Electric Imaging through Evolution, a Modeling Study of Commonalities and Differences

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.

[1]  Gerhard von der Emde,et al.  Discrimination of objects through electrolocation in the weakly electric fish, Gnathonemus petersii , 1990, Journal of Comparative Physiology A.

[2]  Gerhard von der Emde,et al.  Functional foveae in an electrosensory system , 2008, The Journal of comparative neurology.

[3]  B Rasnow,et al.  Electric organ discharges and electric images during electrolocation. , 1999, The Journal of experimental biology.

[4]  Jacob Engelmann,et al.  From static electric images to electric flow: Towards dynamic perceptual cues in active electroreception , 2013, Journal of Physiology-Paris.

[5]  N. Hoshimiya,et al.  TheApteronotus EOD field: Waveform and EOD field simulation , 1980, Journal of comparative physiology.

[6]  Angel A Caputi,et al.  Electrolocation and electrocommunication in pulse gymnotids: signal carriers, pre-receptor mechanisms and the electrosensory mosaic , 2002, Journal of Physiology-Paris.

[7]  A. Caputi,et al.  Electroreception in Gymnotus carapo: pre-receptor processing and the distribution of electroreceptor types. , 2000, The Journal of experimental biology.

[8]  Adriana Migliaro,et al.  Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium , 2011, PloS one.

[9]  A. Caputi,et al.  A field potential analysis of the electromotor system in Gymnotus carapo , 1996, Journal of Comparative Physiology A.

[10]  A. Caputi,et al.  Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo , 1998, The Journal of comparative neurology.

[11]  J. Harlan Meyer,et al.  Behavioral responses of weakly electric fish to complex impedances , 1982, Journal of comparative physiology.

[12]  A. Caputi,et al.  Waveform generation in the weakly electric fish Gymnotus coropinae (Hoedeman): the electric organ and the electric organ discharge , 2009, Journal of Experimental Biology.

[13]  A. Caputi,et al.  The electric image in weakly electric fish: perception of objects of complex impedance. , 2000, The Journal of experimental biology.

[14]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers. , 1990, Journal of neurophysiology.

[15]  Diego Rother,et al.  Electric images of two low resistance objects in weakly electric fish. , 2003, Bio Systems.

[16]  Joseph Bastian,et al.  Frequency response characteristics of electroreceptors in weakly electric fish (Gymnotoidei) with a pulse discharge , 1976, Journal of comparative physiology.

[17]  Brian Rasnow,et al.  Imaging with electricity: how weakly electric fish might perceive objects , 1997 .

[18]  J. Albert,et al.  Phylogeny, biogeography, and electric signal evolution of Neotropical knifefishes of the genus Gymnotus (Osteichthyes: Gymnotidae). , 2010, Molecular phylogenetics and evolution.

[19]  Peter Moller,et al.  Locomotor and electric displays associated with electrolocation during exploratory behavior in mormyrid fish , 1984, Behavioural Brain Research.

[20]  Pedro A Aguilera,et al.  Electroreception in G. carapo: detection of changes in waveform of the electrosensory signals , 2003, Journal of Experimental Biology.

[21]  O. Macadar,et al.  Spatial distribution of the medullary command signal within the electric organ of Gymnotus carapo , 1993, Journal of Comparative Physiology A.

[22]  Angel A. Caputi,et al.  On the haptic nature of the active electric sense of fish , 2013, Brain Research.

[23]  B. Rasnow,et al.  The effects of simple objects on the electric field of Apteronotus , 1996, Journal of Comparative Physiology A.

[24]  A. Caputi,et al.  Waveform generation in Rhamphichthys rostratus (L.) (Teleostei, Gymnotiformes) , 1994, Journal of Comparative Physiology A.

[25]  Gerhard von der Emde,et al.  Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation , 2008, Journal of Experimental Biology.

[26]  D. D. Yager,et al.  Directional characteristics of tuberous electroreceptors in the weakly electric fish, Hypopomus (Gymnotiformes) , 1993, Journal of Comparative Physiology A.

[27]  Henning Scheich,et al.  The Detection of Electric Fields from Electric Organs , 1974 .

[28]  G. von der Emde,et al.  Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii). , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Caputi The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio-temporal electromotor pattern , 1999, The Journal of experimental biology.

[30]  C. Bell,et al.  The electric image in weakly electric fish: physical images of resistive objects in Gnathonemus petersii. , 1998, The Journal of experimental biology.

[31]  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.

[32]  A. Caputi,et al.  Electric organ discharge diversity in the genus Gymnotus: anatomo-functional groups and electrogenic mechanisms , 2013, Journal of Experimental Biology.

[33]  Omar Macadar,et al.  Environmental, seasonal, and social modulations of basal activity in a weakly electric fish , 2007, Physiology & Behavior.

[34]  Eric I. Knudsen,et al.  Spatial aspects of the electric fields generated by weakly electric fish , 1975, Journal of comparative physiology.

[35]  G. Emde,et al.  Imaging of Objects through active electrolocation in Gnathonemus petersii , 2002, Journal of Physiology-Paris.

[36]  P. Moller,et al.  Spatial aspects of electrolocation in the mormyrid fish, Gnathonemus petersii. , 1979, Journal de physiologie.

[37]  A. Caputi,et al.  Waveform generation of the electric organ discharge inGymnotus carapo , 2004, Journal of Comparative Physiology A.

[38]  Angel Ariel Caputi,et al.  Imaging in electrosensory systems , 2010, Interdisciplinary Sciences: Computational Life Sciences.

[39]  Ruben Budelli,et al.  Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system , 2004, Journal of Experimental Biology.

[40]  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.

[41]  A. Caputi,et al.  Electroreception in Gymnotus carapo: differences between self-generated and conspecific-generated signal carriers. , 2001, The Journal of experimental biology.

[42]  P. Hunter,et al.  FEM/BEM NOTES , 2001 .

[43]  M. Toerring,et al.  Motor programmes and electroreception in mormyrid fish , 1979, Behavioral Ecology and Sociobiology.

[44]  Angel A. Caputi,et al.  The electric image in weakly electric fish: I. A data-based model of waveform generation inGymnotus carapo , 1995, Journal of Computational Neuroscience.

[45]  Gerhard von der Emde,et al.  Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I : Discrimination performance , 2010 .

[46]  A. Caputi,et al.  Active Electric Imaging: Body-Object Interplay and Object's “Electric Texture” , 2011, PloS one.

[47]  M. A. MacIver,et al.  Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. , 2001, The Journal of experimental biology.

[48]  R. Budelli,et al.  Peripheral electrosensory imaging by weakly electric fish , 2006, Journal of Comparative Physiology A.

[49]  Roland Pusch,et al.  Electric imaging through active electrolocation: implication for the analysis of complex scenes , 2008, Biological Cybernetics.

[50]  O. Macadar,et al.  Waveform generation of the electric organ discharge inGymnotus carapo , 2004, Journal of Comparative Physiology A.

[51]  K. E. Machin,et al.  The Mechanism of Object Location in Gymnarchus Niloticus and Similar Fish , 1958 .

[52]  Angel A Caputi,et al.  The active electrosensory range of Gymnotus omarorum , 2012, Journal of Experimental Biology.

[53]  H. W. Lissmann On the Function and Evolution of Electric Organs in Fish , 1958 .

[54]  O. Macadar,et al.  Spinal mechanisms of electric organ discharge synchronization in Gymnotus carapo , 1990, Journal of Comparative Physiology A.

[55]  Joseph Bastian,et al.  Frequency response characteristics of electroreceptors in the weakly electric fish,Gymnotus carapo , 1979, Journal of comparative physiology.

[56]  Christopher Assad,et al.  Electric field maps and boundary element simulations of electrolocation in weakly electric fish , 1997 .

[57]  A. Caputi,et al.  The Electric Organ Discharge of Brachyhypopomus pinnicaudatus , 1998, Brain, Behavior and Evolution.

[58]  P. Stoddard,et al.  Predation enhances complexity in the evolution of electric fish signals , 1999, Nature.

[59]  Ruben Budelli,et al.  Electric fish measure distance in the dark , 1998, Nature.

[60]  K. Grant,et al.  The electric image in Gnathonemus petersii , 2002, Journal of Physiology-Paris.

[61]  A. Caputi,et al.  Proximate and ultimate causes of signal diversity in the electric fish Gymnotus , 2013, Journal of Experimental Biology.

[62]  M. Bacher,et al.  A new method for the simulation of electric fields, generated by electric fish, and their distorsions by objects , 1983, Biological Cybernetics.

[63]  Angel A. Caputi,et al.  Species-Specific Diversity of a Fixed Motor Pattern: The Electric Organ Discharge of Gymnotus , 2008, PLoS ONE.

[64]  André Longtin,et al.  Spatial Acuity and Prey Detection in Weakly Electric Fish , 2007, PLoS Comput. Biol..

[65]  James M. Bower,et al.  Imaging with Electricity , 1997 .

[66]  B. Ronacher,et al.  Perception of electric properties of objects in electrolocating weakly electric fish: two-dimensional similarity scaling reveals a City-Block metric , 1994, Journal of Comparative Physiology A.

[67]  Gerhard von der Emde,et al.  Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. II: Electric signalling behaviour , 2010 .

[68]  P. Moller,et al.  Lesions in the nucleus mesencephali exterolateralis: Effects on electrocommunication in the mormyrid fishGnathonemus petersii (Mormyriformes) , 1981, Journal of comparative physiology.

[69]  A. Caputi,et al.  Encoding electric signals by Gymnotus omarorum: Heuristic modeling of tuberous electroreceptor organs , 2012, Brain Research.

[70]  T H Bullock,et al.  Further analysis of sensory coding in electroreceptors of electric fish. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[71]  A. Caputi,et al.  Electric organ activation in Gymnotus carapo: Spinal origin and peripheral mechanisms , 1993, Journal of Comparative Physiology A.

[72]  Adriana Migliaro,et al.  Theoretical Analysis of Pre-Receptor Image Conditioning in Weakly Electric Fish , 2005, PLoS Comput. Biol..

[73]  P. Moller Electric fishes : history and behavior , 1995 .

[74]  G. von der Emde,et al.  Responses of cells in the mormyrid electrosensory lobe to EODs with distorted waveforms: implications for capacitance detection , 1994, Journal of Comparative Physiology A.