Encoding and processing of sensory information in neuronal spike trains

Recently, a statistical signal-processing technique has allowed the information carried by single spike trains of sensory neurons on time-varying stimuli to be characterized quantitatively in a variety of preparations. In weakly electric fish, its application to first-order sensory neurons encoding electric field amplitude (P-receptor afferents) showed that they convey accurate information on temporal modulations in a behaviorally relevant frequency range (<80 Hz). At the next stage of the electrosensory pathway (the electrosensory lateral line lobe, ELL), the information sampled by first-order neurons is used to extract upstrokes and downstrokes in the amplitude modulation waveform. By using signal-detection techniques, we determined that these temporal features are explicitly represented by short spike bursts of second-order neurons (ELL pyramidal cells). Our results suggest that the biophysical mechanism underlying this computation is of dendritic origin. We also investigated the accuracy with which upstrokes and downstrokes are encoded across two of the three somatotopic body maps of the ELL (centromedial and lateral). Pyramidal cells of the centromedial map, in particular I-cells, encode up- and downstrokes more reliably than those of the lateral map. This result correlates well with the significance of these temporal features for a particular behavior (the jamming avoidance response) as assessed by lesion experiments of the centromedial map.

[1]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[2]  H. V. Sorensen,et al.  An overview of sigma-delta converters , 1996, IEEE Signal Process. Mag..

[3]  Walter Heiligenberg,et al.  Neural Nets in Electric Fish , 1991 .

[4]  F Gabbiani,et al.  Feature Extraction by Burst-Like Spike Patterns in Multiple Sensory Maps , 1998, The Journal of Neuroscience.

[5]  R. Schreier,et al.  Delta-sigma data converters : theory, design, and simulation , 1997 .

[6]  M H Ellisman,et al.  TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  J. Juranek,et al.  A sensory brain map for each behavior? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  L. Maler,et al.  Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. , 1998, Journal of neurophysiology.

[9]  R. Fisher THE USE OF MULTIPLE MEASUREMENTS IN TAXONOMIC PROBLEMS , 1936 .

[10]  C A Shumway,et al.  Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

[12]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[13]  Christof Koch,et al.  Computation and the single neuron , 1997, Nature.

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

[15]  Norbert Wiener,et al.  Extrapolation, Interpolation, and Smoothing of Stationary Time Series , 1964 .

[16]  C A Shumway,et al.  Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  Fabrizio Gabbiani,et al.  Principles of spike train analysis , 1996 .

[18]  E. Fortune,et al.  Passive and Active Membrane Properties Contribute to the Temporal Filtering Properties of Midbrain Neurons In Vivo , 1997, The Journal of Neuroscience.

[19]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[20]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[21]  H. Vincent Poor,et al.  An introduction to signal detection and estimation (2nd ed.) , 1994 .

[22]  W Heiligenberg,et al.  Phase-sensitive midbrain neurons in Eigenmannia: neural correlates of the jamming avoidance response. , 1980, Science.

[23]  滋 篠本,et al.  Computation and the single neuron , 1998 .

[24]  L. Maler,et al.  Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering , 1999, The Journal of experimental biology.

[25]  Thomas Kailath,et al.  A general likelihood-ratio formula for random signals in Gaussian noise , 1969, IEEE Trans. Inf. Theory.

[26]  M. E. Nelson,et al.  Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish , 1997, Journal of Comparative Physiology A.

[27]  A. Borst,et al.  Active Membrane Properties and Signal Encoding in Graded Potential Neurons , 1998, The Journal of Neuroscience.

[28]  Turner,et al.  Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe , 1999, The Journal of experimental biology.

[29]  H. Vincent Poor,et al.  An Introduction to Signal Detection and Estimation , 1994, Springer Texts in Electrical Engineering.

[30]  Hiroshi Inose,et al.  A unity bit coding method by negative feedback , 1963 .

[31]  L. Maler,et al.  Oscillatory and burst discharge across electrosensory topographic maps. , 1996, Journal of neurophysiology.

[32]  Andrei N. Kolmogorov,et al.  On the Shannon theory of information transmission in the case of continuous signals , 1956, IRE Trans. Inf. Theory.

[33]  R. H. Hamstra,et al.  Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmannia. , 1973, Journal of neurophysiology.

[34]  C. Koch,et al.  From stimulus encoding to feature extraction in weakly electric fish , 1996, Nature.

[35]  C. Koch,et al.  Coding of time-varying electric field amplitude modulations in a wave-type electric fish. , 1996, Journal of neurophysiology.