Monosynaptic functional connectivity in cerebral cortex during wakefulness and under graded levels of anesthesia

Frontiers in Integrative Neuroscience

Volumn , Issue SEPTEMBER, 2012, Pages

  Vizuete, Jeannette A ^a   Pillay, Siveshigan ^b   Diba, Kamran ^c   Ropella, Kristina M ^a   Hudetz, Anthony G ^b  

^a Marquette University   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Connection strength; Consciousness; Cortical monosynaptic connectivity; Cross correlogram analysis; Excitatory inhibitory balance

Indexed keywords

DESFLURANE;

ANESTHESIA; ANESTHESIA INDUCTION; ANESTHESIA LEVEL; ANIMAL EXPERIMENT; BEHAVIOR CHANGE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN MAPPING; BRAIN REGION; CELL COMMUNICATION; CELL INTERACTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; MALE; MOLECULAR DYNAMICS; MONOSYNAPTIC REFLEX; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NONHUMAN; PROBABILITY; RAT; REVIEW; SPIKE WAVE; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; TASK PERFORMANCE; VISUAL CORTEX; WAKEFULNESS;

EID: 84867073908     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2012.00090     Document Type: Review

References (72)

1. Alkire, M.T., Hudetz, A.G., and Tononi, G. (2008). Consciousness and anesthesia. Science 322, 876-880.
2. Amzica, F. (2009). Basic physiology of burst-suppression. Epilepsia 50 Suppl 12, 38-39.
3. Antognini, J.F., and Kien, N.D. (1995). Potency (minimum alveolar anesthetic concentration) of isoflurane is independent of peripheral anesthetic effects. Anesth Analg 81, 69-72.
4. Banks, M.I., and Pearce, R.A. (1999). Dual actions of volatile anesthetics on GABA(A) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology 90, 120-134.
5. Bartho, P., Hirase, H., Monconduit, L., Zugaro, M., Harris, K.D., and Buzsaki, G. (2004). Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92, 600-608.
6. Bieda, M.C., and Maciver, M.B. (2004). Major role for tonic GABAA conductances in anesthetic suppression of intrinsic neuronal excitability. J Neurophysiol 92, 1658-1667.
7. Brown, E.N., Kass, R.E., and Mitra, P.P. (2004). Multiple neural spike train data analysis: state-of-the-art and future challenges. Nat Neurosci 7, 456-461.
8. Buzsaki, G. (2004). Large-scale recording of neuronal ensembles. Nat Neurosci 7, 446-451.
9. Buzsaki, G. (2006). Rhythms of the Brain. New York: Oxford University Press.
10. Buzsaki, G. (2007). The structure of consciousness. Nature 446, 267.
11. Buzsaki, G., Kaila, K., and Raichle, M. (2007). Inhibition and brain work. Neuron 56, 771-783.
12. Crochet, S., and Petersen, C.C. (2009). Cortical dynamics by layers. Neuron 64, 298-300.
13. Csicsvari, J., Hirase, H., Czurko, A., and Buzsaki, G. (1998). Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179-189.
14. Detsch, O., Kochs, E., Siemers, M., Bromm, B., and Vahle-Hinz, C. (2002). Increased responsiveness of cortical neurons in contrast to thalamic neurons during isoflurane-induced EEG bursts in rats. Neurosci Lett 317, 9-12.
15. Eger, E.I., 2nd, and Johnson, B.H. (1987). Rates of awakening from anesthesia with I-653, halothane, isoflurane, and sevoflurane: a test of the effect of anesthetic concentration and duration in rats. Anesth Analg 66, 977-982.
16. Erchova, I.A., Lebedev, M.A., and Diamond, M.E. (2002). Somatosensory cortical neuronal population activity across states of anaesthesia. Eur J Neurosci 15, 744-752.
17. Fee, M.S., Mitra, P.P., and Kleinfeld, D. (1996). Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. J Neurosci Methods 69, 175-188.
18. Ferrarelli, F., Massimini, M., Sarasso, S., Casali, A., Riedner, B.A., Angelini, G., Tononi, G., and Pearce, R.A. (2010). Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc Natl Acad Sci U S A 107, 2681-2686.
19. Ferron, J.F., Kroeger, D., Chever, O., and Amzica, F. (2009). Cortical inhibition during burst suppression induced with isoflurane anesthesia. J Neurosci 29, 9850-9860.
20. Franks, N.P. (2006). Molecular targets underlying general anaesthesia. Br J Pharmacol 147 Suppl 1, S72-81.
21. Franks, N.P. (2008). General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9, 370-386.
22. Friedman, E.B., Sun, Y., Moore, J.T., Hung, H.T., Meng, Q.C., Perera, P., Joiner, W.J., Thomas, S.A., Eckenhoff, R.G., Sehgal, A., and Kelz, M.B. (2010). A conserved behavioral state barrier impedes transitions between anesthetic-induced unconsciousness and wakefulness: evidence for neural inertia. PLoS One 5, e11903.
23. Fujisawa, S., Amarasingham, A., Harrison, M.T., and Buzsaki, G. (2008). Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 11, 823-833.
24. Fujiwara, S.E., Akema, T., and Izaki, Y. (2008). Cross-correlogram between rat hippocampal and prefrontal neuronal activities. Neuroreport 19, 1777-1782.
25. Garrett, K.M., and Gan, J. (1998). Enhancement of gamma-aminobutyric acidA receptor activity by alpha-chloralose. J Pharmacol Exp Ther 285, 680-686.
26. Gerstein, G.L., and Perkel, D.H. (1969). Simultaneously recorded trains of action potentials: analysis and functional interpretation. Science 164, 828-830.
27. Gugino, L.D., Chabot, R.J., Prichep, L.S., John, E.R., Formanek, V., and Aglio, L.S. (2001). Quantitative EEG changes associated with loss and return of consciousness in healthy adult volunteers anaesthetized with propofol or sevoflurane. Br JAnaesth 87, 421-428.
28. Hara, K., and Harris, R.A. (2002). The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 94, 313-318, table of contents.
29. Harrison, N.L., and Simmonds, M.A. (1985). Quantitative studies on some antagonists of N-methyl D-aspartate in slices of rat cerebral cortex. Br J Pharmacol 84, 381-391.
30. Hemmings, H.C., Jr., Akabas, M.H., Goldstein, P.A., Trudell, J.R., Orser, B.A., and Harrison, N.L. (2005). Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol Sci 26, 503-510.
31. Hentschke, H., Schwarz, C., and Antkowiak, B. (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, 93-102.
32. Hudetz, A.G. (2002). Effect of volatile anesthetics on interhemispheric EEG cross-approximate entropy in the rat. Brain Res 954, 123-131.
33. Hudetz, A.G., and Imas, O.A. (2007). Burst activation of the cerebral cortex by flash stimuli during isoflurane anesthesia in rats. Anesthesiology 107, 983-991.
34. Hudetz, A.G., Vizuete, J.A., and Imas, O.A. (2009). Desflurane selectively suppresses long-latency cortical neuronal response to flash in the rat. Anesthesiology 111, 231-239.
35. Hudetz, A.G., Wood, J.D., and Kampine, J.P. (2003). Cholinergic reversal of isoflurane anesthesia in rats as measured by cross-approximate entropy of the electroencephalogram. Anesthesiology 99, 1125-1131.
36. Imas, O.A., Ropella, K.M., Ward, B.D., Wood, J.D., and Hudetz, A.G. (2005a). Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat. Neurosci Lett 387, 145-150.
37. Imas, O.A., Ropella, K.M., Ward, B.D., Wood, J.D., and Hudetz, A.G. (2005b). Volatile anesthetics enhance flash-induced gamma oscillations in rat visual cortex. Anesthesiology 102, 937-947.
38. Imas, O.A., Ropella, K.M., Wood, J.D., and Hudetz, A.G. (2006). Isoflurane disrupts anterioposterior phase synchronization of flash-induced field potentials in the rat. Neurosci Lett 402, 216-221.
39. Kara, P., and Reid, R.C. (2003). Efficacy of retinal spikes in driving cortical responses. J Neurosci 23, 8547-8557.
40. Kass, R.E., Ventura, V., and Brown, E.N. (2005). Statistical issues in the analysis of neuronal data. J Neurophysiol 94, 8-25.
41. Kreuzer, M., Hentschke, H., Antkowiak, B., Schwarz, C., Kochs, E.F., and Schneider, G. (2010). Cross-approximate entropy of cortical local field potentials quantifies effects of anesthesia--a pilot study in rats. BMC Neurosci 11, 122.
42. Langheim, F.J., Murphy, M., Riedner, B.A., and Tononi, G. (2011). Functional connectivity in slow-wave sleep: identification of synchronous cortical activity during wakefulness and sleep using time series analysis of electroencephalographic data. J Sleep Res 20, 496-505.
43. Lee, U., Kim, S., Noh, G.J., Choi, B.M., Hwang, E., and Mashour, G.A. (2009). The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans. Conscious Cogn 18, 1069-1078.
44. Lidierth, M. (2009). sigTOOL: A MATLAB-based environment for sharing laboratory-developed software to analyze biological signals. J Neurosci Methods 178, 188-196.
45. MacIver, M.B., Mikulec, A.A., Amagasu, S.M., and Monroe, F.A. (1996). Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 85, 823-834.
46. Mcgaraughty, S., and Reinis, S. (1993). Simultaneous multi-and single-unit recordings in the rostral ventromedial medulla of ketamine-anaesthetized rats, and the cross-correlogram analysis of their interactions. Exp Brain Res 92, 489-494.
47. Moffitt, M.A., and Mcintyre, C.C. (2005). Model-based analysis of cortical recording with silicon microelectrodes. Clin Neurophysiol 116, 2240-2250.
48. Murrell, J.C., Waters, D., and Johnson, C.B. (2008). Comparative effects of halothane, isoflurane, sevoflurane and desflurane on the electroencephalogram of the rat. Lab Anim 42, 161-170.
49. Pearce, R.A., Stringer, J.L., and Lothman, E.W. (1989). Effect of volatile anesthetics on synaptic transmission in the rat hippocampus. Anesthesiology 71, 591-598.
50. Pittson, S., Himmel, A.M., and Maciver, M.B. (2004). Multiple synaptic and membrane sites of anesthetic action in the CA1 region of rat hippocampal slices. BMC Neurosci 5, 52.
51. Populin, L.C. (2005). Anesthetics change the excitation/inhibition balance that governs sensory processing in the cat superior colliculus. J Neurosci 25, 5903-5914.
52. Quilichini, P., Sirota, A., and Buzsaki, G. (2010). Intrinsic circuit organization and theta-gamma oscillation dynamics in the entorhinal cortex of the rat. J Neurosci 30, 11128-11142.
53. Rampil, I.J. (1994). Anesthetic potency is not altered after hypothermic spinal cord transection in rats. Anesthesiology 80, 606-610.
54. Rehberg, B., Bouillon, T., Zinserling, J., and Hoeft, A. (1999). Comparative pharmacodynamic modeling of the electroencephalography-slowing effect of isoflurane, sevoflurane, and desflurane. Anesthesiology 91, 397-405.
55. Ries, C.R., and Puil, E. (1999). Ionic mechanism of isoflurane's actions on thalamocortical neurons. J Neurophysiol 81, 1802-1809.
56. Rudolph, U., and Antkowiak, B. (2004). Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5, 709-720.
57. Sakata, S., and Harris, K.D. (2009). Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64, 404-418.
58. Sceniak, M.P., and Maciver, M.B. (2006). Cellular actions of urethane on rat visual cortical neurons in vitro. J Neurophysiol 95, 3865-3874.
59. Schneidman, E., Berry, M.J., 2nd, Segev, R., and Bialek, W. (2006). Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440, 1007-1012.
60. Schumacher, J.W., Schneider, D.M., and Woolley, S.M. (2011). Anesthetic state modulates excitability but not spectral tuning or neural discrimination in single auditory midbrain neurons. J Neurophysiol 106, 500-514.
61. Shew, W.L., Yang, H., Yu, S., Roy, R., and Plenz, D. (2011). Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches. J Neurosci 31, 55-63.
62. Shlens, J., Field, G.D., Gauthier, J.L., Grivich, M.I., Petrusca, D., Sher, A., Litke, A.M., and Chichilnisky, E.J. (2006). The structure of multi-neuron firing patterns in primate retina. J Neurosci 26, 8254-8266.
63. Sleigh, J.W., Vizuete, J.A., Voss, L., Steyn-Ross, A., Steyn-Ross, M., Marcuccilli, C.J., and Hudetz, A.G. (2009). The electrocortical effects of enflurane: experiment and theory. Anesth Analg 109, 1253-1262.
64. Tamas, G., Buhl, E.H., and Somogyi, P. (1997). Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500 (Pt 3), 715-738.
65. Tang, A., Jackson, D., Hobbs, J., Chen, W., Smith, J.L., Patel, H., Prieto, A., Petrusca, D., Grivich, M.I., Sher, A., Hottowy, P., Dabrowski, W., Litke, A.M., and Beggs, J.M. (2008). A maximum entropy model applied to spatial and temporal correlations from cortical networks in vitro. J Neurosci 28, 505-518.
66. Thomson, A.M., West, D.C., Hahn, J., and Deuchars, J. (1996). Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496 (Pt 1), 81-102.
67. Tononi, G., and Edelman, G.M. (1998). Consciousness and the integration of information in the brain. Adv Neurol 77, 245-279; discussion 279-280.
68. Usrey, W.M., Reppas, J.B., and Reid, R.C. (1998). Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384-387.
69. Villeneuve, M.Y., and Casanova, C. (2003). On the use of isoflurane versus halothane in the study of visual response properties of single cells in the primary visual cortex. J Neurosci Methods 129, 19-31.
70. Wang, J.X., and Zochowski, M. (2012). Interactions of excitatory and inhibitory feedback topologies in facilitating pattern separation and retrieval. Neural Comput 24, 32-59.
71. Yizhar, O., Fenno, L.E., Prigge, M., Schneider, F., Davidson, T.J., O'shea, D.J., Sohal, V.S., Goshen, I., Finkelstein, J., Paz, J.T., Stehfest, K., Fudim, R., Ramakrishnan, C., Huguenard, J.R., Hegemann, P., and Deisseroth, K. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178.
72. Yu, S., Huang, D., Singer, W., and Nikolic, D. (2008). A small world of neuronal synchrony. Cereb Cortex 18, 2891-2901.