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. 1996 Jul 1;494(Pt 1):265–278. doi: 10.1113/jphysiol.1996.sp021489

Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat.

I Timofeev 1, D Contreras 1, M Steriade 1
PMCID: PMC1160628  PMID: 8814620

Abstract

1. The fluctuations during various phases of the slow sleep oscillation (< 1 Hz) in synaptic responsiveness of motor cortical (Cx), thalamic reticular (RE) and thalamocortical (TC) neurones were investigated intracellularly in cats under ketamine-xylazine anaesthesia. Orthodromic responses to stimuli applied to brachium conjunctivum (BC) axons and corticothalamic pathways were studied. The phases of slow oscillation consist of a long-hyperpolarized, followed by a sharp depth-negative EEG deflection and a series of faster waves that are associated with the depolarization of Cx and RE neurones, while TC cells display a sequence of IPSPs within the spindle frequency. 2. BC-evoked bisynaptic excitatory postsynaptic potentials (EPSPs) in Cx and RE neurones were drastically reduced in amplitude during the long-lasting hyperpolarization and the early part of the depolarizing phase. By contrast, the BC-evoked monosynaptic EPSPs of TC cells were not diminished during the depth-positive EEG wave, but the hyperpolarization during this phase of the slow oscillation prevented TC neurones transferring prethalamic signals to the cortex. 3. At variance with the diminished bisynaptic EPSPs evoked in response to BC stimuli during the long-lasting hyperpolarization, Cx-evoked monosynaptic EPSPs in Cx cells increased linearly with hyperpolarization during this phase of the slow oscillation. Similarly, the amplitudes of Cx-evoked EPSPs in RE and TC cells were not diminished during the long-lasting hyperpolarization. 4. The diminished responsiveness of Cx and RE neurones to prethalamic volleys during the long-lasting hyperpolarization is attributed to gating processes at the level of TC cells that, because of their hyperpolarization, do not transfer prethalamic information to further relays.

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Selected References

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  1. Ando N., Izawa Y., Shinoda Y. Relative contributions of thalamic reticular nucleus neurons and intrinsic interneurons to inhibition of thalamic neurons projecting to the motor cortex. J Neurophysiol. 1995 Jun;73(6):2470–2485. doi: 10.1152/jn.1995.73.6.2470. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Contreras D., Steriade M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci. 1995 Jan;15(1 Pt 2):604–622. doi: 10.1523/JNEUROSCI.15-01-00604.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Contreras D., Steriade M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J Physiol. 1996 Jan 1;490(Pt 1):159–179. doi: 10.1113/jphysiol.1996.sp021133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Contreras D., Timofeev I., Steriade M. Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol. 1996 Jul 1;494(Pt 1):251–264. doi: 10.1113/jphysiol.1996.sp021488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crunelli V., Haby M., Jassik-Gerschenfeld D., Leresche N., Pirchio M. Cl- - and K+-dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. J Physiol. 1988 May;399:153–176. doi: 10.1113/jphysiol.1988.sp017073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Curró Dossi R., Paré D., Steriade M. Short-lasting nicotinic and long-lasting muscarinic depolarizing responses of thalamocortical neurons to stimulation of mesopontine cholinergic nuclei. J Neurophysiol. 1991 Mar;65(3):393–406. doi: 10.1152/jn.1991.65.3.393. [DOI] [PubMed] [Google Scholar]
  8. Glenn L. L., Steriade M. Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. J Neurosci. 1982 Oct;2(10):1387–1404. doi: 10.1523/JNEUROSCI.02-10-01387.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guido W., Lu S. M., Vaughan J. W., Godwin D. W., Sherman S. M. Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode. Vis Neurosci. 1995 Jul-Aug;12(4):723–741. doi: 10.1017/s0952523800008993. [DOI] [PubMed] [Google Scholar]
  10. Guido W., Weyand T. Burst responses in thalamic relay cells of the awake behaving cat. J Neurophysiol. 1995 Oct;74(4):1782–1786. doi: 10.1152/jn.1995.74.4.1782. [DOI] [PubMed] [Google Scholar]
  11. Hirsch J. C., Fourment A., Marc M. E. Sleep-related variations of membrane potential in the lateral geniculate body relay neurons of the cat. Brain Res. 1983 Jan 24;259(2):308–312. doi: 10.1016/0006-8993(83)91264-7. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Jones E. G., Powell T. P. Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc R Soc Lond B Biol Sci. 1969 Mar 11;172(1027):153–171. doi: 10.1098/rspb.1969.0017. [DOI] [PubMed] [Google Scholar]
  14. Livingstone M. S., Hubel D. H. Effects of sleep and arousal on the processing of visual information in the cat. Nature. 1981 Jun 18;291(5816):554–561. doi: 10.1038/291554a0. [DOI] [PubMed] [Google Scholar]
  15. Nuñez A., Curró Dossi R., Contreras D., Steriade M. Intracellular evidence for incompatibility between spindle and delta oscillations in thalamocortical neurons of cat. Neuroscience. 1992;48(1):75–85. doi: 10.1016/0306-4522(92)90339-4. [DOI] [PubMed] [Google Scholar]
  16. Steriade M., Amzica F., Contreras D. Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci. 1996 Jan;16(1):392–417. doi: 10.1523/JNEUROSCI.16-01-00392.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Steriade M., Amzica F., Nuñez A. Cholinergic and noradrenergic modulation of the slow (approximately 0.3 Hz) oscillation in neocortical cells. J Neurophysiol. 1993 Oct;70(4):1385–1400. doi: 10.1152/jn.1993.70.4.1385. [DOI] [PubMed] [Google Scholar]
  18. Steriade M., Apostol V., Oakson G. Control of unitary activities in cerebellothalamic pathway during wakefulness and synchronized sleep. J Neurophysiol. 1971 May;34(3):389–413. doi: 10.1152/jn.1971.34.3.389. [DOI] [PubMed] [Google Scholar]
  19. Steriade M., Contreras D., Curró Dossi R., Nuñez A. The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci. 1993 Aug;13(8):3284–3299. doi: 10.1523/JNEUROSCI.13-08-03284.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Steriade M., Datta S., Paré D., Oakson G., Curró Dossi R. C. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci. 1990 Aug;10(8):2541–2559. doi: 10.1523/JNEUROSCI.10-08-02541.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Steriade M., Deschênes M., Domich L., Mulle C. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol. 1985 Dec;54(6):1473–1497. doi: 10.1152/jn.1985.54.6.1473. [DOI] [PubMed] [Google Scholar]
  23. Steriade M., Iosif G., Apostol V. Responsiveness of thalamic and cortical motor relays during arousal and various stages of sleep. J Neurophysiol. 1969 Mar;32(2):251–265. doi: 10.1152/jn.1969.32.2.251. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Steriade M., Morin D. Reticular influences on primary and augmenting responses in the somatosensory cortex. Brain Res. 1981 Jan 26;205(1):67–80. doi: 10.1016/0006-8993(81)90720-4. [DOI] [PubMed] [Google Scholar]
  26. Steriade M., Nuñez A., Amzica F. Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci. 1993 Aug;13(8):3266–3283. doi: 10.1523/JNEUROSCI.13-08-03266.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Williams J. A., Comisarow J., Day J., Fibiger H. C., Reiner P. B. State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis. J Neurosci. 1994 Sep;14(9):5236–5242. doi: 10.1523/JNEUROSCI.14-09-05236.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

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