Skip to main content
SpringerLink
Log in

Spontaneous Rhythmic Activity in the Adult Cerebral Cortex In Vitro

  • Protocol
  • First Online:
Isolated Central Nervous System Circuits

Part of the book series: Neuromethods ((NM,volume 73))

Abstract

The cerebral cortex in vivo generates different patterns of rhythmic activities with frequency rates ranging from below 1 Hz to fast frequencies well above 10 Hz. Some of these activities occur in the absence of external input and are a consequence of recurrent connectivity within the cortical network. The cerebral cortex in vitro maintains its recurrent connectivity, at least partly, and thus is able to generate some spontaneous rhythmic patterns as far as there is a certain level of intrinsic excitability in the network. An artificial cerebrospinal fluid (ACSF) with an ionic composition that mimics that in situ (Sanchez-Vives and McCormick, Nature Neuroscience. 3:1027, 2000) provides sufficient excitatory drive for the cortical network in vitro to generate not only slow (<1 Hz) rhythmic activity similar to the one that occurs during slow-wave sleep but also fast rhythms (10–80 Hz). Here, the methods and techniques used to prepare and study active cortical slices from adult animals are described, as well as the importance of methodological variables like temperature and oxygenation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Li CL, Mc Ilwain H (1957) Maintenance of resting membrane potentials in slices of mammalian cerebral cortex and other tissues in vitro. J Physiol 139:178–190

    PubMed  CAS  Google Scholar 

  2. Yamamoto C, McIlwain H (1966) Potentials evoked in vitro in preparations from the mammalian brain. Nature 210:1055–1056

    Article  PubMed  CAS  Google Scholar 

  3. Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302–1320

    PubMed  CAS  Google Scholar 

  4. Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflüger’s Arch 414:600–612

    Article  CAS  Google Scholar 

  5. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027–1034

    Article  PubMed  CAS  Google Scholar 

  6. 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

    PubMed  CAS  Google Scholar 

  7. Aghajanian GK, Rasmussen K (1989) Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3:331–338

    Article  PubMed  CAS  Google Scholar 

  8. Cunningham MO, Davies CH, Bühl EH, Kopell N, Whittington MA (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23:9761–9769

    PubMed  CAS  Google Scholar 

  9. Trapp S, Ballanyi K (2012) Autonomic nervous system in vitro: studying tonically active neurons controlling vagal outflow in rodent brainstem slices. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 1–59

    Google Scholar 

  10. Ye JH, Zhang J, Xiao C, Kong JQ (2006) Patch-clamp studies in the CNS illustrate a simple new method for obtaining viable neurons in rat brain slices: glycerol replacement of NaCl protects CNS neurons. J Neurosci Methods 158:251–259

    Article  PubMed  CAS  Google Scholar 

  11. Finkel A et al (1993) The Axon guide for electrophysiology and biophysics. Axon Instruments Inc, Foster City

    Google Scholar 

  12. Reig R, Mattia M, Compte A, Belmonte C, Sanchez-Vives MV (2010) Temperature modulation of slow and fast cortical rhythms. J Neurophysiol 103:1253–1261

    Article  PubMed  CAS  Google Scholar 

  13. Sanchez-Vives MV, Mattia M, Compte A, Perez-Zabalza M, Winograd M, Descalzo VF, Reig R (2010) Inhibitory modulation of cortical up states. J Neurophysiol 103:1253–1261

    Article  PubMed  Google Scholar 

  14. Chauvette S, Volgushev M, Timofeev I (2010) Origin of active states in local neocortical networks during slow sleep oscillation. Cereb Cortex 20:2660–2674

    Article  PubMed  Google Scholar 

  15. Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64:404–418

    Article  PubMed  CAS  Google Scholar 

  16. Compte A, Sanchez-Vives MV, McCormick DA, Wang XY (2003) Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J Neurophysiol 89:2707–2725

    Article  PubMed  Google Scholar 

  17. Volgushev M, Chauvette S, Mukovski M, Timofeev I (2006) Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations. J Neurosci 26:5665–5672

    Article  PubMed  CAS  Google Scholar 

  18. Shu Y, Hasenstaub A, Badoual M, Bal T, McCormick DA (2003) Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J Neurosci 23:10388–10401

    PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  20. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2002) Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. J Neurosci 22:8691–8704

    PubMed  CAS  Google Scholar 

  21. Contreras D, Timofeev I, Steriade M (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol 494:251–264

    PubMed  CAS  Google Scholar 

  22. Frohlich F, Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2006) Slow state transitions of sustained neural oscillations by activity-dependent modulation of intrinsic excitability. J Neurosci 26:6153–6162

    Article  PubMed  CAS  Google Scholar 

  23. Cunningham MO, Pervouchine DD, Racca C, Kopell NJ, Davies CH, Jones RS, Traub RD, Whittington MA (2006) Neuronal metabolism governs cortical network response state. Proc Natl Acad Sci USA 103:5597–5601

    Article  PubMed  CAS  Google Scholar 

  24. Mann EO, Kohl MM, Paulsen O (2009) Distinct roles of GABAA and GABAB receptors in balancing and terminating persistent cortical activity. J Neurosci 29:7513–7518

    Article  PubMed  CAS  Google Scholar 

  25. Brumberg, J. C., Sanchez-Vives, M. V. & Mccormick, D. A. (2000). Waking up the sleeping slice. In Society for Neuroscience Abstarcts, vol. 26, pp. 1966

    Google Scholar 

  26. Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450–467

    PubMed  CAS  Google Scholar 

  27. Bhattacharjee A, Kaczmarek LK (2005) For K+ channels, Na+ is the new Ca2+. Trends Neurosci 28:422–428

    Article  PubMed  CAS  Google Scholar 

  28. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862–6870

    Article  PubMed  CAS  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. Sanchez-Vives MV, Mattia M, Compte A, Perez-Zabalza M, Winograd M, Descalzo VF, Reig R (2011) Inhibitory modulation of cortical up states. J Neurophysiol 104:1314–1324

    Article  Google Scholar 

  31. Steriade M, Contreras D, Amzica F, Timofeev I (1996) Synchronization of fast (30–40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J Neurosci 16:2788–2808

    PubMed  CAS  Google Scholar 

  32. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423–435

    Article  PubMed  CAS  Google Scholar 

  33. McCormick DA, Shu Y, Hasenstaub A, Sanchez-Vives M, Badoual M, Bal T (2003) Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13:1219–1231

    Article  PubMed  Google Scholar 

  34. Sanchez-Vives MV, Reig R, Descalzo VF et al. (2002) In: FENS (Federation European Neurosciences Societies). Eur J Neurosci, Paris

    Google Scholar 

  35. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10:1185–1199

    Article  PubMed  CAS  Google Scholar 

  36. Sanchez-Vives MV, Reig R, Winograd M et al. (2007) In: Timofeev I (ed) Mechanisms of spontaneous active states in the neocortex, (Research Signpost), Kerala, India, pp 23–44

    Google Scholar 

  37. Reig R, Gallego R, Nowak LG, Sanchez-Vives MV (2006) Impact of cortical network activity on short-term synaptic depression. Cereb Cortex 16:688–695

    Article  PubMed  Google Scholar 

  38. Dickson CT, Biella G, de Curtis M (2003) Slow periodic events and their transition to gamma oscillations in the entorhinal cortex of the isolated guinea pig brain. J Neurophysiol 90:39–46

    Article  PubMed  Google Scholar 

  39. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782–806

    PubMed  CAS  Google Scholar 

  40. Nowak LG, Azouz R, Sanchez-Vives MV, Gray CM, McCormick DA (2003) Electro­physiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J Neurophysiol 89:1541–1566

    Article  PubMed  Google Scholar 

  41. Gonzalez-Burgos G, Barrionuevo G, Lewis DA (2000) Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. Cereb Cortex 10:82–92

    Article  PubMed  CAS  Google Scholar 

  42. Reig R, Sanchez-Vives MV (2007) Synaptic transmission and plasticity in an active cortical network. PLoS One 2:e670

    Article  PubMed  Google Scholar 

  43. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100:13638–13643

    Article  PubMed  CAS  Google Scholar 

  44. Fontanini A, Spano P, Bower JM (2003) Ketamine-xylazine-induced slow (<1.5 Hz) oscillations in the rat piriform (olfactory) cortex are functionally correlated with respiration. J Neurosci 23:7993–8001

    PubMed  CAS  Google Scholar 

  45. Wolansky T, Clement EA, Peters SR, Palczak MA, Dickson CT (2006) Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J Neurosci 26:6213–6329

    Article  PubMed  CAS  Google Scholar 

  46. Kawaguchi Y (2001) Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci 21:7261–7272

    PubMed  CAS  Google Scholar 

  47. Silberberg G, Wu C, Markram H (2004) Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit. J Physiol 556:19–27

    Article  PubMed  CAS  Google Scholar 

  48. van Drongelen W, Koch H, Marcuccilli C, Pena F, Ramirez JM (2003) Synchrony levels during evoked seizure-like bursts in mouse neocortical slices. J Neurophysiol 90:1571–1580

    Article  PubMed  Google Scholar 

  49. Ruiz-Mejias M et al. (2011) Slow and fast rhythms generated in the cerebral cortex of the anesthetized mouse. J Neurophysiol 106(6):2910–2921

    Article  PubMed  Google Scholar 

  50. DeFelipe J (2005) In: Casanova MF (ed) Neocortical modularity and the cell minicolumn. Nova, New York, pp 57–91

    Google Scholar 

  51. DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316

    Article  PubMed  Google Scholar 

  52. Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116–1133

    PubMed  CAS  Google Scholar 

  53. Rockland KS (1985) Anatomical organization of primary Visual Cortex (Area 17) in the Ferret. J Comp Neurol 241:225–236

    Article  PubMed  CAS  Google Scholar 

  54. Lund JS, Yoshioka T, Levitt JB (1993) Comparison of intrinsic connectivity in different areas of Macaque monkey cerebral cortex. Cereb Cortex 3:148–162

    Article  PubMed  CAS  Google Scholar 

  55. Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442

    Article  PubMed  CAS  Google Scholar 

  56. Sanchez-Vives MV, Compte A (2005) Structural statistical properties of the connectivity could underlie the difference in activity propagation velocities in visual and olfactory cortices, In: Lecture notes in computer science Springer Lecture Notes in Computer Science, 2005, Volume 3561/2005, 133–142, DOI: 10.1007/11499220_14 Springer Verlag Berlin Heidelberg133

  57. Cossart R, Aronov D, Yuste R (2003) Attractor dynamics of network UP states in the neocortex. Nature 423:283–288

    Article  PubMed  CAS  Google Scholar 

  58. de Lorente Nó R (1949) In: Fulton JF (ed) Physiology of the nervous system. Oxford University Press, New York, pp 228–330

    Google Scholar 

  59. Latham PE, Richmond BJ, Nelson PG, Nirenberg S (2000) Intrinsic dynamics in neuronal networks. I. Theory. J Neurophysiol 83:808–827

    PubMed  CAS  Google Scholar 

  60. Yamaguchi T (1986) Cerebral extracellular potassium concentration change and cerebral impedance change in short-term ischemia in gerbil. Bull Tokyo Med Dent Univ 33:1–8

    PubMed  CAS  Google Scholar 

  61. Zhang ET, Hansen AJ, Wieloch T, Lauritzen M (1990) Influence of MK-801 on brain extracellular calcium and potassium activities in severe hypoglycemia. J Cereb Blood Flow Metab 10:136–139

    Article  PubMed  CAS  Google Scholar 

  62. Hansen AJ (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65:101–148

    PubMed  CAS  Google Scholar 

  63. Ruangkittisakul A, Panaitescu B, Secchia L, Bobocea N, Kantor C, Kuribayashi J, Iizuka M, Ballanyi K (2012) Isolated brainstem respiratory centers from perinatal rodents. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 61–124

    Google Scholar 

  64. Kantor C, Panaitescu B, Kuribayashi J, Ruangkittisakul A, Jovanovic I, Leung V, Lee TF, MacTavish D, Jhamandas JH, Cheung PY, Ballanyi K (2012) Spontaneous neural network oscillations in hippocampus, cortex, and locus coeruleus of newborn rat and piglet brain slices. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 315–356

    Google Scholar 

  65. Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829–4843

    PubMed  CAS  Google Scholar 

  66. 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

    Article  PubMed  CAS  Google Scholar 

  67. Thompson SM, Masukawa LM, Prince DA (1985) Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro. J Neurosci 5:817–824

    PubMed  CAS  Google Scholar 

  68. Volgushev M, Vidyasagar TR, Chistiakova M, Yousef T, Eysel UT (2000) Membrane properties and spike generation in rat visual cortical cells during reversible cooling. J Physiol 522:59–76

    Article  PubMed  CAS  Google Scholar 

  69. Hodgkin AL, Katz B (1949) The effect of temperature on the electrical activity of the giant axon of the squid. J Physiol 109:240–249

    PubMed  CAS  Google Scholar 

  70. Borst JG, Sakmann B (1998) Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J Physiol 506:143–157

    Article  PubMed  CAS  Google Scholar 

  71. Asztely F, Erdemli G, Kullmann DM (1997) Extrasynaptic glutamate spillover in the hippo­campus: dependence on temperature and the role of active glutamate uptake. Neuron 18:281–293

    Article  PubMed  CAS  Google Scholar 

  72. Volgushev M, Vidyasagar TR, Chistiakova M, Eyzel UT (2000) Synaptic transmission in the neocortex during reversible cooling. Neuro­science 98:9–22

    Article  PubMed  CAS  Google Scholar 

  73. Fujii S, Sasaki H, Ito K, Kaneko K, Kato H (2002) Temperature dependence of synaptic responses in guinea pig hippocampal CA1 neurons in vitro. Cell Mol Neurobiol 22:379–391

    Article  PubMed  CAS  Google Scholar 

  74. Javedan SP, Fisher RS, Eder HG, Smith K, Wu J (2002) Cooling abolishes neuronal network synchronization in rat hippocampal slices. Epilepsia 43:574–580

    Article  PubMed  Google Scholar 

  75. Motamedi GK, Salazar P, Smith EL, Lesser RP, Webber WR, Ortinski PI, Vicini S, Rogawski MA (2006) Termination of epileptiform activity by cooling in rat hippocampal slice epilepsy models. Epilepsy Res 70:200–210

    Article  PubMed  CAS  Google Scholar 

  76. Wu J, Javedan SP, Ellsworth K, Smith K, Fisher RS (2001) Gamma oscillation underlies hyperthermia-induced epileptiform-like spikes in immature rat hippocampal slices. BMC Neurosci 2:18

    Article  PubMed  CAS  Google Scholar 

  77. Esmann M, Skou JC (1988) Temperature-dependencies of various catalytic activities of membrane-bound Na+/K+-ATPase from ox brain, ox kidney and shark rectal gland and of C12E8-solubilized shark Na+/K+-ATPase. Biochim Biophys Acta 944:344–350

    Article  PubMed  CAS  Google Scholar 

  78. Moser EI, Mathiesen LI (1996) Relationship between neuronal activity and brain temperature in rats. Neuroreport 7:1876–1880

    Article  PubMed  CAS  Google Scholar 

  79. Andersen P, Moser EI (1995) Brain temperature and hippocampal function. Hippocampus 5:491–498

    Article  PubMed  CAS  Google Scholar 

  80. Rothman SM (2009) The therapeutic potential of focal cooling for neocortical epilepsy. Neurotherapeutics 6:251–257

    Article  PubMed  Google Scholar 

  81. Rothman SM, Smyth MD, Yang XF, Peterson GP (2005) Focal cooling for epilepsy: an alternative therapy that might actually work. Epilepsy Behav 7:214–221

    Article  PubMed  Google Scholar 

  82. Johnson EW, Olsen KJ (1960) Clinical value of motor nerve conduction velocity determination. J Am Med Assoc 172:2030–2035

    Article  PubMed  CAS  Google Scholar 

  83. Pinto DJ, Patrick SL, Huang WC, Connors BW (2005) Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms. J Neurosci 25:8131–8140

    Article  PubMed  CAS  Google Scholar 

  84. Hajos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O (2009) Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29:319–327

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Based on work supported by the Ministerio de Ciencia e Innovación de España (BFU2011-27094). MVSV’s position is supported by ICREA (Institut Catala de Recerca i Estudis Avançats) at IDIBAPS (Institut d’Investigacions Biomèdiques August Pi i Sunyer). I would like to thank all my collaborators, in particular, R. Reig, M. Ruiz Mejías, V. F. Descalzo, M. Mattia, and M. Winograd.

Author information

Authors and Affiliations

  1. ICREAÐIDIBAPS, Barcelona, Spain

    Maria V. Sanchez-Vives

Authors
  1. Maria V. Sanchez-Vives
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria V. Sanchez-Vives .

Editor information

Editors and Affiliations

  1. Faculty of Medicine & Dentistry, Department of Physiology and Centre for, University of Alberta, N/A 232D, Edmonton, T6G 2S2, Alberta, Canada

    Klaus Ballanyi

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media New York

About this protocol

Cite this protocol

Sanchez-Vives, M.V. (2012). Spontaneous Rhythmic Activity in the Adult Cerebral Cortex In Vitro. In: Ballanyi, K. (eds) Isolated Central Nervous System Circuits. Neuromethods, vol 73. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-020-5_8

Download citation

  • DOI: https://doi.org/10.1007/978-1-62703-020-5_8

  • Published:

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-62703-019-9

  • Online ISBN: 978-1-62703-020-5

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation