Investigating Sleep Homeostasis with Extracellular Recording of Multiunit Activity from the Neocortex in Freely Behaving Rats

  • Vladyslav V. Vyazovskiy
  • Umberto Olcese
  • Giulio Tononi
Part of the Neuromethods book series (NM, volume 67)


Cortical activity during sleep and waking is traditionally investigated with electroencephalography (EEG). The most distinctive feature of neocortical activity during sleep is the occurrence of EEG slow waves, arising from quasi-synchronous periods of activity and silence among cortical neurons. The EEG slow waves are regulated homeostatically: they are larger and have a higher incidence following long waking periods and decrease as a function of time spent asleep. Since intense early sleep seems to be important for restoration, understanding the cellular mechanisms underlying homeostatic regulation of sleep slow waves may appear crucial for understanding sleep function. While macrooscillations recorded with the EEG arise from synchronous activity and silence of large populations of cortical neurons, at present intracellular recording techniques do not allow monitoring the state of more than just a few cells at a time across spontaneous sleep–wake cycle in unrestrained animals. Here, we review a method for chronic recording of extracellular LFP and multiunit activity from the neocortex in freely moving rats. This technique is most useful for addressing cellular mechanisms of sleep homeostasis because it allows monitoring the activity of many cells simultaneously for many hours. The description of the surgical procedure is complemented with a detailed account of spike sorting, which is a crucial step in processing and interpreting extracellular waveforms.

Key words

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


  1. 1.
    MacLean JN, Watson BO, Aaron GB et al (2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48:811–823PubMedCrossRefGoogle Scholar
  2. 2.
    Petersen CC, Hahn TT, Mehta M et al (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100:13638–13643PubMedCrossRefGoogle Scholar
  3. 3.
    Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64:404–418PubMedCrossRefGoogle Scholar
  4. 4.
    Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969–1985PubMedGoogle Scholar
  5. 5.
    Vyazovskiy VV, Olcese U, Lazimy YM et al (2009) Cortical firing and sleep homeostasis. Neuron 63:865–878PubMedCrossRefGoogle Scholar
  6. 6.
    Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6:e216PubMedCrossRefGoogle Scholar
  7. 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 405–417CrossRefGoogle Scholar
  8. 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, PAGoogle Scholar
  9. 9.
    Chauvette S, Volgushev M, Timofeev I (2010) Origin of active states in local neocortical networks during slow sleep oscillation. Cereb Cortex 20(11):2660–2674PubMedCrossRefGoogle Scholar
  10. 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 19:4595–4608PubMedGoogle Scholar
  11. 11.
    Amzica F, Steriade M (1998) Electrophysiological correlates of sleep delta waves. Electroencephalogr Clin Neurophysiol 107:69–83PubMedCrossRefGoogle Scholar
  12. 12.
    Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604–622PubMedGoogle Scholar
  13. 13.
    Buzsáki G (2006) Rhythms of the brain. Oxford University Press, OxfordCrossRefGoogle Scholar
  14. 14.
    Rasch MJ, Gretton A, Murayama Y et al (2008) Inferring spike trains from local field potentials. J Neurophysiol 99:1461–1476PubMedCrossRefGoogle Scholar
  15. 15.
    Lewicki MS (1998) A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9:R53–R78PubMedCrossRefGoogle Scholar
  16. 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 97:746–760PubMedCrossRefGoogle Scholar
  17. 17.
    Holt GR, Koch C (1999) Electrical interactions via the extracellular potential near cell bodies. J Comput Neurosci 6:169–184PubMedCrossRefGoogle Scholar
  18. 18.
    Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37–100PubMedGoogle Scholar
  19. 19.
    Buzsaki G (2004) Large-scale recording of neuronal ensembles. Nat Neurosci 7:446–451PubMedCrossRefGoogle Scholar
  20. 20.
    Gold C, Henze DA, Koch C et al (2006) On the origin of the extracellular action potential waveform: a modeling study. J Neurophysiol 95:3113–3128PubMedCrossRefGoogle Scholar
  21. 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 30:1631–1642PubMedGoogle Scholar
  22. 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 33:33–59PubMedCrossRefGoogle Scholar
  23. 23.
    Katzner S, Nauhaus I, Benucci A et al (2009) Local origin of field potentials in visual cortex. Neuron 61:35–41PubMedCrossRefGoogle Scholar
  24. 24.
    Csicsvari J, Jamieson B, Wise KD et al (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322PubMedCrossRefGoogle Scholar
  25. 25.
    Whittingstall K, Logothetis NK (2009) Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 64:281–289PubMedCrossRefGoogle Scholar
  26. 26.
    Sirota A, Montgomery S, Fujisawa S et al (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683–697PubMedCrossRefGoogle Scholar
  27. 27.
    Manning JR, Jacobs J, Fried I et al (2009) Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci 29:13613–13620PubMedCrossRefGoogle Scholar
  28. 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 26:4535–4545PubMedCrossRefGoogle Scholar
  29. 29.
    Poulet JF, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454:881–885PubMedCrossRefGoogle Scholar
  30. 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 27:5280–5290PubMedCrossRefGoogle Scholar
  31. 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 30:4440–4448PubMedCrossRefGoogle Scholar
  32. 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 13:179–208PubMedCrossRefGoogle Scholar
  33. 33.
    Jones BE (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26:578–586PubMedCrossRefGoogle Scholar
  34. 34.
    Miller DB, O’Callaghan JP (2006) The pharmacology of wakefulness. Metabolism 55:S13–S19PubMedCrossRefGoogle Scholar
  35. 35.
    Boutrel B, Koob GF (2004) What keeps us awake: the neuropharmacology of stimulants and wakefulness-promoting medications. Sleep 27:1181–1194PubMedGoogle Scholar
  36. 36.
    Vyazovskiy VV, Ruijgrok G, Deboer T et al (2006) Running wheel accessibility affects the regional electroencephalogram during sleep in mice. Cereb Cortex 16:328–336PubMedCrossRefGoogle Scholar
  37. 37.
    Gentet LJ, Avermann M, Matyas F et al (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422–435PubMedCrossRefGoogle Scholar
  38. 38.
    Sporns O, Tononi G, Edelman GM (2000) Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Netw 13:909–922PubMedCrossRefGoogle Scholar
  39. 39.
    Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533–557PubMedGoogle Scholar
  40. 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 12:589–600PubMedCrossRefGoogle Scholar
  41. 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 8:461–484PubMedCrossRefGoogle Scholar
  42. 42.
    Robinson TE (1980) Hippocampal rhythmic slow activity (RSA; theta): a critical analysis of selected studies and discussion of possible species-differences. Brain Res 203:69–101PubMedGoogle Scholar
  43. 43.
    Leung LW, Borst JG (1987) Electrical activity of the cingulate cortex. I. Generating mechanisms and relations to behavior. Brain Res 407:68–80PubMedCrossRefGoogle Scholar
  44. 44.
    Murata K, Kameda K (1963) The activity of single cortical neurones of unrestrained cats during sleep and wakefulness. Arch Ital Biol 101:306–331PubMedGoogle Scholar
  45. 45.
    Noda H, Adey WR (1973) Neuronal activity in the association cortex of the cat during sleep, wakefulness and anesthesia. Brain Res 54:243–259PubMedCrossRefGoogle Scholar
  46. 46.
    Hobson JA, McCarley RW (1971) Cortical unit activity in sleep and waking. Electroencephalogr Clin Neurophysiol 30:97–112PubMedCrossRefGoogle Scholar
  47. 47.
    Verzeano M, Negishi K (1960) Neuronal activity in cortical and thalamic networks. J Gen Physiol 43(6):177–195PubMedCrossRefGoogle Scholar
  48. 48.
    Noda H, Adey WR (1970) Firing of neuron pairs in cat association cortex during sleep and wakefulness. J Neurophysiol 33:672–684PubMedGoogle Scholar
  49. 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 206:281–291PubMedCrossRefGoogle Scholar
  50. 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 13:3252–3265PubMedGoogle Scholar
  51. 51.
    Calvet J, Fourment A, Thiefry M (1973) Electrical activity in neocortical projection and association areas during slow wave sleep. Brain Res 52:173–187PubMedCrossRefGoogle Scholar
  52. 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 13:3266–3283PubMedGoogle Scholar
  53. 53.
    Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100–107PubMedCrossRefGoogle Scholar
  54. 54.
    Luczak A, Bartho P, Marguet SL et al (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci USA 104:347–352PubMedCrossRefGoogle Scholar
  55. 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):400–414PubMedCrossRefGoogle Scholar
  56. 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 96:62–70PubMedCrossRefGoogle Scholar
  57. 57.
    Crunelli V, Hughes SW (2009) The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat Neurosci 13:9–17PubMedCrossRefGoogle Scholar
  58. 58.
    Hasenstaub A, Shu Y, Haider B et al (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423–435PubMedCrossRefGoogle Scholar
  59. 59.
    Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027–1034PubMedCrossRefGoogle Scholar
  60. 60.
    Fanselow EE, Connors BW (2010) The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in UP-DOWN states of mouse neocortex. J Neurophysiol 104:596–606PubMedCrossRefGoogle Scholar
  61. 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 194:225–237PubMedCrossRefGoogle Scholar
  62. 62.
    Massimini M, Huber R, Ferrarelli F et al (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862–6870PubMedCrossRefGoogle Scholar
  63. 63.
    Huber R, Deboer T, Tobler I (2000) Topography of EEG dynamics after sleep deprivation in mice. J Neurophysiol 84:1888–1893PubMedGoogle Scholar
  64. 64.
    Huber R, Ghilardi MF, Massimini M et al (2004) Local sleep and learning. Nature 430:78–81PubMedCrossRefGoogle Scholar
  65. 65.
    Vyazovskiy VV, Borbely AA, Tobler I (2002) Interhemispheric sleep EEG asymmetry in the rat is enhanced by sleep deprivation. J Neurophysiol 88:2280–2286PubMedCrossRefGoogle Scholar
  66. 66.
    Vyazovskiy VV, Tobler I, Winsky-Sommerer R (2007) Alteration of behavior in mice by muscimol is associated with regional electroencephalogram synchronization. Neuroscience 147:833–841PubMedCrossRefGoogle Scholar
  67. 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:e2483PubMedCrossRefGoogle Scholar
  68. 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 9:1169–1176PubMedCrossRefGoogle Scholar
  69. 69.
    Krueger JM, Rector DM, Roy S et al (2008) Sleep as a fundamental property of neuronal assemblies. Nat Rev Neurosci 9:910–919PubMedCrossRefGoogle Scholar
  70. 70.
    Riedner BA, Vyazovskiy VV, Huber R et al (2007) Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep 30:1643–1657PubMedGoogle Scholar
  71. 71.
    Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62PubMedCrossRefGoogle Scholar
  72. 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 9:367–371PubMedCrossRefGoogle Scholar
  73. 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 11:200–208PubMedCrossRefGoogle Scholar
  74. 74.
    Vyazovskiy VV, Tobler I (2008) Handedness leads to interhemispheric EEG asymmetry during sleep in the rat. J Neurophysiol 99:969–975PubMedCrossRefGoogle Scholar
  75. 75.
    Borbely AA (1982) A two process model of sleep regulation. Hum Neurobiol 1:195–204PubMedGoogle Scholar
  76. 76.
    Achermann P, Borbely AA (2003) Mathematical models of sleep regulation. Front Biosci 8:s683–s693PubMedCrossRefGoogle Scholar
  77. 77.
    Tobler I, Borbely AA (1986) Sleep EEG in the rat as a function of prior waking. Electroencephalogr Clin Neurophysiol 64:74–76PubMedCrossRefGoogle Scholar
  78. 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 2:65–69PubMedGoogle Scholar
  79. 79.
    Oleksenko AI, Mukhametov LM, Polyakova IG et al (1992) Unihemispheric sleep deprivation in bottlenose dolphins. J Sleep Res 1:40–44PubMedCrossRefGoogle Scholar
  80. 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 3:159–164PubMedCrossRefGoogle Scholar
  81. 81.
    Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62:143–150PubMedCrossRefGoogle Scholar
  82. 82.
    Hill S, Tononi G (2005) Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93:1671–1698PubMedCrossRefGoogle Scholar
  83. 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 30:1617–1630PubMedGoogle Scholar
  84. 84.
    Schwartz AB, Cui XT, Weber DJ et al (2006) Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52:205–220PubMedCrossRefGoogle Scholar
  85. 85.
    Nelson MJ, Pouget P (2010) Do electrode properties create a problem in interpreting local field potential recordings? J Neurophysiol 103:2315–2317PubMedCrossRefGoogle Scholar
  86. 86.
    Kralik JD, Dimitrov DF, Krupa DJ et al (2001) Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods 25:121–150PubMedCrossRefGoogle Scholar
  87. 87.
    Spataro L, Dilgen J, Retterer S et al (2005) Dexamethasone treatment reduces astroglia responses to inserted neuroprosthetic devices in rat neocortex. Exp Neurol 194:289–300PubMedCrossRefGoogle Scholar
  88. 88.
    Zhong Y, Bellamkonda RV (2007) Dexamethasone-coated neural probes elicit attenuated inflammatory response and neuronal loss compared to uncoated neural probes. Brain Res 1148:15–27PubMedCrossRefGoogle Scholar
  89. 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 32:719–729PubMedGoogle Scholar
  90. 90.
    Huber R, Tononi G, Cirelli C (2007) Exploratory behavior, cortical BDNF expression, and sleep homeostasis. Sleep 30:129–139PubMedGoogle Scholar
  91. 91.
    Lemon R, Prochazka A (1984) Methods for neuronal recording in conscious animals. Wiley, ChichesterGoogle Scholar
  92. 92.
    Nicolelis MAL (2008) Methods for neural ensemble recordings, 2nd edn. CRC Press, Boca Raton, FLGoogle Scholar
  93. 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 117:1–12PubMedCrossRefGoogle Scholar
  94. 94.
    Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661–1687PubMedCrossRefGoogle Scholar
  95. 95.
    Tolias AS, Ecker AS, Siapas AG et al (2007) Recording chronically from the same neurons in awake, behaving primates. J Neurophysiol 98:3780–3790PubMedCrossRefGoogle Scholar
  96. 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 135:55–65PubMedCrossRefGoogle Scholar
  97. 97.
    Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York, NYGoogle Scholar
  98. 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 134:9–21PubMedCrossRefGoogle Scholar
  99. 99.
    Tan P-N, Steinbach M, Kumar V (2006) Introduction to data mining, 1st edn. Pearson Addison Wesley, Boston, MAGoogle Scholar
  100. 100.
    Wood F, Black MJ, Vargas-Irwin C et al (2004) On the variability of manual spike sorting. IEEE Trans Biomed Eng 51:912–918PubMedCrossRefGoogle Scholar
  101. 101.
    Hartigan JA (1975) Clustering algorithms. Wiley, New York, NYGoogle Scholar
  102. 102.
    Bezdek JC, Ehrlich R, Full W (1984) Fcm—the fuzzy C-means clustering-algorithm. Comput Geosci 10:191–203CrossRefGoogle Scholar
  103. 103.
    Bishop CM (2006) Pattern recognition and machine learning. Springer, New York, NYGoogle Scholar
  104. 104.
    Ueda N, Nakano R, Ghahramani Z et al (2000) SMEM algorithm for mixture models. Neural Comput 12:2109–2128PubMedCrossRefGoogle Scholar
  105. 105.
    Davies DL, Bouldin DW (1979) Cluster Separation Measure. IEEE Trans Pattern Anal Mach Intell 1:224–227PubMedCrossRefGoogle Scholar
  106. 106.
    Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99–104PubMedCrossRefGoogle Scholar
  107. 107.
    Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476–486PubMedCrossRefGoogle Scholar
  108. 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 92:600–608PubMedCrossRefGoogle Scholar
  109. 109.
    Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22:10966–10975PubMedGoogle Scholar
  110. 110.
    McCormick DA, Connors BW, Lighthall JW et al (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782–806PubMedGoogle Scholar
  111. 111.
    Gray CM, McCormick DA (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274:109–113PubMedCrossRefGoogle Scholar
  112. 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 16:288–296PubMedCrossRefGoogle Scholar
  113. 113.
    Diester I, Nieder A (2008) Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J Neurosci 28:7737–7747PubMedCrossRefGoogle Scholar
  114. 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 93:942–953PubMedCrossRefGoogle Scholar
  115. 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 8:437–450PubMedCrossRefGoogle Scholar
  116. 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 25:3857–3869PubMedCrossRefGoogle Scholar
  117. 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 16:541–552PubMedCrossRefGoogle Scholar
  118. 118.
    Puig MV, Ushimaru M, Kawaguchi Y (2008) Two distinct activity patterns of fast-spiking interneurons during neocortical UP states. Proc Natl Acad Sci USA 105(24):8428–8433PubMedCrossRefGoogle Scholar
  119. 119.
    Tierney PL, Degenetais E, Thierry AM et al (2004) Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20:514–524PubMedCrossRefGoogle Scholar
  120. 120.
    Tseng KY, Mallet N, Toreson KL et al (2006) Excitatory response of prefrontal cortical fast-spiking interneurons to ventral tegmental area stimulation in vivo. Synapse 59:412–417PubMedCrossRefGoogle Scholar
  121. 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):658–674PubMedCrossRefGoogle Scholar
  122. 122.
    Kole MH, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633–647PubMedCrossRefGoogle Scholar
  123. 123.
    Pattle RE (1971) The external action potential of a nerve or muscle fibre in an extended medium. Phys Med Biol 16:673–685CrossRefGoogle Scholar
  124. 124.
    Richerson S, Ingram M, Perry D et al (2005) Classification of the extracellular fields produced by activated neural structures. Biomed Eng Online 4:53PubMedCrossRefGoogle Scholar
  125. 125.
    Schwartz AB (2004) Cortical neural prosthetics. Annu Rev Neurosci 27:487–507PubMedCrossRefGoogle Scholar
  126. 126.
    Polikov VS, Tresco PA, Reichert WM (2005) Response of brain tissue to chronically implanted neural electrodes. J Neurosci Methods 148:1–18PubMedCrossRefGoogle Scholar
  127. 127.
    Biran R, Martin DC, Tresco PA (2005) Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol 195:115–126PubMedCrossRefGoogle Scholar
  128. 128.
    Turner JN, Shain W, Szarowski DH et al (1999) Cerebral astrocyte response to micromachined silicon implants. Exp Neurol 156:33–49PubMedCrossRefGoogle Scholar
  129. 129.
    Greenberg PA, Wilson FA (2004) Functional stability of dorsolateral prefrontal neurons. J Neurophysiol 92:1042–1055PubMedCrossRefGoogle Scholar
  130. 130.
    Nicolelis MA, Dimitrov D, Carmena JM et al (2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci USA 100:11041–11046PubMedCrossRefGoogle Scholar
  131. 131.
    Greenberg PA, Wilson FAW (2004) Functional stability of dorsolateral prefrontal neurons. J Neurophysiol 92:1042–1055PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Vladyslav V. Vyazovskiy
    • 1
  • Umberto Olcese
    • 2
  • Giulio Tononi
    • 1
  1. 1.Department of PsychiatryUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.PERCRO Laboratory, Scuola Superiore Sant’AnnaIstituto Italiano di TecnologiaPisaItaly

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