Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1994 Apr;66(4):978–988. doi: 10.1016/S0006-3495(94)80879-3

A model of the electrophysiological properties of nucleus reticularis thalami neurons.

G V Wallenstein 1
PMCID: PMC1275805  PMID: 8038402

Abstract

A model of the electrophysiological properties of rodent nucleus reticularis thalami (NRT) neurons of the dorsal lateral thalamus was developed using Hodgkin-Huxley style equations. The model incorporated voltage-dependent rate constants and kinetics obtained from recent voltage-clamp experiments in vitro. The intrinsic electroresponsivity of the model cell was found to be similar to several empirical observations. Three distinct modes of oscillatory activity were identified: 1) a pattern of slow rhythmic burst firing (0.5-7 Hz) usually associated with membrane potentials negative to approximately -70 mV which resulted from the interplay of ITs and IK(Ca); 2) at membrane potentials from approximately -69 to -62 mV, rhythmic burst firing in the spindle frequency range (7-12 Hz) developed and was immediately followed by a tonic tail of single spike firing after several bursts. The initial bursting rhythm resulted from the interaction of ITs and IK(Ca), with a slow after-depolarization due to ICAN which mediated the later tonic firing; 3) with further depolarization of the membrane potential positive to approximately -61 mV, sustained tonic firing appeared in the 10-200-Hz frequency range depending on the amplitude of the injected current. The frequency of this firing was also dependent on the maximum conductance of the leak current, IK(leak), and an interaction between the fast currents involved in generating action potentials, INa(fast) and IK(DR), and the persistent Na+ current, INa(P). Transitions between different firing modes were identified and studied parametrically.

Full text

PDF
978

Selected References

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

  1. Asanuma C. Axonal arborizations of a magnocellular basal nucleus input and their relation to the neurons in the thalamic reticular nucleus of rats. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4746–4750. doi: 10.1073/pnas.86.12.4746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asanuma C. Noradrenergic innervation of the thalamic reticular nucleus: a light and electron microscopic immunohistochemical study in rats. J Comp Neurol. 1992 May 8;319(2):299–311. doi: 10.1002/cne.903190209. [DOI] [PubMed] [Google Scholar]
  3. Avanzini G., de Curtis M., Panzica F., Spreafico R. Intrinsic properties of nucleus reticularis thalami neurones of the rat studied in vitro. J Physiol. 1989 Sep;416:111–122. doi: 10.1113/jphysiol.1989.sp017752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bal T., McCormick D. A. Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. J Physiol. 1993 Aug;468:669–691. doi: 10.1113/jphysiol.1993.sp019794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crunelli V., Leresche N. A role for GABAB receptors in excitation and inhibition of thalamocortical cells. Trends Neurosci. 1991 Jan;14(1):16–21. doi: 10.1016/0166-2236(91)90178-w. [DOI] [PubMed] [Google Scholar]
  6. Deschênes M., Madariaga-Domich A., Steriade M. Dendrodendritic synapses in the cat reticularis thalami nucleus: a structural basis for thalamic spindle synchronization. Brain Res. 1985 May 13;334(1):165–168. doi: 10.1016/0006-8993(85)90580-3. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. French C. R., Sah P., Buckett K. J., Gage P. W. A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol. 1990 Jun;95(6):1139–1157. doi: 10.1085/jgp.95.6.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hallanger A. E., Levey A. I., Lee H. J., Rye D. B., Wainer B. H. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol. 1987 Aug 1;262(1):105–124. doi: 10.1002/cne.902620109. [DOI] [PubMed] [Google Scholar]
  11. Harris R. M. Axon collaterals in the thalamic reticular nucleus from thalamocortical neurons of the rat ventrobasal thalamus. J Comp Neurol. 1987 Apr 15;258(3):397–406. doi: 10.1002/cne.902580308. [DOI] [PubMed] [Google Scholar]
  12. Huguenard J. R., Coulter D. A., Prince D. A. A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. J Neurophysiol. 1991 Oct;66(4):1304–1315. doi: 10.1152/jn.1991.66.4.1304. [DOI] [PubMed] [Google Scholar]
  13. Huguenard J. R., Hamill O. P., Prince D. A. Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol. 1988 Mar;59(3):778–795. doi: 10.1152/jn.1988.59.3.778. [DOI] [PubMed] [Google Scholar]
  14. Huguenard J. R., Prince D. A. A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci. 1992 Oct;12(10):3804–3817. doi: 10.1523/JNEUROSCI.12-10-03804.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kay A. R., Wong R. K. Calcium current activation kinetics in isolated pyramidal neurones of the Ca1 region of the mature guinea-pig hippocampus. J Physiol. 1987 Nov;392:603–616. doi: 10.1113/jphysiol.1987.sp016799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lavoie B., Parent A. Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol. 1991 Oct 1;312(1):1–18. doi: 10.1002/cne.903120102. [DOI] [PubMed] [Google Scholar]
  19. McCormick D. A. Cellular mechanisms underlying cholinergic and noradrenergic modulation of neuronal firing mode in the cat and guinea pig dorsal lateral geniculate nucleus. J Neurosci. 1992 Jan;12(1):278–289. doi: 10.1523/JNEUROSCI.12-01-00278.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McCormick D. A. Cholinergic and noradrenergic modulation of thalamocortical processing. Trends Neurosci. 1989 Jun;12(6):215–221. doi: 10.1016/0166-2236(89)90125-2. [DOI] [PubMed] [Google Scholar]
  21. McCormick D. A., Huguenard J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol. 1992 Oct;68(4):1384–1400. doi: 10.1152/jn.1992.68.4.1384. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. McCormick D. A., Prince D. A. Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. 1986 Jan 30-Feb 5Nature. 319(6052):402–405. doi: 10.1038/319402a0. [DOI] [PubMed] [Google Scholar]
  24. McCormick D. A., Prince D. A. Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. J Neurophysiol. 1988 Mar;59(3):978–996. doi: 10.1152/jn.1988.59.3.978. [DOI] [PubMed] [Google Scholar]
  25. McCormick D. A., Wang Z. Serotonin and noradrenaline excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. J Physiol. 1991 Oct;442:235–255. doi: 10.1113/jphysiol.1991.sp018791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mulle C., Madariaga A., Deschênes M. Morphology and electrophysiological properties of reticularis thalami neurons in cat: in vivo study of a thalamic pacemaker. J Neurosci. 1986 Aug;6(8):2134–2145. doi: 10.1523/JNEUROSCI.06-08-02134.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nuñez A., Amzica F., Steriade M. Intrinsic and synaptically generated delta (1-4 Hz) rhythms in dorsal lateral geniculate neurons and their modulation by light-induced fast (30-70 Hz) events. Neuroscience. 1992 Nov;51(2):269–284. doi: 10.1016/0306-4522(92)90314-r. [DOI] [PubMed] [Google Scholar]
  28. Partridge L. D., Swandulla D. Calcium-activated non-specific cation channels. Trends Neurosci. 1988 Feb;11(2):69–72. doi: 10.1016/0166-2236(88)90167-1. [DOI] [PubMed] [Google Scholar]
  29. Pinault D., Deschênes M. Voltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo. Neuroscience. 1992 Nov;51(2):245–258. doi: 10.1016/0306-4522(92)90312-p. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Steriade M., Domich L., Oakson G. Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance. J Neurosci. 1986 Jan;6(1):68–81. doi: 10.1523/JNEUROSCI.06-01-00068.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Steriade M., Gloor P., Llinás R. R., Lopes de Silva F. H., Mesulam M. M. Report of IFCN Committee on Basic Mechanisms. Basic mechanisms of cerebral rhythmic activities. Electroencephalogr Clin Neurophysiol. 1990 Dec;76(6):481–508. doi: 10.1016/0013-4694(90)90001-z. [DOI] [PubMed] [Google Scholar]
  34. Steriade M., Llinás R. R. The functional states of the thalamus and the associated neuronal interplay. Physiol Rev. 1988 Jul;68(3):649–742. doi: 10.1152/physrev.1988.68.3.649. [DOI] [PubMed] [Google Scholar]
  35. Traub R. D., Wong R. K., Miles R., Michelson H. A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J Neurophysiol. 1991 Aug;66(2):635–650. doi: 10.1152/jn.1991.66.2.635. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. 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 Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES