Analysis of bursting in a thalamic neuron model

We extend a quantitative model for low-voltage, slow-wave excitability based on the T-type calcium current (Wang et al. 1991) by juxtaposing it with a Hodgn-Huxley-like model for fast sodium spiking in the high voltage regime to account for the distinct firing modes of thalamic neurons. We employ bifurcation analysis to illustrate the stimulus-response behavior of the full model under both voltage regimes. The model neuron shows continuous sodium spiking when depolarized sufficiently from rest. Depending on the parameters of calcium current inactivation, there are two types of low-voltage responses to a hyperpolarizing current step: a single rebound low threshold spike (LTS) upon release of the step and periodic LTSs. Bursting is seen as sodium spikes ride the LTS crest. In both cases, we analyze the LTS burst response by projecting its trajectory into a fast/slow phase plane. We also use phase plane methods to show that a potassium A-current shifts the threshold for sodium spikes, reducing the number of fast sodium spikes in an LTS burst. It can also annihilate periodic bursting. We extend the previous work of Rose and Hindmarsh (1989a–c) for a thalamic neuron and propose a simpler model for thalamic activity. We consider burst modulation by using a neuromodulator-dependent potassium leakage conductance as a control parameter. These results correspond with experiments showing that the application of certain neurotransmitters can switch firing modes.

[1]  V. I. Krinskiĭ,et al.  [Analysis of the equations of excitable membranes. I. Reduction of the Hodgkins-Huxley equations to a 2d order system]. , 1973, Biofizika.

[2]  D. McCormick,et al.  Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. , 1991, Journal of neurophysiology.

[3]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[4]  J. Hindmarsh,et al.  The assembly of ionic currents in a thalamic neuron I. The three-dimensional model , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[5]  J R Huguenard,et al.  A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. , 1991, Journal of neurophysiology.

[6]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[7]  D. Prince,et al.  Specific petit mal anticonvulsants reduce calcium currents in thalamic neurons , 1989, Neuroscience Letters.

[8]  John Rinzel,et al.  A Formal Classification of Bursting Mechanisms in Excitable Systems , 1987 .

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

[10]  A. Hernández-Cruz,et al.  Identification of two calcium currents in acutely dissociated neurons from the rat lateral geniculate nucleus. , 1989, Journal of neurophysiology.

[11]  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.

[12]  J. Connor,et al.  Neural repetitive firing: modifications of the Hodgkin-Huxley axon suggested by experimental results from crustacean axons. , 1977, Biophysical journal.

[13]  John Rinzel,et al.  Bursting oscillations in an excitable membrane model , 1985 .

[14]  J. Hindmarsh,et al.  The assembly of ionic currents in a thalamic neuron III. The seven-dimensional model , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[15]  Excitability with multiple thresholds. A new mode of dynamic behavior analyzed in a regulated biochemical system. , 1985, Biophysical chemistry.

[16]  E. J. Doedel,et al.  AUTO: a program for the automatic bifurcation analysis of autonomous systems , 1980 .

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

[18]  Kokoz IuM,et al.  [Analysis of the equations of excitable membranes. I. Reduction of the Hodgkins-Huxley equations to a 2d order system]. , 1973 .

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

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

[21]  John R. Huguenard,et al.  Determination of state-dependent processing in Thalamus by single neuron properties and neuromodulators , 1992 .

[22]  J. Hindmarsh,et al.  The assembly of ionic currents in a thalamic neuron. II. The stability and state diagrams , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[23]  J. Rinzel,et al.  A model of the T-type calcium current and the low-threshold spike in thalamic neurons. , 1991, Journal of neurophysiology.

[24]  D. McCormick,et al.  Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. , 1992, Journal of neurophysiology.

[25]  J. Rinzel Excitation dynamics: insights from simplified membrane models. , 1985, Federation proceedings.

[26]  V. Crunelli,et al.  A T‐type Ca2+ current underlies low‐threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. , 1989, The Journal of physiology.

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

[28]  D. Prince,et al.  Slow inactivation of a TEA-sensitive K current in acutely isolated rat thalamic relay neurons. , 1991, Journal of neurophysiology.

[29]  S. Gueron,et al.  Mapping the dynamics of a bursting neuron. , 1993, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  X. Wang Multiple dynamical modes of thalamic relay neurons: Rhythmic bursting and intermittent phase-locking , 1994, Neuroscience.

[31]  G. Aghajanian Modulation of a transient outward current in serotonergic neurones by α1-adrenoceptors , 1985, Nature.

[32]  Nancy Kopell,et al.  Subcellular oscillations and bursting , 1986 .

[33]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

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

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

[36]  J. Hindmarsh,et al.  A model of a thalamic neuron , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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