Burst Firing in the Electrosensory System of Gymnotiform Weakly Electric Fish: Mechanisms and Functional Roles

Neurons across sensory systems and organisms often display complex patterns of action potentials in response to sensory input. One example of such a pattern is the tendency of neurons to fire packets of action potentials (i.e., a burst) followed by quiescence. While it is well known that multiple mechanisms can generate bursts of action potentials at both the single-neuron and the network level, the functional role of burst firing in sensory processing is not so well understood to date. Here we provide a comprehensive review of the known mechanisms and functions of burst firing in processing of electrosensory stimuli in gymnotiform weakly electric fish. We also present new evidence from existing data showing that bursts and isolated spikes provide distinct information about stimulus variance. It is likely that these functional roles will be generally applicable to other systems and species.

[1]  Maurice J Chacron,et al.  Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. , 2007, Journal of neurophysiology.

[2]  Alexander Borst,et al.  Principles of visual motion detection , 1989, Trends in Neurosciences.

[3]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[4]  Hannes P. Saal,et al.  Multiplexing Stimulus Information through Rate and Temporal Codes in Primate Somatosensory Cortex , 2013, PLoS biology.

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

[6]  Zhubo D. Zhang,et al.  Adaptation to second order stimulus features by electrosensory neurons causes ambiguity , 2016, Scientific Reports.

[7]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

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

[9]  André Longtin,et al.  Linear versus nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds. , 2010, Journal of neurophysiology.

[10]  Brent Doiron,et al.  Ghostbursting: A Novel Neuronal Burst Mechanism , 2004, Journal of Computational Neuroscience.

[11]  D. Ferster,et al.  Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. , 1997, Journal of neurophysiology.

[12]  Andre Longtin,et al.  Kinetics of fast short-term depression are matched to spike train statistics to reduce noise. , 2010, Journal of neurophysiology.

[13]  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.

[14]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: II. Sensory Image Cancellation , 2000, Journal of Computational Neuroscience.

[15]  Maurice J. Chacron,et al.  Activation of Parallel Fiber Feedback by Spatially Diffuse Stimuli Reduces Signal and Noise Correlations via Independent Mechanisms in a Cerebellum-Like Structure , 2015, PLoS Comput. Biol..

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

[17]  S. Sherman,et al.  Dual response modes in lateral geniculate neurons: Mechanisms and functions , 1996, Visual Neuroscience.

[18]  Mandyam V. Srinivasan,et al.  Motion detection in insect orientation and navigation , 1999, Vision Research.

[19]  J. Lisman Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[20]  André Longtin,et al.  Noise shaping by interval correlations increases information transfer. , 2004, Physical review letters.

[21]  Maurice J. Chacron,et al.  Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish , 2013, Journal of Experimental Biology.

[22]  André Longtin,et al.  Simple models of bursting and non-bursting P-type electroreceptors , 2001, Neurocomputing.

[23]  D. Hubel,et al.  The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Prince,et al.  A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  W. Reichardt Movement perception in insects , 1969 .

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

[27]  B. Doiron,et al.  Interval coding. I. Burst interspike intervals as indicators of stimulus intensity. , 2007, Journal of neurophysiology.

[28]  Hannes P. Saal,et al.  Millisecond Precision Spike Timing Shapes Tactile Perception , 2012, The Journal of Neuroscience.

[29]  Asaf Keller,et al.  Robust Temporal Coding in the Trigeminal System , 2004, Science.

[30]  Werner Reichardt,et al.  Evaluation of optical motion information by movement detectors , 1987, Journal of Comparative Physiology A.

[31]  Maurice J. Chacron,et al.  Electrosensory Midbrain Neurons Display Feature Invariant Responses to Natural Communication Stimuli , 2015, PLoS Comput. Biol..

[32]  Y. Yaari,et al.  Extracellular Calcium Modulates Persistent Sodium Current-Dependent Burst-Firing in Hippocampal Pyramidal Neurons , 2001, The Journal of Neuroscience.

[33]  M. Chacron,et al.  Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System , 2007, Journal of Neuroscience.

[34]  Maurice J. Chacron,et al.  Parallel sparse and dense information coding streams in the electrosensory midbrain , 2015, Neuroscience Letters.

[35]  L. Maler,et al.  The posterior lateral line lobe of certain gymnotoid fish: Quantitative light microscopy , 1979, The Journal of comparative neurology.

[36]  Brent Doiron,et al.  Deterministic Multiplicative Gain Control with Active Dendrites , 2005, The Journal of Neuroscience.

[37]  M Konishi,et al.  A neural map of interaural intensity differences in the brain stem of the barn owl , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[39]  Eugene M. Izhikevich,et al.  Neural excitability, Spiking and bursting , 2000, Int. J. Bifurc. Chaos.

[40]  Leonard Maler,et al.  Frequency-Tuned Cerebellar Channels and Burst-Induced LTD Lead to the Cancellation of Redundant Sensory Inputs , 2011, The Journal of Neuroscience.

[41]  André Longtin,et al.  Efficient computation via sparse coding in electrosensory neural networks , 2011, Current Opinion in Neurobiology.

[42]  Rüdiger Krahe,et al.  Statistics of the Electrosensory Input in the Freely Swimming Weakly Electric Fish Apteronotus leptorhynchus , 2013, The Journal of Neuroscience.

[43]  L. Maler,et al.  Negative Interspike Interval Correlations Increase the Neuronal Capacity for Encoding Time-Dependent Stimuli , 2001, The Journal of Neuroscience.

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

[45]  L. Maler,et al.  Suprathreshold stochastic firing dynamics with memory in P-type electroreceptors. , 2000, Physical review letters.

[46]  André Longtin,et al.  Routing the Flow of Sensory Signals Using Plastic Responses to Bursts and Isolated Spikes: Experiment and Theory , 2011, The Journal of Neuroscience.

[47]  W Hamish Mehaffey,et al.  Afterpotential Excitability by Delaying a Somatic Depolarizing Current Inactivation Can Increase Cell + Dendritic Na , 2005 .

[48]  M. Chacron,et al.  Sub‐ and suprathreshold adaptation currents have opposite effects on frequency tuning , 2012, The Journal of physiology.

[49]  Joseph Bastian,et al.  Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe , 1986, Journal of Comparative Physiology A.

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

[51]  Leonard Maler,et al.  SK Channels Provide a Novel Mechanism for the Control of Frequency Tuning in Electrosensory Neurons , 2007, The Journal of Neuroscience.

[52]  L. Maler,et al.  Limits of linear rate coding of dynamic stimuli by electroreceptor afferents. , 2007, Journal of neurophysiology.

[53]  A Borst,et al.  Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Patrick McGillivray,et al.  Parallel coding of first and second order stimulus attributes , 2012, BMC Neuroscience.

[55]  Brent Doiron,et al.  Type I Burst Excitability , 2003, Journal of Computational Neuroscience.

[56]  Maurice J Chacron,et al.  Perception and coding of envelopes in weakly electric fishes , 2013, Journal of Experimental Biology.

[57]  Maurice J. Chacron,et al.  Coding stimulus amplitude by correlated neural activity , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  P. Schwindt,et al.  Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. , 1999, Journal of neurophysiology.

[59]  John E. Lewis,et al.  Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus , 2008, Journal of Experimental Biology.

[60]  W. Bair Spike timing in the mammalian visual system , 1999, Current Opinion in Neurobiology.

[61]  Maurice J Chacron,et al.  Subthreshold membrane conductances enhance directional selectivity in vertebrate sensory neurons. , 2010, Journal of neurophysiology.

[62]  Mohsen Jamali,et al.  Coding of envelopes by correlated but not single-neuron activity requires neural variability , 2015, Proceedings of the National Academy of Sciences.

[63]  Maurice J. Chacron,et al.  Bursts and Isolated Spikes Code for Opposite Movement Directions in Midbrain Electrosensory Neurons , 2012, PloS one.

[64]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[65]  Maurice J. Chacron,et al.  Nonrenewal spike train statistics: causes and functional consequences on neural coding , 2011, Experimental Brain Research.

[66]  J. Magee,et al.  Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. , 1999, Journal of neurophysiology.

[67]  André Longtin,et al.  The effects of spontaneous activity, background noise, and the stimulus ensemble on information transfer in neurons , 2003, Network.

[68]  Noah J. Cowan,et al.  Active sensing via movement shapes spatiotemporal patterns of sensory feedback , 2012, Journal of Experimental Biology.

[69]  André Longtin,et al.  Contrast coding in the electrosensory system: parallels with visual computation , 2015, Nature Reviews Neuroscience.

[70]  Maurice J. Chacron,et al.  In vivo conditions influence the coding of stimulus features by bursts of action potentials , 2011, Journal of Computational Neuroscience.

[71]  A. Borst,et al.  Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Hannes P. Saal,et al.  Rate and timing of cortical responses driven by separate sensory channels , 2015, eLife.

[73]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[74]  André Longtin,et al.  Modeling cancelation of periodic inputs with burst-STDP and feedback , 2013, Neural Networks.

[75]  C E Carr,et al.  A Golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: Functional and morphological diversity in the midbrain , 1985, The Journal of comparative neurology.

[76]  M. Chacron,et al.  Neural heterogeneities and stimulus properties affect burst coding in vivo , 2010, Neuroscience.

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

[78]  Leonard Maler,et al.  Intrinsic frequency tuning in ELL pyramidal cells varies across electrosensory maps. , 2008, Journal of neurophysiology.

[79]  Leonard Maler,et al.  Neural heterogeneity and efficient population codes for communication signals. , 2010, Journal of neurophysiology.

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

[81]  Kathleen E Cullen,et al.  The neural encoding of self-motion , 2011, Current Opinion in Neurobiology.

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

[83]  Brent Doiron,et al.  Interval coding. II. Dendrite-dependent mechanisms. , 2007, Journal of neurophysiology.

[84]  S. Sherman Dual response modes in lateral geniculate neurons: mechanisms and functions. , 1996, Visual neuroscience.

[85]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  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.

[87]  André Longtin,et al.  ISI CORRELATIONS AND INFORMATION TRANSFER , 2004 .

[88]  André Longtin,et al.  Cellular and circuit properties supporting different sensory coding strategies in electric fish and other systems , 2012, Current Opinion in Neurobiology.

[89]  Michael G Metzen,et al.  Serotonin selectively enhances perception and sensory neural responses to stimuli generated by same-sex conspecifics , 2013, Proceedings of the National Academy of Sciences.

[90]  Maurice J Chacron,et al.  Population coding by electrosensory neurons. , 2008, Journal of neurophysiology.

[91]  Maurice J Chacron,et al.  Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish. , 2011, Journal of neurophysiology.

[92]  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.

[93]  M. Diamond,et al.  Complementary Contributions of Spike Timing and Spike Rate to Perceptual Decisions in Rat S1 and S2 Cortex , 2015, Current Biology.

[94]  André Longtin,et al.  Dynamics of Deterministic and Stochastic Paired ExcitatoryInhibitory Delayed Feedback , 2003, Neural Computation.

[95]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[96]  M. Chacron,et al.  Neural heterogeneities influence envelope and temporal coding at the sensory periphery , 2011, Neuroscience.

[97]  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 .

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

[99]  Maurice J Chacron,et al.  Differences in the time course of short-term depression across receptive fields are correlated with directional selectivity in electrosensory neurons. , 2009, Journal of neurophysiology.

[100]  Maurice J Chacron,et al.  Sparse coding of natural communication signals in midbrain neurons , 2009, BMC Neuroscience.

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

[102]  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.

[103]  L. Maler,et al.  The cytology of the posterior lateral line lobe of high‐frequency weakly electric fish (gymnotidae): Dendritic differentiation and synaptic specificity in a simple cortex , 1981, The Journal of comparative neurology.

[104]  L. Maler,et al.  Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations , 2005, The Journal of Neuroscience.

[105]  Chengjie G Huang,et al.  Temporal decorrelation by SK channels enables efficient neural coding and perception of natural stimuli , 2016, Nature Communications.

[106]  Leonard Maler,et al.  Burst-Induced Anti-Hebbian Depression Acts through Short-Term Synaptic Dynamics to Cancel Redundant Sensory Signals , 2010, The Journal of Neuroscience.

[107]  Maurice J. Chacron,et al.  Ionic and neuromodulatory regulation of burst discharge controls frequency tuning , 2008, Journal of Physiology-Paris.

[108]  Leonard Maler,et al.  Transient signals trigger synchronous bursts in an identified population of neurons. , 2009, Journal of neurophysiology.

[109]  Maurice J Chacron,et al.  Coding movement direction by burst firing in electrosensory neurons. , 2011, Journal of neurophysiology.

[110]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[111]  M. Nelson,et al.  Logarithmic time course of sensory adaptation in electrosensory afferent nerve fibers in a weakly electric fish. , 1996, Journal of neurophysiology.

[112]  Maurice J Chacron,et al.  SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. , 2009, Journal of neurophysiology.

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

[114]  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.

[115]  R. Llinás,et al.  Electrophysiology of mammalian thalamic neurones in vitro , 1982, Nature.

[116]  C. Carr,et al.  A circuit for detection of interaural time differences in the nucleus laminaris of turtles , 2017, Journal of Experimental Biology.

[117]  Xiao-Jing Wang,et al.  Bursting Neurons Signal Input Slope , 2002, The Journal of Neuroscience.

[118]  Walter Heiligenberg,et al.  Labelling of electroreceptive afferents in a gymnotoid fish by intracellular injection of HRP: The mystery of multiple maps , 1982, Journal of comparative physiology.

[119]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

[120]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: I. Differential Hebbian Learning , 1999, Journal of Computational Neuroscience.

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

[122]  A. Borst,et al.  Common circuit design in fly and mammalian motion vision , 2015, Nature Neuroscience.

[123]  Maurice J Chacron,et al.  Inhibition of SK and M channel-mediated currents by 5-HT enables parallel processing by bursts and isolated spikes. , 2011, Journal of neurophysiology.

[124]  E. Adrian Afferent discharges to the cerebral cortex from peripheral sense organs , 1941, The Journal of physiology.

[125]  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.

[126]  Y. Yaari,et al.  Ionic basis of spike after‐depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. , 1996, The Journal of physiology.

[127]  Michael G Metzen,et al.  Neural Heterogeneities Determine Response Characteristics to Second-, but Not First-Order Stimulus Features , 2015, The Journal of Neuroscience.

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

[129]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

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

[131]  Chun-I Yeh,et al.  Temporal precision in the neural code and the timescales of natural vision , 2007, Nature.

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

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

[134]  Gerry Czerniawski,et al.  Feedback and Feedforward , 2011 .

[135]  André Longtin,et al.  Postsynaptic Receptive Field Size and Spike Threshold Determine Encoding of High-frequency Information via Sensitivity to Synchronous Presynaptic Activity , 2008 .

[136]  Leonard Maler,et al.  Preparing for the unpredictable: adaptive feedback enhances the response to unexpected communication signals. , 2012, Journal of neurophysiology.

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

[138]  J. Rinzel,et al.  Oscillatory and bursting properties of neurons , 1998 .

[139]  L. Maler,et al.  Neural maps in the electrosensory system of weakly electric fish , 2014, Current Opinion in Neurobiology.

[140]  Brent Doiron,et al.  The Spatial Structure of Stimuli Shapes the Timescale of Correlations in Population Spiking Activity , 2012, PLoS Comput. Biol..

[141]  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.

[142]  Michael G Metzen,et al.  Weakly electric fish display behavioral responses to envelopes naturally occurring during movement: implications for neural processing , 2014, Journal of Experimental Biology.

[143]  Gary Marsat,et al.  Bursting Neurons and Ultrasound Avoidance in Crickets , 2012, Front. Neurosci..

[144]  C E Carr,et al.  Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotiform fish: Morphological substrates for parallel processing in the electrosensory system , 1981, The Journal of comparative neurology.

[145]  S. Salzberg,et al.  Non-classical receptive field mediates switch in a sensory neuron ’ s frequency tuning , 2022 .

[146]  Brent Doiron,et al.  Persistent Na+ current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. , 2003, Journal of neurophysiology.

[147]  N. Lesica,et al.  Encoding of Natural Scene Movies by Tonic and Burst Spikes in the Lateral Geniculate Nucleus , 2004, The Journal of Neuroscience.

[148]  André Longtin,et al.  Coding Conspecific Identity and Motion in the Electric Sense , 2012, PLoS Comput. Biol..

[149]  Michael G Metzen,et al.  Neural correlations enable invariant coding and perception of natural stimuli in weakly electric fish , 2016, eLife.

[150]  Maurice J. Chacron,et al.  Experimental and theoretical demonstration of noise shaping by interspike interval correlations (Invited Paper) , 2005, SPIE International Symposium on Fluctuations and Noise.