Origin of active states in local neocortical networks during slow sleep oscillation

Cerebral Cortex

Volumn 20, Issue 11, 2010, Pages 2660-2674

  Chauvette, Sylvain ^a   Volgushev, Maxim ^b,c,d   Timofeev, Igor ^a  

^a CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

^d UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Intracellular; intrinsic; oscillations; sleep; synaptic; synchronization

Indexed keywords

ANESTHESIA INDUCTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; FEMALE; INTRACELLULAR RECORDING; MALE; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; SLOW WAVE SLEEP; SYNAPSE;

EID: 77956370663     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq009     Document Type: Article

References (65)

1. Blake H, Gerard RW. 1937. Brain potentials during sleep. Am J Physiol. 119:692-703.
2. Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C, Devinsky O, Kuzniecky R, Doyle W, Madsen JR, et al. 2009. The human K-complex represents an isolated cortical down-state. Science. 324:1084-1087.
3. Chauvette S, Volgushev M, Mukovski M, Timofeev I. 2007. Local origin and long-range synchrony of active state in neocortex during slow oscillation. In: Timofeev I, editor. Mechanisms of spontaneous active states in the neocortex. Kerala (India): Research Signpost. p. 73-92.
4. Compte A, Sanchez-Vives MV, McCormick DA, Wang X-J. 2003. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J Neurophysiol. 89:2707-2725.
5. Connors BW, Gutnick MJ. 1990. Intrinsic firing patterns of divers neocortical neurons. Trends Neurosci. 13:99-104.
6. Contreras D, Steriade M. 1995. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci. 15:604-622.
7. Cossart R, Aronov D, Yuste R. 2003. Attractor dynamics of network UP states in the neocortex. Nature. 423:283-288.
8. Crochet S, Chauvette S, Boucetta S, Timofeev I. 2005. Modulation of synaptic transmission in neocortex by network activities. Eur J Neurosci. 21:1030-1044.
9. Cruikshank SJ, Lewis TJ, Connors BW. 2007. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neo-cortex. Nat Neurosci. 10:462-468.
10. Crunelli V, Hughes SW. 2010. The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat Neurosci. 13:9-17.
11. DeFelipe J, Farinas I. 1992. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol. 39:563-607.
12. Destexhe A, Rudolph M, Pare D. 2003. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci. 4:739-751.
13. Diesmann M, Gewaltig MO, Aertsen A. 1999. Stable propagation of synchronous spikingincortical neural networks. Nature. 402:529-533.
14. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M, Moss SJ, Haydon PG. 2009. Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci U S A. 106:15037-15042.
15. Fleidervish IA, Gutnick MJ. 1996. Kinetics of slow inactivation of persistent sodium current in layer V neurons of mouse neocortical slices. J Neurophysiol. 76:2125-2130.
16. Gray CM, McCormick DA. 1996. Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science. 274:109-113.
17. Greenberg DS, Houweling AR, Kerr JND. 2008. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci. 11:749-751.
18. Guan D, Lee JCF, Tkatch T, Surmeier DJ, Armstrong WE, Foehring RC. 2006. Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones. J Physiol (Lond). 571:371-389.
19. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci. 26:4535-4545.
20. Hasenstaub A, Sachdev RNS, McCormick DA. 2007. State changes rapidly modulate cortical neuronal responsiveness. J Neurosci. 27:9607-9622.
21. Hassler R, Muhs-Clement K. 1964. Architektonischer Aufbau des sensomotorischen und parietalen Cortex der Katze. J Hirnforschung. 6:377-422.
22. Hu H, Vervaeke K, Storm JF. 2007. M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J Neurosci. 27:1853-1867.
23. Hughes SW, Cope DW, Blethyn KL, Crunelli V. 2002. Cellular mechanisms of the slow (<1 Hz) oscillation in thalamocortical neurons in vitro. Neuron. 33:947-958.
24. Lisman JE. 1997. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20:38-43.
25. Llinas RR. 1988. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science. 242:1654-1664.
26. Luczak A, Bartho P, Marguet SL, Buzsaki G, Harris KD. 2007. Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A. 104:347-352
27. MahonS,VautrelleN,PezardL,SlaghtSJ,DeniauJ-M,ChouvetG,CharpierS. 2006. Distinct patterns of striatal medium spiny neuron activity during the natural sleep-wake cycle. J Neurosci. 26:12587-12595.
28. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 5:793-807.
29. Marsalek P, Koch C, Maunsell J. 1997. On the relationship between synaptic input and spike output jitter in individual neurons. Proc Natl Acad Sci U S A. 94:735-740.
30. Massimini M, Amzica F. 2001. Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. J Neurophysiol. 85:1346-1350.
31. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G. 2004. The sleep slow oscillation as a traveling wave. J Neurosci. 24:6862-6870.
32. McCormick DA, Pape HC. 1990. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurons. J Physiol. 431:291-318.
33. Mitzdorf U. 1985. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev. 65:37-100.
34. Mitzdorf U, Singer W. 1978. Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): a current source density analysis of electrically evoked potentials. Exp Brain Res. 33:371-394.
35. Mukovski M, Chauvette S, Timofeev I, Volgushev M. 2007. Detection of active and silent states in neocortical neurons from the field potential signal during slow-wave sleep. Cereb Cortex. 17:400-414.
36. Nicholson C, Freeman JA. 1975. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J Neurophysiol. 38:356-368.
37. Niedermeyer E, Lopes da Silva F. 2005. Electroencephalography: basic principles, clinical applications and related fields. Philadelphia (PA): Lippincott Williams & Wilkins. p. 1309.
38. Pare D, Lebel E, Lang EJ. 1997. Differential impact of miniature synaptic potentials on the soma and dendrites of pyramidal neurons in vivo. J Neurophysiol. 78:1735-1739.
39. Pedroarena C, Llinas R. 1997. Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons. Proc Natl Acad Sci U S A. 94:724-728.
40. Povysheva NV, Gonzalez-Burgos G, Zaitsev AV, Kroner S, Barrionuevo G, Lewis DA, Krimer LS. 2006. Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex. 16:541-552.
41. Prange O, Murphy TH. 1999. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J Neurosci. 19:6427-6438.
42. Pruss H, Derst C, Lommel R, Veh RW. 2005. Differential distribution of individual subunits of strongly inwardly rectifying potassium channels (Kir2 family) in rat brain. Mol Brain Res. 139:63-79.
43. Rudolph M, Pospischil M, Timofeev I, Destexhe A. 2007. Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J Neurosci. 27:5280-5290.
44. Saganich MJ, Machado E, Rudy B. 2001. Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain. J Neurosci. 21:4609-4624.
45. Sakata S, Harris KD. 2009. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron. 64:404-418.
46. Salin PA, Prince DA. 1996. Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neuro-physiol. 75:1573-1588.
47. Sanchez-Vives MV, Descalzo VF, Reig R, Figueroa NA, Compte A, Gallego R. 2008. Rhythmic spontaneous activity in the piriform cortex. Cereb Cortex. 18:1179-1192.
48. Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 3:1027-1034.
49. Schiller J, Schiller Y, Stuart G, Sakmann B. 1997. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol. 505(Pt 3):605-616.
50. Shu Y, Hasenstaub A, McCormick DA. 2003. Turning on and off recurrent balanced cortical activity. Nature. 423:288-293.
51. Steriade M. 2004. Neocortical cell classes are flexible entities. Nat Rev Neurosci. 5:121-134.
52. Steriade M, Nunez A, Amzica F. 1993a. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 13:3252-3265.
53. Steriade M, Nunez A, Amzica F. 1993b. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillations and other sleep rhythms of electroencephalogram. J Neurosci. 13: 3266-3283.
54. Steriade M, Contreras D, Dossi RC, Nunez A. 1993c. The slow (<1 Hz) oscillation in reticular thalamic and thalamo-cortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci. 13:3284-3299.
55. Steriade M, Timofeev I, Durmuller N, Grenier F. 1998. Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. J Neurophysiol. 79:483-490.
56. Steriade M, Timofeev I, Grenier F. 2001. Natural waking and sleep states: a view from inside neocorticalneurons. J Neurophysiol. 85:1969-1985.
57. Stuart G, Schiller J, Sakmann B. 1997. Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol. 505(Pt 3):617-632. (Pubitemid 28022363)
58. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M. 2000a. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex. 10:1185-1199.
59. Timofeev I, Grenier F, Steriade M. 2000b. Impact of intrinsic properties and synaptic factors on the activity of neocortical networks in vivo. J Physiol (Paris). 94:343-355.
60. Timofeev I, Grenier F, Steriade M. 2001. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci U S A. 98:1924-1929.
61. Timofeev I, Steriade M. 1996. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J Neurophysiol. 76: 4152-4168.
62. Volgushev M, Chauvette S, Mukovski M, Timofeev I. 2006. Precise longrange synchronization of activity and silence in neocortical neurons during slow-wave sleep. J Neurosci. 26:5665-5672.
63. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, Goldman-Rakic PS. 2006. Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci. 9:534-542.
64. Waters J, Helmchen F. 2006. Background synaptic activity is sparse in neocortex. J Neurosci. 26:8267-8277.
65. Zhu L, Blethyn KL, Cope DW, Tsomaia V, Crunelli V, Hughes SW. 2006. Nucleus- and species-specific properties of the slow (<1 Hz) sleep oscillation in thalamocortical neurons. Neuroscience. 141: 621-636. (Pubitemid 44066672)