Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Jun 6;92(12):5577–5581. doi: 10.1073/pnas.92.12.5577

Emergent spindle oscillations and intermittent burst firing in a thalamic model: specific neuronal mechanisms.

X J Wang 1, D Golomb 1, J Rinzel 1
PMCID: PMC41739  PMID: 7777551

Abstract

The rhythmogenesis of 10-Hz sleep spindles is studied in a large-scale thalamic network model with two cell populations: the excitatory thalamocortical (TC) relay neurons and the inhibitory nucleus reticularis thalami (RE) neurons. Spindle-like bursting oscillations emerge naturally from reciprocal interactions between TC and RE neurons. We find that the network oscillations can be synchronized coherently, even though the RE-TC connections are random and sparse, and even though individual neurons fire rebound bursts intermittently in time. When the fast gamma-aminobutyrate type A synaptic inhibition is blocked, synchronous slow oscillations resembling absence seizures are observed. Near-maximal network synchrony is established with even modest convergence in the RE-to-TC projection (as few as 5-10 RE inputs per TC cell suffice). The hyperpolarization-activated cation current (Ih) is found to provide a cellular basis for the intermittency of rebound bursting that is commonly observed in TC neurons during spindles. Such synchronous oscillations with intermittency can be maintained only with a significant degree of convergence for the TC-to-RE projection.

Full text

PDF
5577

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bal T., von Krosigk M., McCormick D. A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J Physiol. 1995 Mar 15;483(Pt 3):665–685. doi: 10.1113/jphysiol.1995.sp020613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barkai E, Kanter I, I, Sompolinsky H. Properties of sparsely connected excitatory neural networks. Phys Rev A. 1990 Jan 15;41(2):590–597. doi: 10.1103/physreva.41.590. [DOI] [PubMed] [Google Scholar]
  3. Buzsáki G. The thalamic clock: emergent network properties. Neuroscience. 1991;41(2-3):351–364. doi: 10.1016/0306-4522(91)90332-i. [DOI] [PubMed] [Google Scholar]
  4. Deschênes M., Paradis M., Roy J. P., Steriade M. Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. J Neurophysiol. 1984 Jun;51(6):1196–1219. doi: 10.1152/jn.1984.51.6.1196. [DOI] [PubMed] [Google Scholar]
  5. Destexhe A., Contreras D., Sejnowski T. J., Steriade M. A model of spindle rhythmicity in the isolated thalamic reticular nucleus. J Neurophysiol. 1994 Aug;72(2):803–818. doi: 10.1152/jn.1994.72.2.803. [DOI] [PubMed] [Google Scholar]
  6. Destexhe A., McCormick D. A., Sejnowski T. J. A model for 8-10 Hz spindling in interconnected thalamic relay and reticularis neurons. Biophys J. 1993 Dec;65(6):2473–2477. doi: 10.1016/S0006-3495(93)81297-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Golomb D., Wang X. J., Rinzel J. Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. J Neurophysiol. 1994 Sep;72(3):1109–1126. doi: 10.1152/jn.1994.72.3.1109. [DOI] [PubMed] [Google Scholar]
  8. Golomb D, Rinzel J. Dynamics of globally coupled inhibitory neurons with heterogeneity. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1993 Dec;48(6):4810–4814. doi: 10.1103/physreve.48.4810. [DOI] [PubMed] [Google Scholar]
  9. Gray C. M. Synchronous oscillations in neuronal systems: mechanisms and functions. J Comput Neurosci. 1994 Jun;1(1-2):11–38. doi: 10.1007/BF00962716. [DOI] [PubMed] [Google Scholar]
  10. Huguenard J. R., McCormick D. A. Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol. 1992 Oct;68(4):1373–1383. doi: 10.1152/jn.1992.68.4.1373. [DOI] [PubMed] [Google Scholar]
  11. Huguenard J. R., Prince D. A. Clonazepam suppresses GABAB-mediated inhibition in thalamic relay neurons through effects in nucleus reticularis. J Neurophysiol. 1994 Jun;71(6):2576–2581. doi: 10.1152/jn.1994.71.6.2576. [DOI] [PubMed] [Google Scholar]
  12. Huguenard J. R., Prince D. A. Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J Neurosci. 1994 Sep;14(9):5485–5502. doi: 10.1523/JNEUROSCI.14-09-05485.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jahnsen H., Llinás R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol. 1984 Apr;349:227–247. doi: 10.1113/jphysiol.1984.sp015154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kopell N., LeMasson G. Rhythmogenesis, amplitude modulation, and multiplexing in a cortical architecture. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10586–10590. doi: 10.1073/pnas.91.22.10586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leresche N., Lightowler S., Soltesz I., Jassik-Gerschenfeld D., Crunelli V. Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. J Physiol. 1991 Sep;441:155–174. doi: 10.1113/jphysiol.1991.sp018744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McCormick D. A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol. 1992 Oct;39(4):337–388. doi: 10.1016/0301-0082(92)90012-4. [DOI] [PubMed] [Google Scholar]
  17. McCormick D. A., Pape H. C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol. 1990 Dec;431:291–318. doi: 10.1113/jphysiol.1990.sp018331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Otis T. S., De Koninck Y., Mody I. Characterization of synaptically elicited GABAB responses using patch-clamp recordings in rat hippocampal slices. J Physiol. 1993 Apr;463:391–407. doi: 10.1113/jphysiol.1993.sp019600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Steriade M., Deschenes M. The thalamus as a neuronal oscillator. Brain Res. 1984 Nov;320(1):1–63. doi: 10.1016/0165-0173(84)90017-1. [DOI] [PubMed] [Google Scholar]
  20. Steriade M., Domich L., Oakson G., Deschênes M. The deafferented reticular thalamic nucleus generates spindle rhythmicity. J Neurophysiol. 1987 Jan;57(1):260–273. doi: 10.1152/jn.1987.57.1.260. [DOI] [PubMed] [Google Scholar]
  21. Wang X. J., Rinzel J. Spindle rhythmicity in the reticularis thalami nucleus: synchronization among mutually inhibitory neurons. Neuroscience. 1993 Apr;53(4):899–904. doi: 10.1016/0306-4522(93)90474-t. [DOI] [PubMed] [Google Scholar]
  22. von Krosigk M., Bal T., McCormick D. A. Cellular mechanisms of a synchronized oscillation in the thalamus. Science. 1993 Jul 16;261(5119):361–364. doi: 10.1126/science.8392750. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES