, M. 2000. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101(2):243–276.CrossRefPubMedGoogle Scholar
  93. Stewart, M., and S. E. Fox. 1989. Detection of an atropine-resistant component of the hippocampal theta rhythm in urethane-anesthetized rats. Brain Res 500(1–2):55–60.CrossRefPubMedGoogle Scholar
  94. Vanderwolf, C. H. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26(4):407–418.CrossRefPubMedGoogle Scholar
  95. Vertes, R. P. 2005. Hippocampal theta rhythm: a tag for short-term memory. Hippocampus 15(7):923–935.CrossRefPubMedGoogle Scholar
  96. Veselis, R. A., and K. O. Pryor. 2009. Propofol amnesia – what is going on in the brain? In Suppressing the mind: anesthetic modulation of memory and consciousness, edited by A. G. Hudetz and R. A. Pearce. New York City: Springer.Google Scholar
  97. Whishaw, I. Q., and C. H. Vanderwolf. 1971. Hippocampal EEG and behavior: effects of variation in body temperature and relation of EEG to vibrissae movement, swimming and shivering. Physiol Behav 6(4):391–397.CrossRefPubMedGoogle Scholar
  98. Whittington, M. A., J. G. Jefferys, and R. D. Traub. 1996. Effects of intravenous anaesthetic agents on fast inhibitory oscillations in the rat hippocampus in vitro. Br J Pharmacol 118(8):1977–1986.PubMedGoogle Scholar
  99. Winegar, B. D., and M. B. MacIver. 2006. Isoflurane depresses hippocampal CA1 glutamate nerve terminals without inhibiting fiber volleys. BMC Neurosci 7:5.CrossRefPubMedGoogle Scholar
  100. Ylinen, A., A. Bragin, Z. Nadasdy, G. Jando, I. Szabo, A. Sik, and G. Buzsaki. 1995. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15(1 Pt 1):30–46.PubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of AnesthesiologyUniversity of Wisconsin, SMPH B6/319 Clinical Science CenterMadisonUSA
  2. 2.Department of AnesthesiologyUniversity of WisconsinMadisonUSA

Personalised recommendations