Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Science Signaling - Call For Papers

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 3 October 1997:
Vol. 278. no. 5335, pp. 130 - 134
DOI: 10.1126/science.278.5335.130
Prev | Table of Contents | Next

Reports

Functional Dynamics of GABAergic Inhibition in the Thalamus

Uhnoh Kim, Maria V. Sanchez-Vives, David A. McCormick *

The inhibitory gamma -aminobutyric acid-containing (GABAergic) neurons of the thalamic reticular and perigeniculate nuclei are involved in the generation of normal and abnormal synchronized activity in thalamocortical networks. An important factor controlling the generation of activity in this system is the amplitude and duration of inhibitory postsynaptic potentials (IPSPs) in thalamocortical cells, which depend on the pattern of activity generated in thalamic reticular and perigeniculate cells. Activation of single ferret perigeniculate neurons generated three distinct patterns of GABAergic IPSPs in thalamocortical neurons of the dorsal lateral geniculate nucleus: Low-frequency tonic discharge resulted in small-amplitude IPSPs mediated by GABAA receptors, burst firing resulted in large-amplitude GABAA IPSPs, and prolonged burst firing activated IPSPs mediated by GABAA and GABAB receptors. These functional properties of GABAergic inhibition can reconfigure the operations of thalamocortical networks into patterns of activity associated with waking, slow-wave sleep, and generalized seizures.

Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, USA.
*   To whom correspondence should be addressed. E-mail: david.mccormick{at}yale.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Corticofugal Projection Inhibits the Auditory Thalamus Through the Thalamic Reticular Nucleus.
Z. Zhang, C.-H. Liu, Y.-Q. Yu, K. Fujimoto, Y.-S. Chan, and J. He (2008)
J Neurophysiol 99, 2938-2945
   Abstract »    Full Text »    PDF »
Bilateral stimulation of the caudal zona incerta nucleus for tremor control.
P Plaha, S Khan, and S S Gill (2008)
J. Neurol. Neurosurg. Psychiatry 79, 504-513
   Abstract »    Full Text »    PDF »
Embryonically Expressed GABA and Glutamate Drive Electrical Activity Regulating Neurotransmitter Specification.
C. M. Root, N. A. Velazquez-Ulloa, G. C. Monsalve, E. Minakova, and N. C. Spitzer (2008)
J. Neurosci. 28, 4777-4784
   Abstract »    Full Text »    PDF »
VPM and PoM Nuclei of the Rat Somatosensory Thalamus: Intrinsic Neuronal Properties and Corticothalamic Feedback.
C. E. Landisman and B. W. Connors (2007)
Cereb Cortex 17, 2853-2865
   Abstract »    Full Text »    PDF »
Corticofugal modulation of the auditory thalamic reticular nucleus of the guinea pig.
M. Xu, C. H. Liu, Y. Xiong, and J. He (2007)
J. Physiol. 585, 15-28
   Abstract »    Full Text »    PDF »
Mechanisms of Reversible GABAA Receptor Plasticity after Ethanol Intoxication.
J. Liang, A. Suryanarayanan, A. Abriam, B. Snyder, R. W. Olsen, and I. Spigelman (2007)
J. Neurosci. 27, 12367-12377
   Abstract »    Full Text »    PDF »
Cortical and Collicular Inputs to Cells in the Rat Paralaminar Thalamic Nuclei Adjacent to the Medial Geniculate Body.
P. H. Smith, E. L. Bartlett, and A. Kowalkowski (2007)
J Neurophysiol 98, 681-695
   Abstract »    Full Text »    PDF »
Reticular nucleus-specific changes in {alpha}3 subunit protein at GABA synapses in genetically epilepsy-prone rats.
X.-B. Liu, J. Coble, G. van Luijtelaar, and E. G. Jones (2007)
PNAS 104, 12512-12517
   Abstract »    Full Text »    PDF »
Heterogeneity of firing properties among rat thalamic reticular nucleus neurons.
S.-H. Lee, G. Govindaiah, and C. L. Cox (2007)
J. Physiol. 582, 195-208
   Abstract »    Full Text »    PDF »
Modulation of Inhibitory Activity by Nitric Oxide in the Thalamus.
S. Yang and C. L. Cox (2007)
J Neurophysiol 97, 3386-3395
   Abstract »    Full Text »    PDF »
Attentional modulation of thalamic reticular neurons..
K. McAlonan, J. Cavanaugh, and R. H. Wurtz (2006)
J. Neurosci. 26, 4444-4450
   Abstract »    Full Text »    PDF »
Coding of Stimulus Frequency by Latency in Thalamic Networks Through the Interplay of GABAB-Mediated Feedback and Stimulus Shape.
D. Golomb, E. Ahissar, and D. Kleinfeld (2006)
J Neurophysiol 95, 1735-1750
   Abstract »    Full Text »    PDF »
Emergence of disinhibition-induced synchrony in the CA3 region of the guinea pig hippocampus in vitro.
I. Cohen, G. Huberfeld, and R. Miles (2006)
J. Physiol. 570, 583-594
   Abstract »    Full Text »    PDF »
Mapping by Laser Photostimulation of Connections Between the Thalamic Reticular and Ventral Posterior Lateral Nuclei in the Rat.
Y.-W. Lam and S. M. Sherman (2005)
J Neurophysiol 94, 2472-2483
   Abstract »    Full Text »    PDF »
Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex.
A. Simon, S. Olah, G. Molnar, J. Szabadics, and G. Tamas (2005)
J. Neurosci. 25, 6278-6285
   Abstract »    Full Text »    PDF »
Globus Pallidus Neurons Dynamically Regulate the Activity Pattern of Subthalamic Nucleus Neurons through the Frequency-Dependent Activation of Postsynaptic GABAA and GABAB Receptors.
N. E. Hallworth and M. D. Bevan (2005)
J. Neurosci. 25, 6304-6315
   Abstract »    Full Text »    PDF »
Modeling Sleep and Wakefulness in the Thalamocortical System.
S. Hill and G. Tononi (2005)
J Neurophysiol 93, 1671-1698
   Abstract »    Full Text »    PDF »
Molecular Organization of the Ferret Visual Thalamus.
H. Kawasaki, J. C. Crowley, F. J. Livesey, and L. C. Katz (2004)
J. Neurosci. 24, 9962-9970
   Abstract »    Full Text »    PDF »
Corticofugal Gating of Auditory Information in the Thalamus: An In Vivo Intracellular Recording Study.
Y.-Q. Yu, Y. Xiong, Y.-S. Chan, and J. He (2004)
J. Neurosci. 24, 3060-3069
   Abstract »    Full Text »    PDF »
GABA Modulates Presynaptic Signalling Mediated by Dinucleotides on Rat Synaptic Terminals.
R. Gomez-Villafuertes, J. Pintor, J. Gualix, and M. T. Miras-Portugal (2004)
J. Pharmacol. Exp. Ther. 308, 1148-1157
   Abstract »    Full Text »    PDF »
Pathway-Specific Action of {gamma}-Hydroxybutyric Acid in Sensory Thalamus and Its Relevance to Absence Seizures.
N. Gervasi, Z. Monnier, P. Vincent, D. Paupardin-Tritsch, S. W. Hughes, V. Crunelli, and N. Leresche (2003)
J. Neurosci. 23, 11469-11478
   Abstract »    Full Text »    PDF »
Target-Specific Neuropeptide Y-Ergic Synaptic Inhibition and Its Network Consequences within the Mammalian Thalamus.
Q.-Q. Sun, S. C. Baraban, D. A. Prince, and J. R. Huguenard (2003)
J. Neurosci. 23, 9639-9649
   Abstract »    Full Text »    PDF »
Inhibitory Interconnections Control Burst Pattern and Emergent Network Synchrony in Reticular Thalamus.
V. S. Sohal and J. R. Huguenard (2003)
J. Neurosci. 23, 8978-8988
   Abstract »    Full Text »    PDF »
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations.
A. DESTEXHE and T. J. SEJNOWSKI (2003)
Physiol Rev 83, 1401-1453
   Abstract »    Full Text »    PDF »
Sedation and Anesthesia Mediated by Distinct GABAA Receptor Isoforms.
D. S. Reynolds, T. W. Rosahl, J. Cirone, G. F. O'Meara, A. Haythornthwaite, R. J. Newman, J. Myers, C. Sur, O. Howell, A. R. Rutter, et al. (2003)
J. Neurosci. 23, 8608-8617
   Abstract »    Full Text »    PDF »
Nature of Inhibitory Postsynaptic Activity in Developing Relay Cells of the Lateral Geniculate Nucleus.
J. Ziburkus, F.-S. Lo, and W. Guido (2003)
J Neurophysiol 90, 1063-1070
   Abstract »    Full Text »    PDF »
Identified Sources and Targets of Slow Inhibition in the Neocortex.
G. Tamas, A. L. A. Simon, and J. Szabadics (2003)
Science 299, 1902-1905
   Abstract »    Full Text »    PDF »
Inhibitory Interactions Between Ferret Thalamic Reticular Neurons.
Y. Shu and D. A. McCormick (2002)
J Neurophysiol 87, 2571-2576
   Abstract »    Full Text »    PDF »
Regulation of the Timing and Pattern of Action Potential Generation in Rat Subthalamic Neurons In Vitro by GABA-A IPSPs.
M. D. Bevan, P. J. Magill, N. E. Hallworth, J. P. Bolam, and C. J. Wilson (2002)
J Neurophysiol 87, 1348-1362
   Abstract »    Full Text »    PDF »
Electrical Synapses in the Thalamic Reticular Nucleus.
C. E. Landisman, M. A. Long, M. Beierlein, M. R. Deans, D. L. Paul, and B. W. Connors (2002)
J. Neurosci. 22, 1002-1009
   Abstract »    Full Text »    PDF »
GABAB and NMDA Receptors Contribute to Spindle-Like Oscillations in Rat Thalamus In Vitro.
R. B. Jacobsen, D. Ulrich, and J. R. Huguenard (2001)
J Neurophysiol 86, 1365-1375
   Abstract »    Full Text »    PDF »
Muscarinic Regulation of Dendritic and Axonal Outputs of Rat Thalamic Interneurons: A New Cellular Mechanism for Uncoupling Distal Dendrites.
J. J. Zhu and P. Heggelund (2001)
J. Neurosci. 21, 1148-1159
   Abstract »    Full Text »    PDF »
C-Terminal Interaction Is Essential for Surface Trafficking But Not for Heteromeric Assembly of GABAB Receptors.
A. Pagano, G. Rovelli, J. Mosbacher, T. Lohmann, B. Duthey, D. Stauffer, D. Ristig, V. Schuler, I. Meigel, C. Lampert, et al. (2001)
J. Neurosci. 21, 1189-1202
   Abstract »    Full Text »    PDF »
Contribution of GABAA and GABAB Receptors to Thalamic Neuronal Activity during Spontaneous Absence Seizures in Rats.
R. Staak and H.-C. Pape (2001)
J. Neurosci. 21, 1378-1384
   Abstract »    Full Text »    PDF »
Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning.
K. McAlonan, V. J. Brown, and E. M. Bowman (2000)
J. Neurosci. 20, 8897-8901
   Abstract »    Full Text »    PDF »
Cortical Feedback Controls the Frequency and Synchrony of Oscillations in the Visual Thalamus.
T. Bal, D. Debay, and A. Destexhe (2000)
J. Neurosci. 20, 7478-7488
   Abstract »    Full Text »    PDF »
Modulation of Absence Seizures by the GABAA Receptor: A Critical Role for Metabotropic Glutamate Receptor 4 (mGluR4).
O. C. Snead III, P. K. Banerjee, M. Burnham, and D. Hampson (2000)
J. Neurosci. 20, 6218-6224
   Abstract »    Full Text »    PDF »
Corticothalamic Inputs Control the Pattern of Activity Generated in Thalamocortical Networks.
H. Blumenfeld and D. A. McCormick (2000)
J. Neurosci. 20, 5153-5162
   Abstract »    Full Text »    PDF »
Functional Correlation of GABAA Receptor alpha Subunits Expression with the Properties of IPSCs in the Developing Thalamus.
M. Okada, K. Onodera, C. Van Renterghem, W. Sieghart, and T. Takahashi (2000)
J. Neurosci. 20, 2202-2208
   Abstract »    Full Text »    PDF »
Regionally Selective Blockade of GABAergic Inhibition by Zinc in the Thalamocortical System: Functional Significance.
J. W. Gibbs III, Y.-F. Zhang, M. D. Shumate, and D. A. Coulter (2000)
J Neurophysiol 83, 1510-1521
   Abstract »    Full Text »    PDF »
Attentional Orienting Is Impaired by Unilateral Lesions of the Thalamic Reticular Nucleus in the Rat.
G. D. Weese, J. M. Phillips, and V. J. Brown (1999)
J. Neurosci. 19, 10135-10139
   Abstract »    Full Text »    PDF »
Increased gamma - and Decreased delta -Oscillations in a Mouse Deficient for a Potassium Channel Expressed in Fast-Spiking Interneurons.
R. H. Joho, C. S. Ho, and G. A. Marks (1999)
J Neurophysiol 82, 1855-1864
   Abstract »    Full Text »    PDF »
Glutamate Inhibits Thalamic Reticular Neurons.
C. L. Cox and S. M. Sherman (1999)
J. Neurosci. 19, 6694-6699
   Abstract »    Full Text »    PDF »
Correlational Structure of Spontaneous Neuronal Activity in the Developing Lateral Geniculate Nucleus in Vivo.
M. Weliky and L. C. Katz (1999)
Science 285, 599-604
   Abstract »    Full Text »
Three GABA Receptor-Mediated Postsynaptic Potentials in Interneurons in the Rat Lateral Geniculate Nucleus.
J. J. Zhu and F.-S. Lo (1999)
J. Neurosci. 19, 5721-5730
   Abstract »    Full Text »    PDF »
Role of GABAB Receptor-Mediated Inhibition in Reciprocal Interareal Pathways of Rat Visual Cortex.
Z. Shao and A. Burkhalter (1999)
J Neurophysiol 81, 1014-1024
   Abstract »    Full Text »    PDF »
Reciprocal Inhibitory Connections and Network Synchrony in the Mammalian Thalamus.
M. M. Huntsman, D. M. Porcello, G. E. Homanics, T. M. DeLorey, and J. R. Huguenard (1999)
Science 283, 541-543
   Abstract »    Full Text »
Lack of tactile pain (allodynia) in lipocalin-type prostaglandin D synthase-deficient mice.
N. Eguchi, T. Minami, N. Shirafuji, Y. Kanaoka, T. Tanaka, A. Nagata, N. Yoshida, Y. Urade, S. Ito, and O. Hayaishi (1999)
PNAS 96, 726-730
   Abstract »    Full Text »    PDF »
The Functional Influence of Burst and Tonic Firing Mode on Synaptic Interactions in the Thalamus.
U. Kim and D. A. McCormick (1998)
J. Neurosci. 18, 9500-9516
   Abstract »    Full Text »    PDF »
Spike-and-Wave Oscillations Based on the Properties of GABAB Receptors.
A. Destexhe (1998)
J. Neurosci. 18, 9099-9111
   Abstract »    Full Text »    PDF »
Functional and Ionic Properties of a Slow Afterhyperpolarization in Ferret Perigeniculate Neurons In Vitro.
U. Kim and D. A. Mccormick (1998)
J Neurophysiol 80, 1222-1235
   Abstract »    Full Text »    PDF »
Effect of Bicuculline on Thalamic Activity: A Direct Blockade of IAHP in Reticularis Neurons.
F. Debarbieux, J. Brunton, and S. Charpak (1998)
J Neurophysiol 79, 2911-2918
   Abstract »    Full Text »    PDF »
Propagating Activity Patterns in Large-Scale Inhibitory Neuronal Networks.
J. Rinzel, D. Terman, X. Wang, and B. Ermentrout (1998)
Science 279, 1351-1355
   Abstract »    Full Text »
Functional Properties of Perigeniculate Inhibition of Dorsal Lateral Geniculate Nucleus Thalamocortical Neurons In Vitro.
M. V. Sanchez-Vives and D. A. McCormick (1997)
J. Neurosci. 17, 8880-8893
   Abstract »    Full Text »    PDF »
Inhibitory Interactions between Perigeniculate GABAergic Neurons.
M. V. Sanchez-Vives, T. Bal, and D. A. McCormick (1997)
J. Neurosci. 17, 8894-8908
   Abstract »    Full Text »    PDF »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)