Population coding by electrosensory neurons.

Sensory stimuli typically activate many receptors at once and therefore should lead to increases in correlated activity among central neurons. Such correlated activity could be a critical feature in the encoding and decoding of information in central circuits. Here we characterize correlated activity in response to two biologically relevant classes of sensory stimuli in the primary electrosensory nuclei, the electrosensory lateral line lobe, of the weakly electric fish Apteronotus leptorhynchus. Our results show that these neurons can display significant correlations in their baseline activities that depend on the amount of receptive field overlap. A detailed analysis of spike trains revealed that correlated activity resulted predominantly from a tendency to fire synchronous or anti-synchronous bursts of spikes. We also explored how different stimulation protocols affected correlated activity: while prey-like stimuli increased correlated activity, conspecific-like stimuli decreased correlated activity. We also computed the correlations between the variabilities of each neuron to repeated presentations of the same stimulus (noise correlations) and found lower amounts of noise correlation for communication stimuli. Therefore the decrease in correlated activity seen with communication stimuli is caused at least in part by reduced noise correlations. This differential modulation in correlated activity occurred because of changes in burst firing at the individual neuron level. Our results show that different categories of behaviorally relevant input will differentially affect correlated activity. In particular, we show that the number of correlated bursts within a given time window could be used by postsynaptic neurons to distinguish between both stimulus categories.

[1]  Daeyeol Lee,et al.  Effects of noise correlations on information encoding and decoding. , 2006, Journal of neurophysiology.

[2]  Maurice J Chacron,et al.  Nonlinear information processing in a model sensory system. , 2006, Journal of neurophysiology.

[3]  Brent Doiron,et al.  Non-classical receptive field mediates switch in a sensory neuron's frequency tuning , 2003, Nature.

[4]  Joseph G. Hoffman,et al.  Physical Techniques in Biological Research , 1963 .

[5]  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.

[6]  Joseph Bastian,et al.  The physiology and morphology of two types of electrosensory neurons in the weakly electric fishApteronotus leptorhynchus , 1984, Journal of Comparative Physiology A.

[7]  Insight into the mechanisms of neuronal processing from electric fish , 2003, Current Opinion in Neurobiology.

[8]  K. Frank,et al.  CHAPTER 2 – MICROELECTRODES FOR RECORDING AND STIMULATION , 1964 .

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

[10]  Maurice J Chacron,et al.  Electroreceptor neuron dynamics shape information transmission , 2005, Nature Neuroscience.

[11]  S. Sherman Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[12]  Fabrizio Gabbiani,et al.  Burst firing in sensory systems , 2004, Nature Reviews Neuroscience.

[13]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[14]  M. A. MacIver,et al.  Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. , 1999, The Journal of experimental biology.

[15]  D. Mastronarde Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. , 1983, Journal of neurophysiology.

[16]  D. Johnston,et al.  Slow Recovery from Inactivation of Na+ Channels Underlies the Activity-Dependent Attenuation of Dendritic Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1997, The Journal of Neuroscience.

[17]  L. Maler,et al.  Plastic and Nonplastic Pyramidal Cells Perform Unique Roles in a Network Capable of Adaptive Redundancy Reduction , 2004, Neuron.

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

[19]  Brent Doiron,et al.  Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli , 2003, Nature.

[20]  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.

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

[22]  Leonard Maler,et al.  Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis , 1993 .

[23]  J. Bastian,et al.  Dendritic modulation of burst-like firing in sensory neurons. , 2001, Journal of neurophysiology.

[24]  Nathaniel B Sawtell,et al.  From sparks to spikes: information processing in the electrosensory systems of fish , 2005, Current Opinion in Neurobiology.

[25]  Brent Doiron,et al.  Parallel Processing of Sensory Input by Bursts and Isolated Spikes , 2004, The Journal of Neuroscience.

[26]  Gary J. Rose,et al.  Frequency-Dependent PSP Depression Contributes to Low-Pass Temporal Filtering in Eigenmannia , 1999, The Journal of Neuroscience.

[27]  J. Bastian,et al.  The role of amino acid neurotransmitters in the descending control of electroreception , 1993, Journal of Comparative Physiology A.

[28]  C. Koch,et al.  Encoding of visual information by LGN bursts. , 1999, Journal of neurophysiology.

[29]  A. B. Bonds,et al.  Stimulus-dependent modulation of spike burst length in cat striate cortical cells. , 1997, Journal of neurophysiology.

[30]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[31]  Jan J. Koenderink,et al.  Information in channel-coded systems: correlated receivers , 1992, Biological Cybernetics.

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

[33]  Daeyeol Lee,et al.  Coding and transmission of information by neural ensembles , 2004, Trends in Neurosciences.

[34]  G. Laurent,et al.  Distinct Mechanisms for Synchronization and Temporal Patterning of Odor-Encoding Neural Assemblies , 1996, Science.

[35]  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.

[36]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[37]  Leonard Maler,et al.  The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus , 2004, Anatomy and Embryology.

[38]  N. Lemon,et al.  Conditional spike backpropagation generates burst discharge in a sensory neuron. , 2000, Journal of neurophysiology.

[39]  André Longtin,et al.  To Burst or Not to Burst? , 2004, Journal of Computational Neuroscience.

[40]  Sheila Nirenberg,et al.  Decoding neuronal spike trains: How important are correlations? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[41]  N. Uchida,et al.  Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. , 1999, Journal of neurophysiology.

[42]  D. Contreras,et al.  Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. , 1998, Journal of neurophysiology.

[43]  Maurice J Chacron,et al.  Feedback and Feedforward Control of Frequency Tuning to Naturalistic Stimuli , 2005, The Journal of Neuroscience.

[44]  L Maler,et al.  The nucleus praeeminentialis: A Golgi study of a feedback center in the electrosensory system of gymnotid fish , 1983, The Journal of comparative neurology.

[45]  Christof Koch,et al.  Stimulus Encoding and Feature Extraction by Multiple Sensory Neurons , 2002, The Journal of Neuroscience.

[46]  Brent Doiron,et al.  A Dynamic Dendritic Refractory Period Regulates Burst Discharge in the Electrosensory Lobe of Weakly Electric Fish , 2003, The Journal of Neuroscience.

[47]  D. Baylor,et al.  Concerted Signaling by Retinal Ganglion Cells , 1995, Science.

[48]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[49]  S. Sherman,et al.  Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: A comparison with corticogeniculate terminals , 1997, The Journal of comparative neurology.

[50]  H. Sompolinsky,et al.  Population coding in neuronal systems with correlated noise. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[52]  J. Bastian Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  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.

[54]  S. Panzeri,et al.  An exact method to quantify the information transmitted by different mechanisms of correlational coding. , 2003, Network.

[55]  Erika E. Fanselow,et al.  Thalamic bursting in rats during different awake behavioral states , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  R W Guillery,et al.  The role of the thalamus in the flow of information to the cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[57]  A. Aertsen,et al.  On the significance of correlations among neuronal spike trains , 2004, Biological Cybernetics.

[58]  J. Bastian Electrolocation: II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells inApteronotus albifrons , 1981 .

[59]  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.

[60]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[61]  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.

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

[63]  TJ Gawne,et al.  How independent are the messages carried by adjacent inferior temporal cortical neurons? , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[65]  A Longtin,et al.  Model of gamma frequency burst discharge generated by conditional backpropagation. , 2001, Journal of neurophysiology.

[66]  J. Bastian,et al.  Plasticity of feedback inputs in the apteronotid electrosensory system. , 1999, The Journal of experimental biology.

[67]  E. Fortune,et al.  Short-term synaptic plasticity as a temporal filter , 2001, Trends in Neurosciences.

[68]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[69]  E Ahissar,et al.  Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Abeles Quantification, smoothing, and confidence limits for single-units' histograms , 1982, Journal of Neuroscience Methods.

[71]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[72]  J Bastian Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter. , 1996, Journal of neurophysiology.

[73]  Michael J. Berry,et al.  Redundancy in the Population Code of the Retina , 2005, Neuron.

[74]  W Hamish Mehaffey,et al.  High-Threshold K+ Current Increases Gain by Offsetting a Frequency-Dependent Increase in Low-Threshold K+ Current , 2005, The Journal of Neuroscience.

[75]  Haim Sompolinsky,et al.  Nonlinear Population Codes , 2004, Neural Computation.

[76]  Maurice J Chacron,et al.  Receptive Field Organization Determines Pyramidal Cell Stimulus-Encoding Capability and Spatial Stimulus Selectivity , 2002, The Journal of Neuroscience.

[77]  L. Maler,et al.  Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). , 1998, Journal of neurophysiology.

[78]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[79]  Eric S Fortune,et al.  The decoding of electrosensory systems , 2006, Current Opinion in Neurobiology.

[80]  J Bastian,et al.  Plasticity in an electrosensory system. I. General features of a dynamic sensory filter. , 1996, Journal of neurophysiology.

[81]  Gary J Rose,et al.  Voltage-gated Na+ channels enhance the temporal filtering properties of electrosensory neurons in the torus. , 2003, Journal of neurophysiology.

[82]  J. Gallant,et al.  Natural Stimulation of the Nonclassical Receptive Field Increases Information Transmission Efficiency in V1 , 2002, The Journal of Neuroscience.

[83]  P. Latham,et al.  Synergy, Redundancy, and Independence in Population Codes, Revisited , 2005, The Journal of Neuroscience.

[84]  T. Shibasaki,et al.  Retinal ganglion cells act largely as independent encoders , 2001 .

[85]  J. Bastian Electrolocation: I. How the electroreceptors ofApteronotus albifrons code for moving objects and other electrical stimuli , 1981 .

[86]  Michael J. Berry,et al.  Synergy, Redundancy, and Independence in Population Codes , 2003, The Journal of Neuroscience.

[87]  J. Alves-Gomes,et al.  Systematic biology of gymnotiform and mormyriform electric fishes: phylogenetic relationships, molecular clocks and rates of evolution in the mitochondrial rRNA genes , 1999, The Journal of experimental biology.

[88]  K O Johnson,et al.  Sensory discrimination: decision process. , 1980, Journal of neurophysiology.