Weakly electric fish distinguish between envelope stimuli arising from different behavioral contexts

ABSTRACT Understanding how sensory information is processed by the brain in order to give rise to behavior remains poorly understood in general. Here, we investigated the behavioral responses of the weakly electric fish Apteronotus albifrons to stimuli arising from different contexts, by measuring changes in the electric organ discharge (EOD) frequency. Specifically, we focused on envelopes, which can arise either because of movement (i.e. motion envelopes) or because of interactions between the electric fields of three of more fish (i.e. social envelopes). Overall, we found that the animal's EOD frequency effectively tracked the detailed time course of both motion and social envelopes. In general, behavioral sensitivity (i.e. gain) decreased while phase lag increased with increasing envelope and carrier frequency. However, changes in gain and phase lag as a function of changes in carrier frequency were more prominent for motion than for social envelopes in general. Importantly, we compared behavioral responses to motion and social envelopes with similar characteristics. Although behavioral sensitivities were similar, we observed an increased response lag for social envelopes, primarily for low carrier frequencies. Thus, our results imply that the organism can, based on behavioral responses, distinguish envelope stimuli resulting from movement from those that instead result from social interactions. We discuss the implications of our results for neural coding of envelopes and propose that behavioral responses to motion and social envelopes are mediated by different neural circuits in the brain. Summary: Weakly electric fish can experience stimuli arising from different behavioral contexts; we provide the first evidence that they can distinguish envelopes arising from movement from those that occur during social interactions.

[1]  Noah J. Cowan,et al.  Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals , 2012, Journal of Experimental Biology.

[2]  Zachary M. Smith,et al.  Chimaeric sounds reveal dichotomies in auditory perception , 2002, Nature.

[3]  Gérard Faucon,et al.  Temporal envelope processing in the human auditory cortex: Response and interconnections of auditory cortical areas , 2008, Hearing Research.

[4]  Chengjie G Huang,et al.  SK channel subtypes enable parallel optimized coding of behaviorally relevant stimulus attributes: A review , 2017, Channels.

[5]  Fan-Gang Zeng,et al.  Speech recognition with amplitude and frequency modulations. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Gelfand,et al.  Comprar Hearing: An Introduction to Psychological and Physiological Acoustics, Fifth Edition | Stanley Gelfand | 9781420088663 | Informa Healthcare , 2009 .

[7]  A. Derrington,et al.  Temporal resolution of dichoptic and second-order motion mechanisms , 1998, Vision Research.

[8]  Keith Langley,et al.  Stereopsis from contrast envelopes , 1999, Vision Research.

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

[10]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Christopher K. Kovach,et al.  Temporal Envelope of Time-Compressed Speech Represented in the Human Auditory Cortex , 2009, The Journal of Neuroscience.

[12]  Mariana M. Marquez,et al.  Serotonin Selectively Increases Detectability of Motion Stimuli in the Electrosensory System , 2018, eNeuro.

[13]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[14]  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.

[15]  Gary J. Rose,et al.  Insights into neural mechanisms and evolution of behaviour from electric fish , 2004, Nature Reviews Neuroscience.

[16]  Robert A. Frazor,et al.  Independence of luminance and contrast in natural scenes and in the early visual system , 2005, Nature Neuroscience.

[17]  C. Schreiner,et al.  Spectral envelope coding in cat primary auditory cortex: linear and non‐linear effects of stimulus characteristics , 1998, The European journal of neuroscience.

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

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

[20]  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.

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

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

[23]  D Kleinfeld,et al.  Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. , 1997, Journal of neurophysiology.

[24]  André Longtin,et al.  The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope , 2006, Proceedings of the National Academy of Sciences.

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

[26]  Leonard Maler,et al.  Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size , 2009, The Journal of comparative neurology.

[27]  Hiroki Tanaka,et al.  Neural Basis for Stereopsis from Second-Order Contrast Cues , 2006, The Journal of Neuroscience.

[28]  Ari Rosenberg,et al.  The Y Cell Visual Pathway Implements a Demodulating Nonlinearity , 2011, Neuron.

[29]  Stanley A. Gelfand,et al.  Hearing: An Introduction to Psychological and Physiological Acoustics, Fourth Edition , 1998 .

[30]  S. Prescott,et al.  Integration Time in a Subset of Spinal Lamina I Neurons Is Lengthened by Sodium and Calcium Currents Acting Synergistically to Prolong Subthreshold Depolarization , 2005, The Journal of Neuroscience.

[31]  Leonard Maler,et al.  Receptive field organization across multiple electrosensory maps. II. Computational analysis of the effects of receptive field size on prey localization , 2009, The Journal of comparative neurology.

[32]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[33]  Masashi Kawasaki,et al.  Physiology of Tuberous Electrosensory Systems , 2005 .

[34]  Julie E. Elie,et al.  Neural processing of natural sounds , 2014, Nature Reviews Neuroscience.

[35]  Michael J. Hawken,et al.  Macaque VI neurons can signal ‘illusory’ contours , 1993, Nature.

[36]  D. Oertel The role of timing in the brain stem auditory nuclei of vertebrates. , 1999, Annual review of physiology.

[37]  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.

[38]  Michael S. Lewicki,et al.  Efficient coding of natural sounds , 2002, Nature Neuroscience.

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

[40]  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.

[41]  W. Metzner,et al.  Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. , 1999, The Journal of experimental biology.

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

[44]  Z. Fuzessery,et al.  Neuronal sensitivity to interaural time differences in the sound envelope in the auditory cortex of the pallid bat , 2000, Hearing Research.

[45]  A Moiseff,et al.  Time and intensity cues are processed independently in the auditory system of the owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[48]  Leonard Maler,et al.  Central Neuroanatomy of Electrosensory Systems in Fish , 2005 .

[49]  D. Robinson,et al.  Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. , 1987, Journal of neurophysiology.

[50]  Michael G Metzen,et al.  Electrosensory processing in Apteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species. , 2016, Journal of neurophysiology.

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

[52]  Peter Heil,et al.  Coding of temporal onset envelope in the auditory system , 2003, Speech Commun..

[53]  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.

[54]  Rüdiger Krahe,et al.  Species differences in group size and electrosensory interference in weakly electric fishes: Implications for electrosensory processing , 2010, Behavioural Brain Research.

[55]  C. Baker,et al.  Temporal and spatial response to second-order stimuli in cat area 18. , 1998, Journal of neurophysiology.

[56]  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.

[57]  Chengjie G Huang,et al.  Optimized Parallel Coding of Second-Order Stimulus Features by Heterogeneous Neural Populations , 2016, The Journal of Neuroscience.

[58]  A. Fairhall,et al.  Multiple Timescale Encoding of Slowly Varying Whisker Stimulus Envelope in Cortical and Thalamic Neurons In Vivo , 2010, The Journal of Neuroscience.

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

[60]  L. Maler,et al.  An atlas of the brain of the electric fish Apteronotus leptorhynchus , 1991, Journal of Chemical Neuroanatomy.

[61]  C. Baker Central neural mechanisms for detecting second-order motion , 1999, Current Opinion in Neurobiology.

[62]  Michael G Metzen,et al.  Stimulus background influences phase invariant coding by correlated neural activity , 2017, eLife.

[63]  Refractor Vision , 2000, The Lancet.