Skip to main content

The Fine Structure of Slow-Wave Sleep Oscillations: from Single Neurons to Large Networks

  • Chapter
Sleep and Anesthesia

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 15))

Abstract

This chapter reviews experiments, analyses and models of neuronal activity in the thalamus and cerebral cortex during wake and sleep states. The emphasis is on how the microscopic (units, intracellular) and macroscopic (LFPs, EEG) activity organizes within the different states. In a first part, the correspondence between electroencephalogram (EEG) oscillations and neuronal activity is reviewed. Two types of oscillations are then examined in more detail: spindle (7–14 Hz) and slow (0.1–4 Hz) oscillations. For each, experiments and models are contrasted. Implications of these experimental and modeling results onto the role of slow-wave sleep in consolidating memories are discussed.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

Similar content being viewed by others

Notes

  1. 1.

    The absolute conductance is lower in activated states compared to Up-states, but both states are characterized by similar ratios between excitatory and inhibitory conductances (Rudolph et al. 2005).

References

  • Bal T, Debay D, Destexhe A (2000) Cortical feedback controls the frequency and synchrony of oscillations in the visual thalamus. J Neurosci 20(7478):7478–7488

    PubMed  CAS  Google Scholar 

  • Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem 11:697–704

    Article  PubMed  Google Scholar 

  • Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (1999) Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABA a receptor potentials. Nat Neurosci 2:168–174

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Berger H (1929) Über den zeitlichen verlauf der negativen schwankung des nervenstroms. Arch Ges Physiol 1:173

    Google Scholar 

  • Blethyn KL, Hughes SW, Tóth TI, Cope DW, Crunelli V (2006) Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J Neurosci 26:2474–2486

    Article  PubMed  CAS  Google Scholar 

  • Blumenfeld H, McCormick DA (2000) Corticothalamic inputs control the pattern of activity generated in thalamocortical networks. J Neurosci 20:5153–5162

    PubMed  CAS  Google Scholar 

  • Brette R, Gerstner W (2005) Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol 94:3637–3642

    Article  PubMed  Google Scholar 

  • Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8:183–208

    Article  PubMed  CAS  Google Scholar 

  • Buzsaki G (2006) Rhythms of the Brain. Oxford University Press, London

    Book  Google Scholar 

  • 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 

  • Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99–104

    Article  PubMed  CAS  Google Scholar 

  • Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604–622

    PubMed  CAS  Google Scholar 

  • Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996a) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771–774

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Contreras D, Destexhe A, Steriade M (1997) Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J Neurophysiol 78:335–350

    PubMed  CAS  Google Scholar 

  • 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 

  • Destexhe A (1992) Nonlinear dynamics of the rhythmical activity of the brain. PhD thesis, Université Libre de Bruxelles, Brussels, Belgium. http://cns.iaf.cnrs-gif.fr/alain_thesis.html

  • Destexhe A (1998) Spike-and-wave oscillations based on the properties of GABA b receptors. J Neurosci 18:9099–9111

    PubMed  CAS  Google Scholar 

  • Destexhe A (2009) Self-sustained asynchronous irregular states and up/down states in thalamic, cortical and thalamocortical networks of nonlinear integrate-and-fire neurons. J Comput Neurosci 27:493–506

    Article  PubMed  Google Scholar 

  • Destexhe A, Sejnowski TJ (2001) Thalamocortical Assemblies. Monographs of the Physiological Society. Oxford University Press, London

    Google Scholar 

  • Destexhe A, Sejnowski TJ (2003) Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol Rev 83:1401–1453

    PubMed  CAS  Google Scholar 

  • Destexhe A, Babloyantz A, Sejnowski TJ (1993) Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. Biophys J 65:1538–1552

    Article  PubMed  CAS  Google Scholar 

  • Destexhe A, Contreras D, Sejnowski TJ, Steriade M (1994a) A model of spindle rhythmicity in the isolated thalamic reticular nucleus. J Neurophysiol 72:803–818

    PubMed  CAS  Google Scholar 

  • Destexhe A, Contreras D, Sejnowski TJ, Steriade M (1994b) Modeling the control of reticular thalamic oscillations by neuromodulators. Neuroreport 5:2217–2220

    Article  PubMed  CAS  Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1994c) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput 6:14–18

    Article  Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1994d) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1:195–230

    Article  PubMed  CAS  Google Scholar 

  • Destexhe A, Bal T, McCormick DA, Sejnowski TJ (1996) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J Neurophysiol 76:2049–2070

    PubMed  CAS  Google Scholar 

  • Destexhe A, Contreras D, Steriade M (1998) Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 79:999–1016

    PubMed  CAS  Google Scholar 

  • Destexhe A, Contreras D, Steriade M (1999a) Cortically-induced coherence of a thalamic-generated oscillation. Neuroscience 92:427–443

    Article  PubMed  CAS  Google Scholar 

  • Destexhe A, Contreras D, Steriade M (1999b) Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J Neurosci 19:4595–4608

    PubMed  CAS  Google Scholar 

  • Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic ‘up’ states fragments of wakefulness? Trends Neurosci 30:334–342

    Article  PubMed  CAS  Google Scholar 

  • El Boustani S, Pospischil M, Rudolph-Lilith M, Destexhe A (2007) Activated cortical states: experiments, analyses and models. J Physiol Paris 101:99–109

    Article  PubMed  Google Scholar 

  • Gloor P, Fariello RG (1988) Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci 11:63–68

    Article  PubMed  CAS  Google Scholar 

  • Golomb D, Wang XJ, Rinzel J (1996) Propagation of spindle waves in a thalamic slice model. J Neurophysiol 75:750–769

    PubMed  CAS  Google Scholar 

  • Golshani P, Liu XB, Jones EG (2001) Differences in quantal amplitude reflect glur4-subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc Natl Acad Sci USA 98:4172–4177

    Article  PubMed  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Huntsman MM, Porcello DM, Homanics GE, DeLorey TM, Huguenard JR (1999) Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 283:541–543

    Article  PubMed  CAS  Google Scholar 

  • Jahnsen H, Llinás RR (1984) Electrophysiological properties of guinea-pig thalamic neurons: an in vitro study. J Physiol Lond 349:205–226

    PubMed  CAS  Google Scholar 

  • Kim U, Bal T, McCormick DA (1995) Spindle waves are propagating synchronized oscillations in the ferret lgnd in vitro. J Neurophysiol 74:1301–1323

    PubMed  CAS  Google Scholar 

  • Kumar A, Schrader S, Aertsen A, Rotter S (2008) The high-conductance state of cortical networks. Neural Comput 20:1–43

    Article  PubMed  Google Scholar 

  • Lüthi A, McCormick DA (1998) Periodicity of thalamic synchronized oscillations: the role of Ca2+-mediated upregulation of I h . Neuron 20:553–563

    Article  PubMed  Google Scholar 

  • McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337–388

    Article  PubMed  CAS  Google Scholar 

  • Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12:919–926

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro S, Gervasoni D, Soares ES, Zhou Y, Lin SC, Pantoja J, Lavine M, Nicolelis MAL (2004) Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2:126–137

    Article  Google Scholar 

  • 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 94:2805–2821

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • Scheibel ME, Scheibel AB (1966) Patterns of organization in specific and nonspecific thalamic fields. In: DA P, M Y (eds) The thalamus. Columbia University Press, New York, pp 13–46

    Google Scholar 

  • Scheibel ME, Scheibel AB (1967) Structural organization of nonspecific thalamic nuclei and their projection toward cortex. Brain Res 6:60–94

    Article  PubMed  CAS  Google Scholar 

  • Sirota A, Csicsvari J, Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100:2065–2069

    Article  PubMed  CAS  Google Scholar 

  • Steriade M (2003) Neuronal substrates of sleep and epilepsy. Cambridge University Press, Cambridge

    Google Scholar 

  • Steriade M (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86:1–39

    PubMed  CAS  Google Scholar 

  • Steriade M, Deschênes M (1984) The thalamus as a neuronal oscillator. Brain Res 8:1–63

    Article  Google Scholar 

  • Steriade M, Contreras D, Curró Dossi R, Nunez A (1993a) The slow (<1 Hz) oscillation in reticular thalamus and thalamocortical neurons. Scenario of sleep rhythms generation in interacting thalamic and neocortical networks. J Neurosci 13:3284–3299

    PubMed  CAS  Google Scholar 

  • Steriade M, McCormick DA, Sejnowski TJ (1993b) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:697–685

    Article  Google Scholar 

  • Steriade M, Nunez A, Amzica F (1993c) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266–3282

    PubMed  CAS  Google Scholar 

  • Steriade M, Nunez A, Amzica F (1993d) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252–3265

    PubMed  CAS  Google Scholar 

  • Steriade M, Jones EG, McCormick DA (1997) Thalamus. Elsevier, Amsterdam

    Google Scholar 

  • 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 

  • 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 

  • Timofeev I, Grenier F, Steriade M (2001) Disfacilitation and active inhibition in the neocortex during the natural sleepwake cycle: an intracellular study. Proc Natl Acad Sci USA 98:1924–1929

    Article  PubMed  CAS  Google Scholar 

  • Vogels TP, Rajan K, Abbott LF (2005) Neural network dynamics. Annu Rev Neurosci 28:357–376

    Article  PubMed  CAS  Google Scholar 

  • von Krosigk M, Bal T, McCormick DA (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261:361–364

    Article  Google Scholar 

  • Wang XJ, Rinzel J (1993) Spindle rhythmicity in the reticularis thalami nucleus - synchronization among inhibitory neurons. Neuroscience 53:899–904

    Article  PubMed  CAS  Google Scholar 

  • Wang XJ, Golomb D, Rinzel J (1995) Emergent spindle oscillations and intermittent burst firing in a thalamic model: specific neuronal mechanisms. Proc Natl Acad Sci USA 92:5577–5581

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Research supported by CNRS, ANR (HR-CORTEX grant), the European Community (FET grants FACETS FP6-015879, BRAINSCALES FP7-269921) and the NIH (R01EY020765).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Destexhe .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Destexhe, A., Contreras, D. (2011). The Fine Structure of Slow-Wave Sleep Oscillations: from Single Neurons to Large Networks. In: Hutt, A. (eds) Sleep and Anesthesia. Springer Series in Computational Neuroscience, vol 15. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0173-5_4

Download citation

Publish with us

Policies and ethics