Journal of Neurophysiology, Vol 54, Issue 6 1473-1497, Copyright © 1985 by APS

ARTICLES

Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami

M. Steriade, M. Deschenes, L. Domich and C. Mulle

The effects of depriving thalamic relay and intralaminar nuclei from their reticularis thalami (RE) inputs were investigated in acute and chronic experiments on cat. In acutely prepared animals, two (frontal and parasagittal) thalamic transections were made; extracellular and intracellular recordings were performed in RE-disconnected thalamic nuclei. In chronic experiments, the RE nuclear complex was lesioned by means of kainic acid injections; the activity of RE-deprived thalamocortical neurons was extracellularly studied during wakefulness and synchronized sleep. Two features distinguish RE-deprived nuclei from normal thalamic nuclei: absence of spindle-wave rhythmicity and all-burst activity of neurons. The abolition of spindle-related rhythms (sequences of 7- to 14-Hz waves recurring periodically with a rhythm of 0.1-0.2 Hz) in RE-disconnected thalamic nuclei and ipsilateral neocortical areas contrasted with normal spindling rhythmicity in contralateral EEG leads. Spontaneously occurring, rhythmic, long-lasting inhibitory postsynaptic potentials (IPSPs), as observed in intact preparations, were no longer observed in RE-disconnected thalamic neurons. The remaining inhibitory events consisted of short-duration IPSPs. The possibility that RE nucleus is a pacemaker for spindling rhythms, imposing them through inhibitory projections to target thalamic areas, is supported by our concurrent experiments that indicate RE neurons preserve their rhythmicity after disconnection from their major (cortical and thalamic) input sources. RE-deprived thalamocortical neurons exclusively exhibit high-frequency spike bursts whose intrinsic structure is identical to that of intact thalamic relay cells. Instead of the spindle-related sequences of bursts seen in normal animals, the bursts of RE-disconnected thalamocortical neurons are single events, with a dramatic rhythmicity at 1-2 Hz. The presumed mechanism of this rhythmicity is the periodic activation of a low-threshold somatic conductance whose deinactivation is brought about by temporal integration of short-lasting IPSPs. It is known that high-frequency spike bursts of thalamic relay neurons result from hyperpolarization of cell membrane. We blocked the underlying inhibitory events by bicuculline and reversibly changed the all-burst activity of RE-disconnected neurons into a tonic mode. Since the only activity of RE-deprived thalamocortical neurons consists of burst discharges, we hypothesize that local-circuit GABAergic neurons are released from inhibition after RE disconnection or lesion.

This article has been cited by other articles:

				Z. Zhang, C.-H. Liu, Y.-Q. Yu, K. Fujimoto, Y.-S. Chan, and J. He Corticofugal Projection Inhibits the Auditory Thalamus Through the Thalamic Reticular Nucleus J Neurophysiol, June 1, 2008; 99(6): 2938 - 2945. [Abstract] [Full Text] [PDF]

				P Plaha, S Filipovic, and S S Gill Induction of parkinsonian resting tremor by stimulation of the caudal zona incerta nucleus: a clinical study J. Neurol. Neurosurg. Psychiatry, May 1, 2008; 79(5): 514 - 521. [Abstract] [Full Text] [PDF]

				P. M. Joksovic, A. Doctor, B. Gaston, and S. M. Todorovic Functional Regulation of T-Type Calcium Channels by S-Nitrosothiols in the Rat Thalamus J Neurophysiol, April 1, 2007; 97(4): 2712 - 2721. [Abstract] [Full Text] [PDF]

				S. Pangratz-Fuehrer, U. Rudolph, and J. R. Huguenard Giant Spontaneous Depolarizing Potentials in the Developing Thalamic Reticular Nucleus J Neurophysiol, March 1, 2007; 97(3): 2364 - 2372. [Abstract] [Full Text] [PDF]

				P. M. Joksovic, M. T. Nelson, V. Jevtovic-Todorovic, M. K. Patel, E. Perez-Reyes, K. P. Campbell, C.-C. Chen, and S. M. Todorovic CaV3.2 is the major molecular substrate for redox regulation of T-type Ca2+ channels in the rat and mouse thalamus J. Physiol., July 15, 2006; 574(2): 415 - 430. [Abstract] [Full Text] [PDF]

				V. S. Sohal, S. Pangratz-Fuehrer, U. Rudolph, and J. R. Huguenard Intrinsic and synaptic dynamics interact to generate emergent patterns of rhythmic bursting in thalamocortical neurons. J. Neurosci., April 19, 2006; 26(16): 4247 - 4255. [Abstract] [Full Text] [PDF]

				P. M Joksovic, D. A Bayliss, and S. M Todorovic Different kinetic properties of two T-type Ca2+ currents of rat reticular thalamic neurones and their modulation by enflurane J. Physiol., July 1, 2005; 566(1): 125 - 142. [Abstract] [Full Text] [PDF]

				P. Fuentealba, I. Timofeev, M. Bazhenov, T. J. Sejnowski, and M. Steriade Membrane Bistability in Thalamic Reticular Neurons During Spindle Oscillations J Neurophysiol, January 1, 2005; 93(1): 294 - 304. [Abstract] [Full Text] [PDF]

				P. Fuentealba, I. Timofeev, and M. Steriade From The Cover: Prolonged hyperpolarizing potentials precede spindle oscillations in the thalamic reticular nucleus PNAS, June 29, 2004; 101(26): 9816 - 9821. [Abstract] [Full Text] [PDF]

				K. H. Lee, C. Broberger, U. Kim, and D. A. McCormick Histamine modulates thalamocortical activity by activating a chloride conductance in ferret perigeniculate neurons PNAS, April 27, 2004; 101(17): 6716 - 6721. [Abstract] [Full Text] [PDF]

				A. DESTEXHE and T. J. SEJNOWSKI Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations Physiol Rev, October 1, 2003; 83(4): 1401 - 1453. [Abstract] [Full Text] [PDF]

				J. Mu, W. B. Carden, N. C. Kurukulasuriya, G. M. Alexander, and D. W. Godwin Ethanol Influences on Native T-Type Calcium Current in Thalamic Sleep Circuitry J. Pharmacol. Exp. Ther., October 1, 2003; 307(1): 197 - 204. [Abstract] [Full Text] [PDF]

				M. Salami, C. Itami, T. Tsumoto, and F. Kimura Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex PNAS, May 13, 2003; 100(10): 6174 - 6179. [Abstract] [Full Text] [PDF]

				D. M. Porcello, S. D. Smith, and J. R. Huguenard Actions of U-92032, a T-Type Ca2+ Channel Antagonist, Support a Functional Linkage Between IT and Slow Intrathalamic Rhythms J Neurophysiol, January 1, 2003; 89(1): 177 - 185. [Abstract] [Full Text] [PDF]

				H. J. Tschampa, J. W. Herms, W. J. Schulz-Schaeffer, B. Maruschak, O. Windl, U. Jastrow, I. Zerr, B. J. Steinhoff, S. Poser, and H. A. Kretzschmar Clinical findings in sporadic Creutzfeldt-Jakob disease correlate with thalamic pathology Brain, November 1, 2002; 125(11): 2558 - 2566. [Abstract] [Full Text] [PDF]

				M. Bazhenov, I. Timofeev, M. Steriade, and T. J. Sejnowski Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States J. Neurosci., October 1, 2002; 22(19): 8691 - 8704. [Abstract] [Full Text] [PDF]

				M. Steriade Impact of Network Activities on Neuronal Properties in Corticothalamic Systems J Neurophysiol, July 1, 2001; 86(1): 1 - 39. [Abstract] [Full Text] [PDF]

				L. M. Miller and C. E. Schreiner Stimulus-Based State Control in the Thalamocortical System J. Neurosci., September 15, 2000; 20(18): 7011 - 7016. [Abstract] [Full Text] [PDF]

				M. Bazhenov, I. Timofeev, M. Steriade, and T. Sejnowski Spiking-Bursting Activity in the Thalamic Reticular Nucleus Initiates Sequences of Spindle Oscillations in Thalamic Networks J Neurophysiol, August 1, 2000; 84(2): 1076 - 1087. [Abstract] [Full Text] [PDF]

				V. Tancredi, G. Biagini, M. D'Antuono, J. Louvel, R. Pumain, and M. Avoli Spindle-Like Thalamocortical Synchronization in a Rat Brain Slice Preparation J Neurophysiol, August 1, 2000; 84(2): 1093 - 1097. [Abstract] [Full Text] [PDF]

				J. J. Zhu, W. W. Lytton, J.-T. Xue, and D. J. Uhlrich An Intrinsic Oscillation in Interneurons of the Rat Lateral Geniculate Nucleus J Neurophysiol, February 1, 1999; 81(2): 702 - 711. [Abstract] [Full Text] [PDF]

				V. S. Sohal and J. R. Huguenard Long-Range Connections Synchronize Rather Than Spread Intrathalamic Oscillations: Computational Modeling and In Vitro Electrophysiology J Neurophysiol, October 1, 1998; 80(4): 1736 - 1751. [Abstract] [Full Text] [PDF]

				M. J. Hartmann and J. M. Bower Oscillatory Activity in the Cerebellar Hemispheres of Unrestrained Rats J Neurophysiol, September 1, 1998; 80(3): 1598 - 1604. [Abstract] [Full Text] [PDF]

				F. Debarbieux, J. Brunton, and S. Charpak Effect of Bicuculline on Thalamic Activity: A Direct Blockade of IAHP in Reticularis Neurons J Neurophysiol, June 1, 1998; 79(6): 2911 - 2918. [Abstract] [Full Text] [PDF]

				A. Destexhe, M. Neubig, D. Ulrich, and J. Huguenard Dendritic Low-Threshold Calcium Currents in Thalamic Relay Cells J. Neurosci., May 15, 1998; 18(10): 3574 - 3588. [Abstract] [Full Text] [PDF]

				I. Timofeev and M. Steriade Cellular Mechanisms Underlying Intrathalamic Augmenting Responses of Reticular and Relay Neurons J Neurophysiol, May 1, 1998; 79(5): 2716 - 2729. [Abstract] [Full Text] [PDF]

				A. Destexhe, D. Contreras, and M. Steriade Mechanisms Underlying the Synchronizing Action of Corticothalamic Feedback Through Inhibition of Thalamic Relay Cells J Neurophysiol, February 1, 1998; 79(2): 999 - 1016. [Abstract] [Full Text] [PDF]

				M. V. Sanchez-Vives and D. A. McCormick Functional Properties of Perigeniculate Inhibition of Dorsal Lateral Geniculate Nucleus Thalamocortical Neurons In Vitro J. Neurosci., November 15, 1997; 17(22): 8880 - 8893. [Abstract] [Full Text] [PDF]

				M. V. Sanchez-Vives, T. Bal, and D. A. McCormick Inhibitory Interactions between Perigeniculate GABAergic Neurons J. Neurosci., November 15, 1997; 17(22): 8894 - 8908. [Abstract] [Full Text] [PDF]

				U. Kim, M. V. Sanchez-Vives, and D. A. McCormick Functional Dynamics of GABAergic Inhibition in the Thalamus Science, October 3, 1997; 278(5335): 130 - 134. [Abstract] [Full Text]

				D. Ulrich and J. R. Huguenard GABAA-Receptor-Mediated Rebound Burst Firing and Burst Shunting in Thalamus J Neurophysiol, September 1, 1997; 78(3): 1748 - 1751. [Abstract] [Full Text] [PDF]

				C. L. Cox, J. R. Huguenard, and D. A. Prince Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus PNAS, August 5, 1997; 94(16): 8854 - 8859. [Abstract] [Full Text] [PDF]

				D. Contreras, A. Destexhe, and M. Steriade Intracellular and Computational Characterization of the Intracortical Inhibitory Control of Synchronized Thalamic Inputs In Vivo J Neurophysiol, July 1, 1997; 78(1): 335 - 350. [Abstract] [Full Text] [PDF]

				M. Steriade and I. Timofeev Short-Term Plasticity during Intrathalamic Augmenting Responses in Decorticated Cats J. Neurosci., May 15, 1997; 17(10): 3778 - 3795. [Abstract] [Full Text] [PDF]

				W. W. Lytton, D. Contreras, A. Destexhe, and M. Steriade Dynamic Interactions Determine Partial Thalamic Quiescence in a Computer Network Model of Spike-and-Wave Seizures J Neurophysiol, April 1, 1997; 77(4): 1679 - 1696. [Abstract] [Full Text] [PDF]

				D. Contreras, A. Destexhe, T. J. Sejnowski, and M. Steriade Spatiotemporal Patterns of Spindle Oscillations in Cortex and Thalamus J. Neurosci., February 1, 1997; 17(3): 1179 - 1196. [Abstract] [Full Text] [PDF]

				R. A. Warren and E. G. Jones Maturation of Neuronal Form and Function in a Mouse Thalamo-Cortical Circuit J. Neurosci., January 1, 1997; 17(1): 277 - 295. [Abstract] [Full Text] [PDF]

				M Steriade, D. McCormick, and T. Sejnowski Thalamocortical oscillations in the sleeping and aroused brain Science, October 29, 1993; 262(5134): 679 - 685. [Abstract] [PDF]

				M von Krosigk, T Bal, and D. McCormick Cellular mechanisms of a synchronized oscillation in the thalamus Science, July 16, 1993; 261(5119): 361 - 364. [Abstract] [PDF]

				R. Greene, H. Haas, and R. McCarley A low threshold calcium spike mediates firing pattern alterations in pontine reticular neurons Science, November 7, 1986; 234(4777): 738 - 740. [Abstract] [PDF]

				M. Steriade The GABAergic reticular nucleus: A preferential target of corticothalamic projections PNAS, March 27, 2001; 98(7): 3625 - 3627. [Full Text] [PDF]