How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate

Information from the senses must be compressed into the limited range of responses that spiking neurons can generate. For optimal compression, the neuron's response should match the statistics of stimuli encountered in nature. Given a maximum firing rate, a nerve cell should learn to use each available firing rate equally often. Given a set mean firing rate, it should self-organize to respond with high firing rates only to comparatively rare events. Here we derive an unsupervised learning rule that continuously adapts membrane conductances of a Hodgkin-Huxley model neuron to optimize the representation of sensory information in the firing rate. Maximizing information transfer between the stimulus and the cell's firing rate can be interpreted as a non-Hebbian developmental mechanism.

[1]  D. Kernell,et al.  Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents , 1963, The Journal of physiology.

[2]  Amiel Feinstein,et al.  Information and information stability of random variables and processes , 1964 .

[3]  F. Reif,et al.  Fundamentals of Statistical and Thermal Physics , 1965 .

[4]  R. Stein,et al.  The information capacity of nerve cells using a frequency code. , 1967, Biophysical journal.

[5]  Kumpati S. Narendra,et al.  Adaptation and learning in automatic systems , 1974 .

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

[7]  S. Laughlin A Simple Coding Procedure Enhances a Neuron's Information Capacity , 1981, Zeitschrift fur Naturforschung. Section C, Biosciences.

[8]  M. Lings,et al.  Articles , 1967, Soil Science Society of America Journal.

[9]  William Bialek,et al.  Reading a Neural Code , 1991, NIPS.

[10]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  R. Baddeley,et al.  A statistical analysis of natural images matches psychophysically derived orientation tuning curves , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Anthony J. Bell,et al.  Self-organization in Real Neurons: Anti-Hebb in 'Channel Space'? , 1991, NIPS.

[13]  Ralph Linsker,et al.  Local Synaptic Learning Rules Suffice to Maximize Mutual Information in a Linear Network , 1992, Neural Computation.

[14]  C. Gray,et al.  Visually evoked oscillations of membrane potential in cells of cat visual cortex. , 1992, Science.

[15]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[16]  M. Tovée,et al.  Information encoding and the responses of single neurons in the primate temporal visual cortex. , 1993, Journal of neurophysiology.

[17]  E. Marder,et al.  Activity-dependent regulation of conductances in model neurons. , 1993, Science.

[18]  D. Ruderman The statistics of natural images , 1994 .

[19]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[20]  Dale Purves,et al.  Neural Activity And The Growth Of The Brain , 1994 .

[21]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[22]  J. Rushen Neural activity and the growth of the brain , 1995 .

[23]  N. Spitzer,et al.  Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients , 1995, Nature.

[24]  E. Marder,et al.  Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Lucien T. Thompson,et al.  Trace Eyeblink Conditioning Increases CA1 Excitability in a Transient and Learning-Specific Manner , 1996, The Journal of Neuroscience.

[26]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[27]  Christof Koch,et al.  Coding of Time-Varying Signals in Spike Trains of Integrate-and-Fire Neurons with Random Threshold , 1999, Neural Computation.

[28]  L. Abbott,et al.  Responses of neurons in primary and inferior temporal visual cortices to natural scenes , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  Michael J. Berry,et al.  Adaptation of retinal processing to image contrast and spatial scale , 1997, Nature.

[30]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

[31]  R. Douglas,et al.  An intracellular study of the contrast-dependence of neuronal activity in cat visual cortex. , 1997, Cerebral cortex.

[32]  K. Deisseroth,et al.  Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons , 1998, Nature.

[33]  Rob R. de Ruyter van Steveninck,et al.  The metabolic cost of neural information , 1998, Nature Neuroscience.

[34]  D. Alkon,et al.  Intracellular Correlates of Acquisition and Long-Term Memory of Classical Conditioning in Purkinje Cell Dendrites in Slices of Rabbit Cerebellar Lobule HVI , 1998, The Journal of Neuroscience.

[35]  C. Goodman,et al.  Synapse-specific control of synaptic efficacy at the terminals of a single neuron , 1998, Nature.

[36]  R. G. Morris D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949 , 1999, Brain Research Bulletin.

[37]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[38]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .