Enhanced neuronal response induced by fast inhibition.

We report a facilitatory role of inhibitory synaptic input that can enhance a neuron's firing rate, in contrast to the conventional belief that inhibition suppresses firing. We study this phenomenon using the Hodgkin-Huxley model of spike generation with random Poisson trains of subthreshold excitatory and inhibitory inputs. Enhancement occurs when, by chance, brief inhibition leads excitation with a favorable timing and counterintuitively induces a reduction of the spike threshold. The basic mechanism is also illustrated with the phase-plane analysis of a two variable model.

[1]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[2]  Christian Leibold,et al.  Stability analysis of asynchronous states in neuronal networks with conductance-based inhibition. , 2004, Physical review letters.

[3]  J Rinzel,et al.  A theoretical basis for large coefficient of variation and bimodality in neuronal interspike interval distributions. , 1983, Journal of theoretical biology.

[4]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[5]  Pierre Meyrand,et al.  A switch between two modes of synaptic transmission mediated by presynaptic inhibition , 1995, Nature.

[6]  S Coombes,et al.  Clustering through postinhibitory rebound in synaptically coupled neurons. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[7]  G. P. Moore,et al.  Pacemaker Neurons: Effects of Regularly Spaced Synaptic Input , 1964, Science.

[8]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[9]  Jianfeng Feng,et al.  Variability of Firing of Hodgkin-Huxley and FitzHugh-Nagumo Neurons with Stochastic Synaptic Input , 1999 .

[10]  H. L. Bryant,et al.  Spike initiation by transmembrane current: a white‐noise analysis. , 1976, The Journal of physiology.

[11]  Eugene M. Izhikevich,et al.  Resonate-and-fire neurons , 2001, Neural Networks.

[12]  B. Grothe,et al.  New roles for synaptic inhibition in sound localization , 2003, Nature Reviews 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]  D. Signorini,et al.  Neural networks , 1995, The Lancet.

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

[16]  N. Brunel,et al.  Firing frequency of leaky intergrate-and-fire neurons with synaptic current dynamics. , 1998, Journal of theoretical biology.

[17]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[18]  Jianfeng Feng,et al.  Increasing inhibitory input increases neuronal firing rate: why and when? Diffusion process cases , 2001 .

[19]  G B Ermentrout,et al.  Bistability in pulse propagation in networks of excitatory and inhibitory populations. , 2001, Physical review letters.

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

[21]  S. W. Kuffler,et al.  SYNAPTIC INHIBITION IN AN ISOLATED NERVE CELL , 1955, The Journal of general physiology.

[22]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[23]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[24]  W. K. Luk,et al.  Synchronization and sensitivity enhancement of the Hodgkin-Huxley neurons due to inhibitory inputs , 2000, Biological Cybernetics.

[25]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[26]  D. Hansel,et al.  Existence and stability of persistent states in large neuronal networks. , 2001, Physical review letters.

[27]  S Redner,et al.  Steady state of an inhibitory neural network. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  J. Huguenard,et al.  Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. , 1999, Science.

[29]  D James Surmeier,et al.  Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus , 2005, The Journal of Neuroscience.

[30]  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.

[31]  J. Rinzel,et al.  Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. , 2004, Journal of neurophysiology.

[32]  Zhenghan Wang,et al.  Postinhibitory rebound delay and weak synchronization in Hodgkin-Huxley neuronal networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.