Synchrony of Fast-Spiking Interneurons Interconnected by GABAergic and Electrical Synapses

Fast-spiking (FS) interneurons have specific types (Kv3.1/3.2 type) of the delayed potassium channel, which differ from the conventional Hodgkin-Huxley (HH) type potassium channel (Kv1.3 type) in several aspects. In this study, we show dramatic effects of the Kv3.1/3.2 potassium channel on the synchronization of the FS interneurons. We show analytically that two identical electrically coupled FS interneurons modeled with Kv3.1/3.2 channel fire synchronously at arbitrary firing frequencies, unlike similarly coupled FS neurons modeled with Kv1.3 channel that show frequency-dependent synchronous and antisynchronous firing states. Introducing GABA A receptor-mediated synaptic connections into an FS neuron pair tends to induce an antisynchronous firing state, even if the chemical synapses are bidirectional. Accordingly, an FS neuron pair connected simultaneously by electrical and chemical synapses achieves both synchronous firing state and antisynchronous firing state in a physiologically plausible range of the conductance ratio between electrical and chemical synapses. Moreover, we find that a large-scale network of FS interneurons connected by gap junctions and bidirectional GABAergic synapses shows similar bistability in the range of gamma frequencies (3070 Hz).

[1]  A. Erisir,et al.  Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. , 1999, Journal of neurophysiology.

[2]  B. Connors,et al.  A network of electrically coupled interneurons drives synchronized inhibition in neocortex , 2000, Nature Neuroscience.

[3]  S. Hestrin,et al.  Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Bernardo Rudy,et al.  Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing , 2001, Trends in Neurosciences.

[5]  Toshio Aoyagi,et al.  Phase Locking States in Network of Inhibitory Neurons: A Putative Role of Gap Junction , 2002 .

[6]  K. Kaneko.  Clustering, coding, switching, hierarchical ordering, and control in a network of chaotic elements , 1990 .

[7]  J. Rinzel,et al.  Rhythmogenic effects of weak electrotonic coupling in neuronal models. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Frotscher,et al.  Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Bard Ermentrout,et al.  When inhibition not excitation synchronizes neural firing , 1994, Journal of Computational Neuroscience.

[10]  Carson C. Chow,et al.  Frequency Control in Synchronized Networks of Inhibitory Neurons , 1998, Journal of Computational Neuroscience.

[11]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[12]  N Kopell,et al.  Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks , 2001, The Journal of Neuroscience.

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

[14]  Kerry McAlonan,et al.  Thalamic Reticular Nucleus Activation Reflects Attentional Gating during Classical Conditioning , 2000, The Journal of Neuroscience.

[15]  M. Steriade,et al.  Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. , 1998, Journal of neurophysiology.

[16]  Carson C. Chow,et al.  Dynamics of Spiking Neurons with Electrical Coupling , 2000, Neural Computation.

[17]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[18]  G. Ermentrout,et al.  Frequency Plateaus in a Chain of Weakly Coupled Oscillators, I. , 1984 .

[19]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[20]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[21]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Germán Mato,et al.  Synchrony in Excitatory Neural Networks , 1995, Neural Computation.

[23]  Wulfram Gerstner,et al.  What Matters in Neuronal Locking? , 1996, Neural Computation.

[24]  T Fukai,et al.  THE ROLE OF Ca 2 þ-DEPENDENT CATIONIC CURRENT IN GENERATING GAMMA FREQUENCY RHYTHMIC BURSTS : MODELING STUDY , 2002 .

[25]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

[26]  Hansel,et al.  Clustering in globally coupled phase oscillators. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[27]  K. Okuda.  Variety and generality of clustering in globally coupled oscillators , 1993 .

[28]  P. Somogyi,et al.  Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons , 1995, Nature.

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

[30]  T. Sejnowski,et al.  Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. , 2000, Journal of neurophysiology.

[31]  A. Agmon,et al.  Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex , 2001, The Journal of Neuroscience.

[32]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[33]  Hansel,et al.  Clustering and slow switching in globally coupled phase oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[35]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[36]  L. Wang,et al.  Electrophysiological and pharmacological characterization of a mammalian Shaw channel expressed in NIH 3T3 fibroblasts. , 1995, Journal of neurophysiology.

[37]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[38]  Carson C. Chow,et al.  Synchronization and Oscillatory Dynamics in Heterogeneous, Mutually Inhibited Neurons , 1998, Journal of Computational Neuroscience.

[39]  John Rinzel,et al.  Dynamics of Spiking Neurons Connected by Both Inhibitory and Electrical Coupling , 2003, Journal of Computational Neuroscience.

[40]  Idan Segev,et al.  Methods in neuronal modeling: From synapses to networks , 1989 .

[41]  Y. Kang,et al.  Electrophysiological and morphological characteristics of layer VI pyramidal cells in the cat motor cortex. , 1994, Journal of neurophysiology.

[42]  Haruko Matsui,et al.  Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behaviour , 1998, Nature.

[43]  Tomoki Fukai,et al.  Gamma Rhythmic Bursts: Coherence Control in Networks of Cortical Pyramidal Neurons , 2003, Neural Computation.

[44]  S. Sherman,et al.  Thalamic relay functions. , 2001, Progress in brain research.

[45]  Sherman Sm,et al.  Thalamic relay functions. , 2001 .

[46]  Tomoki Fukai,et al.  Influences of synaptic location on the synchronization of rhythmic bursting neurons. , 2004 .

[47]  Y. Kuramoto,et al.  Slow switching in globally coupled oscillators: robustness and occurrence through delayed coupling. , 2000, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  W. Singer,et al.  Temporal Coding in the Brain , 1994, Research and Perspectives in Neurosciences.

[49]  S. Hestrin,et al.  Electrical synapses between Gaba-Releasing interneurons , 2001, Nature Reviews Neuroscience.

[50]  G. Ermentrout,et al.  Analysis of neural excitability and oscillations , 1989 .

[51]  Bard Ermentrout,et al.  Type I Membranes, Phase Resetting Curves, and Synchrony , 1996, Neural Computation.

[52]  J. White,et al.  Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[53]  C. Holmgren,et al.  Coincident Spiking Activity Induces Long-Term Changes in Inhibition of Neocortical Pyramidal Cells , 2001, The Journal of Neuroscience.