Neural correlations enable invariant coding and perception of natural stimuli in weakly electric fish

Neural representations of behaviorally relevant stimulus features displaying invariance with respect to different contexts are essential for perception. However, the mechanisms mediating their emergence and subsequent refinement remain poorly understood in general. Here, we demonstrate that correlated neural activity allows for the emergence of an invariant representation of natural communication stimuli that is further refined across successive stages of processing in the weakly electric fish Apteronotus leptorhynchus. Importantly, different patterns of input resulting from the same natural communication stimulus occurring in different contexts all gave rise to similar behavioral responses. Our results thus reveal how a generic neural circuit performs an elegant computation that mediates the emergence and refinement of an invariant neural representation of natural stimuli that most likely constitutes a neural correlate of perception. DOI: http://dx.doi.org/10.7554/eLife.12993.001

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

[2]  J. Craig,et al.  Shape Invariant Coding of Motion Direction in Somatosensory Cortex , 2010, PLoS biology.

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

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

[5]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[6]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

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

[8]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[9]  J. Movshon The velocity tuning of single units in cat striate cortex. , 1975, The Journal of physiology.

[10]  Michael J. Berry,et al.  Selectivity for multiple stimulus features in retinal ganglion cells. , 2006, Journal of neurophysiology.

[11]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[12]  H. Zakon,et al.  EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips , 2002, Journal of Physiology-Paris.

[13]  Y. Cohen,et al.  The what, where and how of auditory-object perception , 2013, Nature Reviews Neuroscience.

[14]  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.

[15]  Leonard Maler,et al.  A Synchronization-Desynchronization Code for Natural Communication Signals , 2006, Neuron.

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

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

[18]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

[19]  Walter Heiligenberg,et al.  The neural basis of a sensory filter in the Jamming Avoidance Response: No grandmother cells in sight , 1981, Journal of comparative physiology.

[20]  J. Reynolds,et al.  Trade-off between curvature tuning and position invariance in visual area V4 , 2013, Proceedings of the National Academy of Sciences.

[21]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[22]  Tim Gollisch,et al.  Modeling convergent ON and OFF pathways in the early visual system , 2008, Biological Cybernetics.

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

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

[25]  J. DiCarlo,et al.  Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey , 1999, The Journal of Neuroscience.

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

[27]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[28]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[29]  Tomaso A. Poggio,et al.  A Canonical Neural Circuit for Cortical Nonlinear Operations , 2008, Neural Computation.

[30]  Charles S. Zuker,et al.  The Coding of Temperature in the Drosophila Brain , 2011, Cell.

[31]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

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

[33]  Stephen A. Baccus,et al.  Segregation of object and background motion in the retina , 2003, Nature.

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

[35]  Stephen E. Clarke,et al.  The neural dynamics of sensory focus , 2015, Nature communications.

[36]  J. Alonso,et al.  Complex Receptive Fields in Primary Visual Cortex , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[37]  M. Tachibana,et al.  Synchronized retinal oscillations encode essential information for escape behavior in frogs , 2005, Nature Neuroscience.

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

[39]  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.

[40]  Neil C. Rabinowitz,et al.  Constructing Noise-Invariant Representations of Sound in the Auditory Pathway , 2013, PLoS biology.

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

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

[43]  S. Berti The role of auditory transient and deviance processing in distraction of task performance: a combined behavioral and event-related brain potential study , 2013, Front. Hum. Neurosci..

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

[45]  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.

[46]  Jerry D. Nguyenkim,et al.  Arginine vasotocin modulates a sexually dimorphic communication behavior in the weakly electric fish Apteronotus leptorhynchus. , 2001, The Journal of experimental biology.

[47]  G. Rose,et al.  Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[49]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

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

[51]  Gustavo Deco,et al.  Stimulus-dependent variability and noise correlations in cortical MT neurons , 2013, Proceedings of the National Academy of Sciences.

[52]  Tomaso Poggio,et al.  Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex , 2007, The Journal of Neuroscience.

[53]  Henriette Walz,et al.  Encoding of communication signals in heterogeneous populations of electroreceptors , 2013 .

[54]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[55]  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.

[56]  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.

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

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

[59]  Nicole C. Rust,et al.  Selectivity and Tolerance (“Invariance”) Both Increase as Visual Information Propagates from Cortical Area V4 to IT , 2010, The Journal of Neuroscience.

[60]  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.

[61]  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.

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

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

[64]  Maurice J Chacron,et al.  Effects of restraint and immobilization on electrosensory behaviors of weakly electric fish. , 2009, ILAR journal.

[65]  James J. DiCarlo,et al.  How Does the Brain Solve Visual Object Recognition? , 2012, Neuron.

[66]  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.

[67]  D. Barbour Intensity-invariant coding in the auditory system , 2011, Neuroscience & Biobehavioral Reviews.

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

[69]  M. Wehr,et al.  Nonoverlapping Sets of Synapses Drive On Responses and Off Responses in Auditory Cortex , 2010, Neuron.

[70]  Brian S Nelson,et al.  Sex and species differences in neuromodulatory input to a premotor nucleus: a comparative study of substance P and communication behavior in weakly electric fish. , 2005, Journal of neurobiology.

[71]  Sreekanth H. Chalasani,et al.  Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans , 2007, Nature.

[72]  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.

[73]  B. Boycott,et al.  Morphology and topography of on- and off-alpha cells in the cat retina , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

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

[76]  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.

[77]  G. Zupanc,et al.  Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus , 2006, Journal of Comparative Physiology.

[78]  Bruno A Olshausen,et al.  Sparse coding of sensory inputs , 2004, Current Opinion in Neurobiology.

[79]  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.

[80]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[81]  Eric Shea-Brown,et al.  Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. , 2008, Physical review letters.

[82]  Lindsey J. Macpherson,et al.  Temperature representation in the Drosophila brain , 2015, Nature.

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

[84]  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..

[85]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

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

[87]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

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

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

[90]  R. Christopher deCharms,et al.  Primary cortical representation of sounds by the coordination of action-potential timing , 1996, Nature.

[91]  John E. Lewis,et al.  The effect of difference frequency on electrocommunication: Chirp production and encoding in a species of weakly electric fish, Apteronotus leptorhynchus , 2008, Journal of Physiology-Paris.

[92]  B. Boycott,et al.  Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[93]  Brett A. Johnson,et al.  Relational representation in the olfactory system , 2007, Proceedings of the National Academy of Sciences.

[94]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .