Abstract
Sensory information reaches the cerebral cortex through the thalamus, which differentially relays this input depending on the state of arousal1,2,3,4,5. Such ‘gating’ involves inhibition of the thalamocortical relay neurons by the reticular nucleus of the thalamus6,7,8, but the underlying mechanisms are poorly understood. We reconstructed the thalamocortical circuit as an artificial and biological hybrid network in vitro. With visual input simulated as retinal cell activity, we show here that when the gain in the thalamic inhibitory feedback loop is greater than a critical value, the circuit tends towards oscillations—and thus imposes a temporal decorrelation of retinal cell input and thalamic relay output. This results in the functional disconnection of the cortex from the sensory drive, a feature typical of sleep states. Conversely, low gain in the feedback inhibition and the action of noradrenaline, a known modulator of arousal4,9,10, converge to increase input–output correlation in relay neurons. Combining gain control of feedback inhibition and modulation of membrane excitability thus enables thalamic circuits to finely tune the gating of spike transmission from sensory organs to the cortex.
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References
Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996)
Coenen, A. M. L. & Vendrick, A. J. H. Determination of the transfer ratio of cat's geniculate neurons through quasi-intracellular recordings and the relation with the level of alertness. Exp. Brain Res. 14, 227–242 (1972)
Livingstone, M. S. & Hubel, D. H. Effects of sleep and arousal on the processing of visual information in the cat. Nature 291, 554–561 (1981)
Steriade, M., Jones, E. G. & McCormick, D. A. Thalamus, Organization and Function 533–685 (Elsevier Science, Oxford, 1997)
Steriade, M., McCormick, D. A. & Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685 (1993)
Yingling, C. D. & Skinner, J. E. Gating of thalamic input to cerebral cortex by nucleus reticularis thalami. Attention, voluntary contraction and event-related cerebral potentials. Prog. Clin. Neurophysiol. 1, 70–96 (1977)
Ahlsen, G., Lindström, S. & Lo, F. S. Interaction between inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Exp. Brain Res. 58, 134–143 (1985)
Montero, V. M. Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a ‘focal attention’ hypothesis. Neuroscience 91, 805–817 (1999)
McCormick, D. A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39, 337–388 (1992)
Aston-Jones, G., Chiang, C. & Alexinsky, T. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog. Brain. Res. 88, 501–520 (1991)
Le Masson, G., Le Masson, S. & Moulins, M. From conductances to neural network properties: analysis of simple circuits using the hybrid network method. Prog. Biophys. Mol. Biol. 64, 201–220 (1995)
Le Masson, S., Laflaquière, A., Bal, T. & Le Masson, G. Analog circuits for modeling biological neural networks: design and applications. IEEE Trans. Biomed. Eng. 64, 638–645 (1999)
Sharp, A. A., O'Neil, M. B., Abbott, L. F. & Marder, E. Dynamic clamp: computer generated conductances in real neurons. J. Neurophysiol. 69, 992–995 (1993)
Kim, U. & McCormick, D. A. The functional influence of burst and tonic firing mode on synaptic interactions in the thalamus. J. Neurosci. 18, 9500–9516 (1998)
McCormick, D. A. & Bal, T. Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185–215 (1997)
von Krosigk, M., Bal, T. & McCormick, D. A. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261, 361–364 (1993)
Usrey, W. M. & Reid, R. C. Synchronous activity in the visual system. Annu. Rev. Physiol. 61, 435–456 (1999)
Troy, J. B. & Robson, J. G. Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Vis. Neurosci. 9, 535–553 (1992)
Bal, T. & McCormick, D. A. What stops synchronized thalamocortical oscillations? Neuron 17, 297–308 (1996)
Mukherjee, P. & Kaplan, E. Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. J. Neurophysiol. 74, 1222–1242 (1995)
Lee, K. H. & McCormick, D. A. Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17, 309–321 (1996)
Funke, K., Pape, H. C. & Eysel, U. T. Noradrenergic modulation of retinogeniculate transmission in the cat. J. Physiol. (Lond.) 463, 169–191 (1993)
Contreras, D., Destexhe, A., Sejnowski, T. J. & Steriade, M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274, 771–774 (1996)
Snead, O. C. III Basic mechanisms of generalized absence seizures. Ann. Neurol. 37, 146–157 (1995)
Bal, T., Debay, D. & Destexhe, A. Cortical feedback controls the frequency and synchrony of oscillations in the visual thalamus. J. Neurosci. 20, 7478–7488 (2000)
Kim, U., Sanchez-Vives, M. V. & McCormick, D. A. Functional dynamics of GABAergic inhibition in the thalamus. Science 278, 130–134 (1997)
McCormick, D. A. & Huguenard, J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68, 1384–1400 (1992)
Destexhe, A., Mainen, Z. F. & Sejnowski, T. J. Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comput. Neurosci. 3, 195–230 (1994)
Destexhe, A., Bal, T., McCormick, D. A. & Sejnowski, T. J. Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J. Neurophysiol. 76, 2049–2070 (1996)
Williams, S. R. & Stuart, G. J. Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J. Neurosci. 15, 1307–1317 (2000)
Acknowledgements
We are grateful to K. Grant, Y. Fregnac, S. Oliet, F. Nagy, A. Destexhe, M. Rudolph and B. Gutkin for in-depth discussion and comments on the manuscript; G. Sadoc, N. Gazère and E. Barbe for their technical input; and A. Destexhe for theoretical simulations. This research was supported by the Groupement d'Intérêt Scientifique Sciences de la Cognition, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Plan Pluriformation du Ministère de la Recherche, Fondation pour la Recherche sur l'Epilepsie, and the Institut Electricité Santé de France.
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Le Masson, G., Renaud-Le Masson, S., Debay, D. et al. Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417, 854–858 (2002). https://doi.org/10.1038/nature00825
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DOI: https://doi.org/10.1038/nature00825
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