A model of spindle rhythmicity in the isolated thalamic reticular nucleus.

1. The oscillatory properties of the isolated reticular (RE) thalamus were modeled with the use of compartmental models of RE cells. Hodgkin-Huxley type kinetic models of ionic channels were derived from voltage- and current-clamp data from RE cells. Interactions between interconnected RE cells were simulated with the use of a kinetic model of gamma-aminobutyric acid (GABA) inhibitory synapses. 2. The intrinsic bursting properties of RE cells in the model were due to the presence of a low-threshold Ca2+ current and two Ca(2+)-activated currents. The properties of these model RE cells were compared with RE neurons recorded intracellularly in vivo in cats. 3. Model RE cells densely interconnected with GABAA synapses produced synchronous oscillations at a frequency close to that of spindles (7-14 Hz). Networks of RE neurons organized in a two-dimensional array with only proximal connectivity also exhibited synchronized oscillations in the spindle range. In addition, the proximally connected network showed periods of high and low synchronicity, giving rise to waxing and waning oscillations in the population of RE cells. 4. The spatiotemporal behavior of the network was investigated during waxing and waning oscillations. The waxing and waning emerged as an alternation between periods of desynchronized and synchronized activity, corresponding to periods of irregular and coherent spatial activity. During synchronized periods, the network displayed propagating coherent waves of synchronous activity that had a tendency to form spirals. 5. Networks of model RE neurons fully connected through GABAB synapses exhibited perfectly synchronous oscillations at lower frequencies (0.5-1 Hz), but two-dimensional networks with proximal GABAB connectivity failed to synchronize. 6. These simulations demonstrate that networks of model neurons that include the main intrinsic currents found in RE cells can generate waxing and waning oscillatory activity similar to the spindle rhythmicity observed in the isolated RE nucleus in vivo. The model reveals the interplay between the intrinsic rhythmic properties of RE cells and the fast synaptic interactions in organizing synchronized rhythmicity.

[1]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[2]  R. Morison,et al.  ELECTRICAL ACTIVITY OF THE THALAMUS AND BASAL GANGLIA IN DECORTICATE CATS , 1945 .

[3]  S. Andersson,et al.  Physiological basis of the alpha rhythm , 1968 .

[4]  A. Scheibel,et al.  Specialized organizational patterns within the nucleus reticularis thalami of the cat. , 1972, Experimental neurology.

[5]  D. Perkel,et al.  Motor Pattern Production in Reciprocally Inhibitory Neurons Exhibiting Postinhibitory Rebound , 1974, Science.

[6]  D. Perkel,et al.  Quantitative methods for predicting neuronal behavior , 1981, Neuroscience.

[7]  M. Deschenes,et al.  Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. , 1985, Journal of neurophysiology.

[8]  Mircea Steriade,et al.  Dendrodendritic synapses in the cat reticularis thalami nucleus: a structural basis for thalamic spindle synchronization , 1985, Brain Research.

[9]  E. G. Jones,et al.  The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  G Oakson,et al.  Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. , 1986, The Journal of physiology.

[11]  David A. McCormick,et al.  Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance , 1986, Nature.

[12]  M. Deschenes,et al.  Morphology and electrophysiological properties of reticularis thalami neurons in cat: in vivo study of a thalamic pacemaker , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  G Oakson,et al.  Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus. , 1987, Journal of neurophysiology.

[14]  M. Deschenes,et al.  The deafferented reticular thalamic nucleus generates spindle rhythmicity. , 1987, Journal of neurophysiology.

[15]  M. Curtis,et al.  Electrophysiological characteristics of morphologically identified reticular thalamic neurons from rat slices , 1988, Neuroscience.

[16]  L. D. Partridge,et al.  Calcium-activated non-specific cation channels , 1988, Trends in Neurosciences.

[17]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[19]  A. VanDongen,et al.  Newly identified brain potassium channels gated by the guanine nucleotide binding protein Go. , 1988, Science.

[20]  G Avanzini,et al.  Intrinsic properties of nucleus reticularis thalami neurones of the rat studied in vitro. , 1989, The Journal of physiology.

[21]  D. Prince,et al.  Printed in Great Britain , 2005 .

[22]  C. Koch,et al.  Multiple channels and calcium dynamics , 1989 .

[23]  E. G. Jones,et al.  Thalamic oscillations and signaling , 1990 .

[24]  D. McCormick,et al.  Properties of a hyperpolarization‐activated cation current and its role in rhythmic oscillation in thalamic relay neurones. , 1990, The Journal of physiology.

[25]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[26]  D. McCormick,et al.  Serotonin and noradrenaline excite GABAergic neurones of the guinea‐pig and cat nucleus reticularis thalami. , 1991, The Journal of physiology.

[27]  R. Traub,et al.  Neuronal Networks of the Hippocampus , 1991 .

[28]  I. Soltesz,et al.  Two inward currents and the transformation of low‐frequency oscillations of rat and cat thalamocortical cells. , 1991, The Journal of physiology.

[29]  A. Depaulis,et al.  Involvement of intrathalamic GABA b neurotransmission in the control of absence seizures in the rat , 1992, Neuroscience.

[30]  D. McCormick,et al.  A model of the electrophysiological properties of thalamocortical relay neurons. , 1992, Journal of neurophysiology.

[31]  V. Crunelli,et al.  Computer simulation of the pacemaker oscillations of thalamocortical cells. , 1992, Neuroreport.

[32]  W. A. Wilson,et al.  The role of GABAB receptor activation in absence seizures of lethargic (lh/lh) mice. , 1992, Science.

[33]  A. Babloyantz,et al.  Cortical Coherent Activity Induced by Thalamic Oscillations , 1992 .

[34]  D. Prince,et al.  A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Xiao-Jing Wang,et al.  Alternating and Synchronous Rhythms in Reciprocally Inhibitory Model Neurons , 1992, Neural Computation.

[36]  I. Mody,et al.  Modulation of decay kinetics and frequency of GABAA receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal neurons , 1992, Neuroscience.

[37]  T. Sejnowski,et al.  Computer model of ethosuximide's effect on a thalamic neuron , 1992, Annals of neurology.

[38]  P. Gage Activation and modulation of neuronal K+ channels by GABA , 1992, Trends in Neurosciences.

[39]  D. McCormick,et al.  Mechanisms of oscillatory activity in guinea‐pig nucleus reticularis thalami in vitro: a mammalian pacemaker. , 1993, The Journal of physiology.

[40]  T. Sejnowski,et al.  A model for 8-10 Hz spindling in interconnected thalamic relay and reticularis neurons. , 1993, Biophysical journal.

[41]  Golomb,et al.  Dynamics of globally coupled inhibitory neurons with heterogeneity. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[42]  A. Selverston,et al.  Modeling the gastric mill central pattern generator of the lobster with a relaxation-oscillator network. , 1993, Journal of neurophysiology.

[43]  D Contreras,et al.  Electrophysiological properties of cat reticular thalamic neurones in vivo. , 1993, The Journal of physiology.

[44]  Michael L. Hines,et al.  NEURON — A Program for Simulation of Nerve Equations , 1993 .

[45]  I. Módy,et al.  Characterization of synaptically elicited GABAB responses using patch‐clamp recordings in rat hippocampal slices. , 1993, The Journal of physiology.

[46]  D. McCormick,et al.  Cellular mechanisms of a synchronized oscillation in the thalamus. , 1993, Science.

[47]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[48]  J. Rinzel,et al.  Spindle rhythmicity in the reticularis thalami nucleus: Synchronization among mutually inhibitory neurons , 1993, Neuroscience.

[49]  T J Sejnowski,et al.  Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. , 1993, Biophysical journal.

[50]  A Babloyantz,et al.  A model of the inward current Ih and its possible role in thalamocortical oscillations. , 1993, Neuroreport.

[51]  Terrence J. Sejnowski,et al.  An Efficient Method for Computing Synaptic Conductances Based on a Kinetic Model of Receptor Binding , 1994, Neural Computation.

[52]  J. Rinzel,et al.  Clustering in globally coupled inhibitory neurons , 1994 .

[53]  F. Segal,et al.  A CHARACTERIZATION OF , 2022 .