Investigating sleep homeostasis with extracellular recording of multiunit activity from the neocortex in freely behaving rats

Neuromethods

Volumn 67, Issue , 2012, Pages 237-258

  Vyazovskiy, Vladyslav V ^a   Olcese, Umberto ^b   Tononi, Giulio ^a  

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

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Extracellular recordings; Local filed potentials; Multiunit activity; Neocortex; Rats; Sleep homeostasis; Spike sorting

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CLINICAL PROTOCOL; CRANIOTOMY; DATA ANALYSIS; ELECTROCORTICOGRAPHY; EXPERIMENTAL DESIGN; EXPERIMENTAL RAT; EXTRACELLULAR SPACE; INTRACELLULAR RECORDING; LATENT PERIOD; MICROELECTRODE; NEOCORTEX; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; NONREM SLEEP; PRIORITY JOURNAL; RAT; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; SPIKE WAVE; SURGICAL TECHNIQUE; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS;

EID: 84859771989     PISSN: 08932336     EISSN: 19406045     Source Type: Book Series    
DOI: 10.1007/7657_2011_22     Document Type: Article

References (131)

1. MacLean JN, Watson BO, Aaron GB .et al.2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48:811-823
2. Petersen CC, Hahn TT, MehtaM.et al.2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100:13638-13643
3. Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64:404-418
4. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985
5. Vyazovskiy VV, Olcese U, Lazimy YM .et al.2009) Cortical firing and sleep homeostasis. Neuron 63:865-878
6. Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6:e216
7. Borbély AA, Achermann P (2005) Sleep homeostasis and models of sleep regulation. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine. W. B. Saunders, Philadelphia, PA, pp 405-417
8. Tobler I (2005) Phylogeny of sleep regulation. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine. W. B. Saunders, Philadelphia, PA
9. Chauvette S, Volgushev M, Timofeev I (2010) Origin of active states in local neocortical networks during slow sleep oscillation. Cereb Cortex 20(11):2660-2674
10. Destexhe A, Contreras D, Steriade M (1999) Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J Neurosci 19:4595-4608
11. Amzica F, Steriade M (1998) Electrophysiological correlates of sleep delta waves. Electroencephalogr Clin Neurophysiol 107:69-83
12. Contreras D, SteriadeM(1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604-622
13. Buzsáki G (2006) Rhythms of the brain. Oxford University Press, Oxford
14. Rasch MJ, Gretton A, Murayama Y .et al.2008) Inferring spike trains from local field potentials. J Neurophysiol 99:1461-1476
15. Lewicki MS (1998) A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9: R53-R78
16. Shu Y, Duque A, Yu Y .et al.2007) Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings. J Neurophysiol 97:746-760
17. Holt GR, Koch C (1999) Electrical interactions via the extracellular potential near cell bodies. J Comput Neurosci 6:169-184
18. 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
19. Buzsaki G (2004) Large-scale recording of neuronal ensembles. Nat Neurosci 7:446-451
20. Gold C, Henze DA, Koch C .et al.2006) On the origin of the extracellular action potential waveform: a modeling study. J Neurophysiol 95:3113-3128
21. Vyazovskiy VV, Riedner BA, Cirelli C .et al.2007) Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. Sleep 30:1631-1642
22. Mitzdorf U (1987) Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. Int J Neurosci 33:33-59
23. Katzner S, Nauhaus I, Benucci A .et al.2009) Local origin of field potentials in visual cortex. Neuron 61:35-41
24. Csicsvari J, Jamieson B, Wise KD .et al.2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322
25. Whittingstall K, Logothetis NK (2009) Frequency- band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 64:281-289
26. Sirota A, Montgomery S, Fujisawa S .et al.2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683-697
27. Manning JR, Jacobs J, Fried I .et al.2009) Broadband shifts in local field potential power spectra are correlated with singleneuron spiking in humans. J Neurosci 29:13613-13620
28. Haider B, Duque A, Hasenstaub AR .et al.2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545
29. Poulet JF, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454:881-885
30. Rudolph M, Pospischil M, Timofeev I .et al.2007) Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J Neurosci 27:5280-5290
31. Okun M, Naim A, Lampl I (2010) The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J Neurosci 30:4440-4448
32. Villablanca JR (2004) Counterpointing the functional role of the forebrain and of the brainstem in the control of the sleep-waking system. J Sleep Res 13:179-208
33. Jones BE (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26:578-586
34. Miller DB, O'Callaghan JP (2006) The pharmacology of wakefulness. Metabolism 55: S13-S19
35. Boutrel B, Koob GF (2004) What keeps us awake: the neuropharmacology of stimulants and wakefulness-promoting medications. Sleep 27:1181-1194
36. Vyazovskiy VV, Ruijgrok G, Deboer T .et al.2006) Running wheel accessibility affects the regional electroencephalogram during sleep in mice. Cereb Cortex 16:328-336
37. Gentet LJ, Avermann M, Matyas F .et al.2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422-435
38. Sporns O, Tononi G, Edelman GM (2000) Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Netw 13:909-922
39. Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533-557
40. Petsche H, Stumpf C (1960) Topographic and toposcopic study of origin and spread of the regular synchronized arousal pattern in the rabbit. Electroencephalogr Clin Neurophysiol 12:589-600
41. Whishaw IQ, Vanderwolf CH (1973) Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav Biol 8:461-484
42. Robinson TE (1980) Hippocampal rhythmic slow activity (RSA; theta): a critical analysis of selected studies and discussion of possible species- differences. Brain Res 203:69-101
43. Leung LW, Borst JG (1987) Electrical activity of the cingulate cortex. I. Generating mechanisms and relations to behavior. Brain Res 407:68-80
44. Murata K, Kameda K (1963) The activity of single cortical neurones of unrestrained cats during sleep and wakefulness. Arch Ital Biol 101:306-331
45. Noda H, Adey WR (1973) Neuronal activity in the association cortex of the cat during sleep, wakefulness and anesthesia. Brain Res 54:243-259
46. Hobson JA, McCarley RW (1971) Cortical unit activity in sleep and waking. Electroencephalogr Clin Neurophysiol 30:97-112
47. Verzeano M, Negishi K (1960) Neuronal activity in cortical and thalamic networks. J Gen Physiol 43(6):177-195
48. Noda H, Adey WR (1970) Firing of neuron pairs in cat association cortex during sleep and wakefulness. J Neurophysiol 33:672-684
49. Burns BD, Stean JP, Webb AC (1979) The effects of sleep on neurons in isolated cerebral cortex. Proc R Soc Lond B Biol Sci 206:281-291
50. Steriade M, Nunez A, Amzica F (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components J. Neurosci. 13 3252-3265
51. Calvet J, Fourment A, ThiefryM(1973) Electrical activity in neocortical projection and association areas during slow wave sleep. Brain Res 52:173-187
52. Steriade M, Nunez A, Amzica F (1993) Intracellular analysis of relations between the slow ((<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram J. Neurosci. 13 3266-3283
53. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107
54. Luczak A, Bartho P, Marguet SL .et al.2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci USA 104:347-352
55. Mukovski M, Chauvette S, Timofeev I .et al.2007) Detection of active and silent states in neocortical neurons from the field potential signal during slow-wave sleep. Cereb Cortex 17(2):400-414
56. Molle M, Yeshenko O, Marshall L .et al.2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96:62-70
57. Crunelli V, Hughes SW (2009) The slow (<1 Hz) rhythm of non-REM sleep: A dialogue between three cardinal oscillators Nat. Neurosci. 13 9-17
58. Hasenstaub A, Shu Y, Haider B .et al.2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423-435
59. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027-1034
60. Fanselow EE, Connors BW (2010) The roles of somatostatin-expressing (GIN) and fastspiking inhibitory interneurons in UPDOWN states of mouse neocortex. J Neurophysiol 104:596-606
61. Webb AC (1976) The effects of changing levels of arousal on the spontaneous activity of cortical neurones: I. Sleep and wakefulness. Proc R Soc Lond B Biol Sci 194:225-237
62. Massimini M, Huber R, Ferrarelli F .et al.2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862-6870
63. Huber R, Deboer T, Tobler I (2000) Topography of EEG dynamics after sleep deprivation in mice. J Neurophysiol 84:1888-1893
64. Huber R, Ghilardi MF, Massimini M .et al.2004) Local sleep and learning. Nature 430:78-81
65. Vyazovskiy VV, Borbely AA, Tobler I (2002) Interhemispheric sleep EEG asymmetry in the rat is enhanced by sleep deprivation. J Neurophysiol 88:2280-2286
66. Vyazovskiy VV, Tobler I, Winsky-Sommerer R (2007) Alteration of behavior in mice by muscimol is associated with regional electroencephalogram synchronization. Neuroscience 147:833-841
67. De Gennaro L, Fratello F, Marzano C .et al.2008) Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. PLoS One 3:e2483
68. Huber R, Ghilardi MF, Massimini M .et al.2006) Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci 9:1169-1176
69. Krueger JM, Rector DM, Roy S .et al.2008) Sleep as a fundamental property of neuronal assemblies. Nat Rev Neurosci 9:910-919
70. Riedner BA, Vyazovskiy VV, Huber R .et al.2007) Sleep homeostasis and cortical synchronization: III. A high-density EEG studyof sleep slow waves in humans. Sleep 30:1643-1657
71. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49-62
72. Vyazovskiy V, Borbely AA, Tobler I (2000) Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J Sleep Res 9:367-371
73. Vyazovskiy VV, Cirelli C, Pfister-Genskow M .et al.2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11:200-208
74. Vyazovskiy VV, Tobler I (2008) Handedness leads to interhemispheric EEG asymmetry during sleep in the rat. J Neurophysiol 99:969-975
75. Borbely AA (1982) A two process model of sleep regulation. Hum Neurobiol 1:195-204
76. Achermann P, Borbely AA (2003) Mathematical models of sleep regulation. Front Biosci 8: s683-s693
77. Tobler I, Borbely AA (1986) Sleep EEG in the rat as a function of prior waking. Electroencephalogr Clin Neurophysiol 64:74-76
78. Cajochen C, Foy R, Dijk DJ (1999) Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans. Sleep Res Online 2:65-69
79. Oleksenko AI, Mukhametov LM, Polyakova IG .et al.1992) Unihemispheric sleep deprivation in bottlenose dolphins. J Sleep Res 1:40-44
80. Kattler H, Dijk DJ, Borbely AA (1994) Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J Sleep Res 3:159-164
81. Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143-150
82. Hill S, Tononi G (2005) Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93:1671-1698
83. Esser SK, Hill SL, Tononi G (2007) Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 30:1617-1630
84. Schwartz AB, Cui XT, Weber DJ .et al.2006) Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52:205-220
85. Nelson MJ, Pouget P (2010) Do electrode properties create a problem in interpreting local field potential recordings? J Neurophysiol 103:2315-2317
86. Kralik JD, Dimitrov DF, Krupa DJ .et al.2001) Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods 25:121-150
87. Spataro L, Dilgen J, Retterer S .et al.2005) Dexamethasone treatment reduces astroglia responses to inserted neuroprosthetic devices in rat neocortex. Exp Neurol 194:289-300
88. Zhong Y, Bellamkonda RV (2007) Dexamethasone- coated neural probes elicit attenuated inflammatory response and neuronal loss compared to uncoated neural probes. Brain Res 1148:15-27
89. Hanlon EC, Faraguna U, Vyazovskiy VV .et al.2009) Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep 32:719-729
90. Huber R, Tononi G, Cirelli C (2007) Exploratory behavior, cortical BDNF expression, and sleep homeostasis. Sleep 30:129-139
91. Lemon R, Prochazka A (1984) Methods for neuronal recording in conscious animals. Wiley, Chichester
92. Nicolelis MAL (2008) Methods for neural ensemble recordings, 2nd edn. CRC Press, Boca Raton, FL
93. Hulata E, Segev R, Ben-Jacob E (2002) A method for spike sorting and detection based on wavelet packets and Shannon's mutual information. J Neurosci Methods 117:1-12
94. Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661-1687
95. Tolias AS, Ecker AS, Siapas AG .et al.2007) Recording chronically from the same neurons in awake, behaving primates. J Neurophysiol 98:3780-3790
96. Zhang PM, Wu JY, Zhou Y .et al.2004) Spike sorting based on automatic template reconstruction with a partial solution to the overlapping problem. J Neurosci Methods 135:55-65
97. Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York, NY
98. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21
99. Tan P-N, Steinbach M, Kumar V (2006) Introduction to data mining, 1st edn. Pearson Addison Wesley, Boston, MA
100. Wood F, Black MJ, Vargas-Irwin C .et al.2004) On the variability of manual spike sorting. IEEE Trans Biomed Eng 51:912-918
101. Hartigan JA (1975) Clustering algorithms. Wiley, New York, NY
102. Bezdek JC, Ehrlich R, Full W (1984) Fcm- the fuzzy C-means clustering-algorithm. Comput Geosci 10:191-203
103. Bishop CM (2006) Pattern recognition and machine learning. Springer, New York, NY
104. Ueda N, NakanoR, GhahramaniZ.et al.2000) SMEM algorithm for mixture models. Neural Comput 12:2109-2128
105. Davies DL, Bouldin DW (1979) Cluster Separation Measure. IEEE Trans Pattern Anal Mach Intell 1:224-227
106. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99-104
107. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486
108. Bartho P, Hirase H, Monconduit L .et al.2004) Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92:600-608
109. Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22:10966-10975
110. McCormick DA, Connors BW, Lighthall JW .et al.1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806
111. 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
112. Diaz-Mataix L, Artigas F, Celada P (2006) Activation of pyramidal cells in rat medial prefrontal cortex projecting to ventral tegmental area by a 5-HT1A receptor agonist. Eur Neuropsychopharmacol 16:288-296
113. Diester I, Nieder A (2008) Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J Neurosci 28:7737-7747
114. Gonzalez-Burgos G, Krimer LS, Povysheva NV .et al.2005) Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93:942-953
115. Jung MW, Qin Y, McNaughton BL .et al.1998) Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8:437-450
116. Mallet N, Le Moine C, Charpier S .et al.2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25:3857-3869
117. Povysheva NV, Gonzalez-Burgos G, Zaitsev AV .et al.2006) Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex 16:541-552
118. PuigMV, UshimaruM, Kawaguchi Y (2008) Two distinct activity patterns of fast-spiking interneurons during neocortical UP states. Proc Natl Acad Sci USA 105 (24):8428-8433
119. Tierney PL, Degenetais E, Thierry AM .et al.2004) Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20:514-524
120. Tseng KY, Mallet N, Toreson KL .et al.2006) Excitatory response of prefrontal cortical fastspiking interneurons to ventral tegmental area stimulation in vivo. Synapse 59:412-417
121. Valenti O, Grace AA (2009) Entorhinal cortex inhibits medial prefrontal cortex and modulates the activity states of electrophysiologically characterized pyramidal neurons in vivo. Cereb Cortex 19 (3):658-674
122. Kole MH, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633-647
123. Pattle RE (1971) The external action potential of a nerve or muscle fibre in an extended medium. Phys Med Biol 16:673-685
124. Richerson S, Ingram M, Perry D .et al.2005) Classification of the extracellular fields produced by activated neural structures. Biomed Eng Online 4:53
125. Schwartz AB (2004) Cortical neural prosthetics. Annu Rev Neurosci 27:487-507
126. Polikov VS, Tresco PA, Reichert WM (2005) Response of brain tissue to chronically implanted neural electrodes. J Neurosci Methods 148:1-18
127. Biran R,MartinDC, Tresco PA (2005)Neuronal cell loss accompanies the brain tissueresponse to chronically implanted siliconmicroelectrode arrays. Exp Neurol 195:115-126
128. Turner JN, Shain W, Szarowski DH .et al.1999) Cerebral astrocyte response to micromachined silicon implants. Exp Neurol 156:33-49
129. Greenberg PA, Wilson FA (2004) Functional stability of dorsolateral prefrontal neurons. J Neurophysiol 92:1042-1055
130. Nicolelis MA, Dimitrov D, Carmena JM .et al.2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci USA 100:11041-11046
131. Greenberg PA, Wilson FAW (2004) Functional stability of dorsolateral prefrontal neurons. J Neurophysiol 92:1042-1055