Skip to main content
SpringerLink
Log in

Timing Excitation and Inhibition in the Cortical Network

  • Chapter
  • First Online:
Coherent Behavior in Neuronal Networks

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 3))

Abstract

The interaction between excitation and inhibition in the cerebral cortex network determines the emergent patterns of activity. Here we analyze the specific engagement of excitation and inhibition during a physiological network function such as slow oscillatory activity ( < 1 Hz), during which up and down cortical states alternate. This slow rhythm represents a well-characterized physiological activity with a range of experimental models from in vitro maintained cortical slices to sleeping animals. Excitatory and inhibitory events impinging on individual neurons were identified during up and down network states, which were recognized by the population activity. The accumulation of excitatory and inhibitory events at the beginning of up states was remarkably synchronized in the cortex both in vitro and in vivo. The same synchronization prevailed during the transition from up to down states. The absolute number of detected synaptic events pointed as well towards a delicate balance between excitation and inhibition in the network. The mechanistic and connectivity rules that can support these experimental findings are explored using a biologically inspired computer model of the cortical network.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909–926.

    PubMed  CAS  Google Scholar 

  2. Bernander O, Koch C, Douglas RJ (1994) Amplification and linearization of distal synaptic input to cortical pyramidal cells. J Neurophysiol 72:2743–2753.

    PubMed  CAS  Google Scholar 

  3. Blackwell K, Czubayko U, Plenz D (2003) Quantitative estimate of synaptic inputs to striatal neurons during up and down states in vitro. J Neurosci 23:9123–9132.

    PubMed  CAS  Google Scholar 

  4. Borg-Graham LJ, Monier C, Fregnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393:369–373.

    Article  PubMed  CAS  Google Scholar 

  5. Compte A, Sanchez-Vives MV, McCormick DA, Wang XJ (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 

  6. Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV (2008) Spontaneous high-frequency (10–80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci 28:13828–13844.

    Article  PubMed  CAS  Google Scholar 

  7. Contreras D, Timofeev I, Steriade M (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol 494 (Pt 1): 251–264.

    PubMed  CAS  Google Scholar 

  8. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17–32.

    PubMed  CAS  Google Scholar 

  9. Dantzker JL, Callaway EM (1998) The development of local, layer-specific visual cortical axons in the absence of extrinsic influences and intrinsic activity. J Neurosci 18:4145–4154.

    PubMed  CAS  Google Scholar 

  10. Descalzo VF, Nowak LG, Brumberg JC, McCormick DA, Sanchez-Vives MV (2005) Slow adaptation in fast-spiking neurons of visual cortex. J Neurophysiol 93:1111–1118.

    Article  PubMed  CAS  Google Scholar 

  11. Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419–451. Review.

    Google Scholar 

  12. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476–2489.

    PubMed  CAS  Google Scholar 

  13. Fairen A, DeFelipe J, Regidor J (1984) Non pyramidal neurons: general account. In: Cerebral Cortex (Peters AaJEG, ed.). London: Plenum Press.

    Google Scholar 

  14. Feldman ML (1984) Morphology of the neocortical pyramidal neuron. In: Cerebral Cortex (Peters AaJEG, ed.). London: Plenum Press.

    Google Scholar 

  15. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72–75.

    Article  PubMed  CAS  Google Scholar 

  16. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75–79.

    Article  PubMed  CAS  Google Scholar 

  17. 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 

  18. Hebb DO (1949) The organization of behavior. New York:Wiley.

    Google Scholar 

  19. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387–396.

    PubMed  CAS  Google Scholar 

  20. Kruglikov I, Rudy B (2008) Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58:911–924.

    Article  PubMed  CAS  Google Scholar 

  21. Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22:361–374.

    Article  PubMed  CAS  Google Scholar 

  22. Lorente de Nó R (1938) Analysis of the activity of the chains of internuncial neurons. J Neurophysiol 1:207–244.

    Google Scholar 

  23. Lund, JS and Wu, CQ (1997) Local circuit neurons of macaque monkey striate cortex: IV. Neurons of laminae 1–3A. J Comp Neurol 384:109–126.

    Article  PubMed  CAS  Google Scholar 

  24. 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.

    Article  PubMed  CAS  Google Scholar 

  25. 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 

  26. Megias M, Emri Z, Freund TF, Gulyas AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527–540.

    Article  PubMed  CAS  Google Scholar 

  27. Monier C, Fournier J, Fregnac Y (2008) In vitro and in vivo measures of evoked excitatory and inhibitory conductance dynamics in sensory cortices. J Neurosci Methods 169:323–365.

    Article  PubMed  CAS  Google Scholar 

  28. 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 

  29. Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11:535–537.

    Article  PubMed  CAS  Google Scholar 

  30. Pare D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J Neurophysiol 79:1450–1460.

    PubMed  CAS  Google Scholar 

  31. Peters A (2002) Examining neocortical circuits: some background and facts. J Neurocytol 31:183–193.

    Article  PubMed  CAS  Google Scholar 

  32. Reig R, Sanchez-Vives MV (2007) Synaptic transmission and plasticity in an active cortical network. Plos One 2(7):e670.

    Article  PubMed  Google Scholar 

  33. Rudolph M, Pelletier JG, Paré D, Destexhe A (2005) Characterization of synaptic conductances and integrative properties during electrically induced EEG-activated states in neocortical neurons in vivo. J Neurophysiol. Oct 94(4):2805–2821. Epub 2005 Jul 13.

    Google Scholar 

  34. 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.

    Article  PubMed  CAS  Google Scholar 

  35. 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 

  36. Schwindt PC, Crill WE (1997) Modification of current transmitted from apical dendrite to soma by blockade of voltage- and Ca2 +-dependent conductances in rat neocortical pyramidal neurons. J Neurophysiol 78:187–198.

    PubMed  CAS  Google Scholar 

  37. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870–3896.

    PubMed  CAS  Google Scholar 

  38. Shu Y, Hasenstaub A, McCormick DA (2003a) Turning on and off recurrent balanced cortical activity. Nature 423:288–293.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  40. Somogyi P, Kisvarday ZF, Martin KA, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261–294.

    Article  PubMed  CAS  Google Scholar 

  41. 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.

    PubMed  CAS  Google Scholar 

  42. Steriade M, Nunez A, Amzica F (1993b) Intracellular analysis of relations between the slow ( < 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266–3283.

    PubMed  CAS  Google Scholar 

  43. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969–1985.

    PubMed  CAS  Google Scholar 

  44. Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77:1697–1715.

    PubMed  CAS  Google Scholar 

  45. Thomson AM, West DC, Hahn J, Deuchars J (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496 (Pt 1):81–102.

    PubMed  CAS  Google Scholar 

  46. 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.

    Article  PubMed  CAS  Google Scholar 

  47. 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 

  48. Trevelyan AJ, Watkinson O (2005) Does inhibition balance excitation in neocortex? Prog Biophys Mol Biol 87:109–143.

    Article  PubMed  Google Scholar 

  49. Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19:9587–9603.

    PubMed  CAS  Google Scholar 

  50. Wang XJ, Buzsaki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402–6413.

    PubMed  CAS  Google Scholar 

  51. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–446.

    Article  PubMed  CAS  Google Scholar 

  52. 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial support from Ministerio de Ciencia e Innovación (MICINN) to MVSV and AC is acknowledged. RR was partially supported by the FP7 EU (Synthetic Forager FP7- ICT-217148) and by MICINN.

Author information

Authors and Affiliations

  1. Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), 08036, Barcelona, Spain

    Maria V. Sanchez-Vives

  2. Institució Catalana de Recerca i Estudis Avançats (ICREA), 08036, Barcelona, Spain

    Maria V. Sanchez-Vives

Authors
  1. Albert Compte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramon Reig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. 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. Dept. Mathematics, University of Houston, Phillip G. Hoffman Hall 651, Houston, 77204-3008, U.S.A.

    Kre¿imir Josic

  2. Dept. Mathematics, University of Pittsburgh, Thackeray Hall 301, Pittsburgh, 15260, U.S.A.

    Jonathan Rubin

  3. Universitat de les Illes Balears, CSIC, Palma de Mallorca, 07122, Spain

    Manuel Matias

  4. Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico, 04510, Mexico

    Ranulfo Romo

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Compte, A., Reig, R., Sanchez-Vives, M.V. (2009). Timing Excitation and Inhibition in the Cortical Network. In: Josic, K., Rubin, J., Matias, M., Romo, R. (eds) Coherent Behavior in Neuronal Networks. Springer Series in Computational Neuroscience, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0389-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation