Breakdown of effective connectivity during slow wave sleep: Investigating the mechanism underlying a cortical gate using large-scale modeling

Journal of Neurophysiology

Volumn 102, Issue 4, 2009, Pages 2096-2111

  Esser, Steve K ^a,b   Hill, Sean ^c   Tononi, Giulio ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; AROUSAL; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; NERVE CELL; NERVE CELL NETWORK; NEUROANATOMY; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; POTASSIUM CONDUCTANCE; PRIMATE; PRIORITY JOURNAL; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SLOW WAVE SLEEP; SPIKE WAVE; SYNAPSE; SYNAPTIC INHIBITION; THALAMOCORTICAL TRACT; WAKEFULNESS;

ALGORITHMS; CEREBRAL CORTEX; COMPUTER SIMULATION; ELECTROENCEPHALOGRAPHY; GAMMA-AMINOBUTYRIC ACID; HUMANS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; PERCEPTION; POTASSIUM CHANNELS; SLEEP; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMUS; TRANSCRANIAL MAGNETIC STIMULATION; WAKEFULNESS;

EID: 70350279036     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00059.2009     Document Type: Article

References (89)

1. Abbott LF, Varela JA, Sen K, Nelson SB. Synaptic depression and cortical gain control. Science 275: 220-224, 1997. (Pubitemid 27034764)
2. Addy RO, Dinner DS, Luders H, Lesser RP, Morris HH, Wyllie E. The effects of sleep on median nerve short latency somatosensory evoked potentials. Electroencephalogr Clin Neurophysiol 74: 105-111, 1989. (Pubitemid 19075652)
3. Alkire MT, Hudetz AG, Tononi G. Consciousness and anesthesia. Science 322: 876-880, 2008.
4. Amadeo M, Shagass C. Brief latency click-evoked potentials during waking and sleep in man. Psychophysiology 10: 244-250, 1973.
5. Baranyi A, Szente MB, Woody CD. Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. I. Patterns of firing activity and synaptic responses. J Neurophysiol 69: 1850-1864, 1993a.
6. Baranyi A, Szente MB, Woody CD. Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. Membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. J Neurophysiol 69: 1865-1879, 1993b.
7. Barbas H, Rempel-Clower N. Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7: 635-646, 1997. (Pubitemid 27467975)
8. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J Neurosci 22: 8691-8704, 2002. (Pubitemid 35387610)
9. Born J, Rasch B, Gais S. Sleep to remember. Neuroscientist 12: 410-424, 2006.
10. Buzas P, Kovacs K, Ferecsko AS, Budd JM, Eysel UT, Kisvarday ZF. Model-based analysis of excitatory lateral connections in the visual cortex. J Comp Neurol 499: 861-881, 2006. (Pubitemid 44892815)
11. Buzsaki G. Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7, Suppl 1: 17-23, 1998. (Pubitemid 28332614)
12. Campbell KB, Bartoli EA. Human auditory evoked potentials during natural sleep: the early components. Electroencephalogr Clin Neurophysiol 65: 142-149, 1986. (Pubitemid 16125144)
13. Colrain IM. The K-complex: a 7-decade history. Sleep 28: 255-273, 2005.
14. Compte A, Sanchez-Vives MV, McCormick DA, Wang XJ. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J Neurophysiol 89: 2707-2725, 2003. (Pubitemid 36570233)
15. Crochet S, Chauvette S, Boucetta S, Timofeev I. Modulation of synaptic transmission in neocortex by network activities. Eur J Neurosci 21: 1030-1044, 2005. (Pubitemid 40461055)
16. Deiber MP, Ibanez V, Bastuji H, Fischer C, Mauguiere F. Changes of middle latency auditory evoked potentials during natural sleep in humans. Neurology 39: 806-813, 1989. (Pubitemid 19150156)
17. Destexhe A, Bal T, McCormick DA, Sejnowski TJ. Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J Neurophysiol 76: 2049-2070, 1996. (Pubitemid 26322639)
18. Destexhe A, Rudolph M, Pare D. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751, 2003. (Pubitemid 37280153)
19. Destexhe A, Sejnowski TJ. G protein activation kinetics and spillover of gamma-aminobutyric acid may account for differences between inhibitory responses in the hippocampus and thalamus. Proc Natl Acad Sci USA 92: 9515-9519, 1995.
20. Disney AA, Domakonda KV, Aoki C. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J Comp Physiol 499: 49-63, 2006. (Pubitemid 44423695)
21. Emerson RG, Sgro JA, Pedley TA, Hauser WA. State-dependent changes in the N20 component of the median nerve somatosensory evoked potential. Neurology 38: 64-68, 1988. (Pubitemid 18028094)
22. Erwin R, Buchwald JS. Midlatency auditory evoked responses: differential effects of sleep in the human. Electroencephalogr Clin Neurophysiol 65: 383-392, 1986. (Pubitemid 16048437)
23. Esser SK, Hill SL, Tononi G. Modeling the effects of transcranial magnetic stimulation on cortical circuits. J Neurophysiol 94: 622-639, 2005. (Pubitemid 40923274)
24. Farley GR. Neural firing in ventrolateral thalamic nucleus during conditioned vocal behavior in cats. Exp Brain Res Exp Hirnf 115: 493-506, 1997.
25. Feldmeyer D, Lubke J, Silver RA, Sakmann B. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol 538: 803-822, 2002. (Pubitemid 35190073)
26. + current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol 493: 83-97, 1996.
27. Fox PT, Narayana S, Tandon N, Sandoval H, Fox SP, Kochunov P, Lancaster JL. Column-based model of electric field excitation of cerebral cortex. Hum Brain Mapp 22: 1-14, 2004. (Pubitemid 38586096)
28. Gerstein GL, Perkel DH. Simultaneously recorded trains of action potentials: analysis and functional interpretation. Science 164: 828-830, 1969.
29. Gil Z, Connors BW, Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19: 679-686, 1997. (Pubitemid 27430753)
30. Godschalk M, Lemon RN, Kuypers HG, Ronday HK. Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study. Exp Brain Res Exp Hirnf 56: 410-424, 1984. (Pubitemid 14022768)
31. Gonzalez-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953, 2005.
32. Haas HL. Cholinergic disinhibition in hippocampal slices of the rat. Brain Res 233: 200-204, 1982. (Pubitemid 12213673)
33. Haider B, Duque A, Hasenstaub AR, McCormick DA. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26: 4535-4545, 2006. (Pubitemid 44315353)
34. Hamill OP, Huguenard JR, Prince DA. Patch-clamp studies of voltage-gated currents in identified neurons of the rat cerebral cortex. Cereb Cortex 1: 48-61, 1991.
35. Hill S, Tononi G. Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93: 1671-1698, 2005. (Pubitemid 40283749)
36. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544, 1952.
37. Huguenard JR, McCormick DA. Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol 68: 1373-1383, 1992.
38. Jones EG. A new view of specific and nonspecific thalamocortical connections. Adv Neurol 77: 49-71, discussion 72-143, 1998.
39. Jones EG. Thalamic organization and function after Cajal. Prog Brain Res 136: 333-357, 2002.
40. Jones EG, Hendry SH. Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1: 222-246, 1989.
41. Kakigi R, Naka D, Okusa T, Wang X, Inui K, Qiu Y, Tran TD, Miki K, Tamura Y, Nguyen TB, Watanabe S, Hoshiyama M. Sensory perception during sleep in humans: a magnetoencephalograhic study. Sleep Med 4: 493-507, 2003. (Pubitemid 38145652)
42. Kitamura Y, Kakigi R, Hoshiyama M, Koyama S, Nakamura A. Effects of sleep on somatosensory evoked responses in human: a magnetoencephalographic study. Brain Res Cogn Brain Res 4: 275-279, 1996. (Pubitemid 26390786)
43. Koos T, Tepper JM. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 22: 529-535, 2002. (Pubitemid 34049092)
44. Maccabee PJ, Amassian VE, Eberle LP, Cracco RQ. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol 460: 201-219, 1993.
45. Madison DV, Lancaster B, Nicoll RA. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7: 733-741, 1987. (Pubitemid 17032590)
46. Marshall L, Helgadottir H, Molle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature 444: 610-613, 2006. (Pubitemid 44864437)
47. Massimini M, Ferrarelli F, Esser SK, Riedner BA, Huber R, Murphy M, Peterson MJ, Tononi G. Triggering sleep slow waves by transcranial magnetic stimulation. Proc Natl Acad Sci USA 104: 8496-8501, 2007. (Pubitemid 47175516)
48. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science 309: 2228-2232, 2005. (Pubitemid 41396075)
49. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G. The sleep slow oscillation as a traveling wave. J Neurosci 24: 6862-6870, 2004. (Pubitemid 39045442)
50. McCormick DA. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39: 337-388, 1992.
51. Metherate R, Ashe JH. Synaptic interactions involving acetylcholine, glutamate, and GABA in rat auditory cortex. Exp Brain Res Exp Hirnf 107: 59-72, 1995.
52. + current in rat neocortical pyramidal neurons. J Neurophysiol 79: 1579-1582, 1998.
53. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65: 37-100, 1985. (Pubitemid 15165385)
54. Mountcastle VB. The columnar organization of the neocortex. Brain 120: 701-722, 1997.
55. Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, and Tononi G. Characterizing sleep slow waves: a source modeling approach. Proc Natl Acad Sci USA 106: 1608-1613, 2009.
56. Myme CI, Sugino K, Turrigiano GG, Nelson SB. The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J Neurophysiol 90: 771-779, 2003. (Pubitemid 37092562)
57. Noda T, Yamamoto T. Response properties and morphological identification of neurons in the cat motor cortex. Brain Res 306: 197-206, 1984. (Pubitemid 14090458)
58. Nunez PL, Srinivasan R. Electric Fields of the Brain: The Neurophysics of EEG. Oxford, UK: Oxford Univ Press, 2006.
59. Picton TW, Hillyard SA, Krausz HI, Galambos R. Human auditory evoked potentials. I. Evaluation of components. Electroencephalogr Clin Neurophysiol 36: 179-190, 1974.
60. Portas CM, Krakow K, Allen P, Josephs O, Armony JL, Frith CD. Auditory processing across the sleep-wake cycle: simultaneous EEG and fMRI monitoring in humans. Neuron 28: 991-999, 2000. (Pubitemid 32038087)
61. Press WH, Teukolsky SA, Vetterling WT, Flannery BP. Numerical Recipes in C the Art of Scientific Computing. Cambridge University Press, 1992.
62. Raeva S, Vainberg N, Dubinin V. Analysis of spontaneous activity patterns of human thalamic ventrolateral neurons and their modifications due to functional brain changes. Neuroscience 88: 365-376, 1999. (Pubitemid 28480000)
63. Rosanova M, Timofeev I. Neuronal mechanisms mediating the variability of somatosensory evoked potentials during sleep oscillations in cats. J Physiol 562: 569-582, 2005.
64. Rudolph M, Pospischil M, Timofeev I, Destexhe A. Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J Neurosci 27: 5280-5290, 2007. (Pubitemid 46790168)
65. 2+ -dependent PKC. J Neurophysiol 98: 952-965, 2007.
66. Sejnowski TJ, Destexhe A. Why do we sleep? Brain Res 886: 208-223, 2000.
67. Sherman SM, Guillery RW. Functional organization of thalamocortical relays. J Neurophysiol 76: 1367-1395, 1996.
68. Sherman SM, Guillery RW, Sherman SM. Exploring the Thalamus and its Role in Cortical Function. Cambridge, MA: MIT Press, 2006.
69. Steriade M, Jones EG, Llinás RR. Thalamic Oscillations and Signaling. New York: Wiliey, 1990.
70. Steriade M, Timofeev I, Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969-1985, 2001.
71. Swadlow HA. Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J Neurophysiol 71: 437-453, 1994.
72. Thielscher A, Kammer T. Linking physics with physiology in TMS: a sphere field model to determine the cortical stimulation site in TMS. Neuroimage 17: 1117-1130, 2002. (Pubitemid 35333835)
73. Thomson AM, West OC, Hahn J, Deuchars J. Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496: 81-102, 1996. (Pubitemid 26345578)
74. Thomson AM, Destexhe A. Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices. Neuroscience 92: 1193-1215, 1999. (Pubitemid 29292559)
75. Thomson AM, West DC, Wang Y, Bannister AP. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12: 936-953, 2002. (Pubitemid 34894730)
76. Timofeev I, Contreras D, Steriade M. Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol 494: 265-278, 1996. (Pubitemid 26238015)
77. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10: 1185-1199, 2000. (Pubitemid 30954306)
78. Tokuno H, Nambu A. Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb Cortex 10: 58-68, 2000. (Pubitemid 30022833)
79. Tononi G. An information integration theory of consciousness. BMC Neurosci 5: 42, 2004.
80. Tononi G, Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62: 143-150, 2003.
81. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev 10: 49-62, 2006.
82. Tononi G, Sporns O. Measuring information integration. BMC Neurosci 4: 31, 2003.
83. Valentino RJ, Dingledine R. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1: 784-792, 1981. (Pubitemid 11011843)
84. 2+ unblock of NMDA receptors limits their contribution to spike generation in cortical pyramidal neurons. J Neurophysiol 89: 2778-2783, 2003.
85. Vautrin J, Barker JL. Presynaptic quantal plasticity: Katz's original hypothesis revisited. Synapse 47: 184-199, 2003. (Pubitemid 36056832)
86. Walker MP, Stickgold R. Sleep, memory, and plasticity. Annu Rev Psychol 57: 139-166, 2006.
87. Wang XJ. Fast burst firing and short-term synaptic plasticity: a model of neocortical chattering neurons. Neuroscience 89: 347-362, 1999.
88. Zikopoulos B, Barbas H. Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS ONE 2: e848, 2007.
89. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.