Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation

SUMMARY Weakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions – the Schnauzenorgan and the nasal region – can be termed electric fovea but they serve separate functions during active electrolocation.

[1]  Tim Malmström,et al.  Pupil shapes and lens optics in the eyes of terrestrial vertebrates , 2006, Journal of Experimental Biology.

[2]  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.

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

[4]  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.

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

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

[8]  Sheryl Coombs,et al.  Information-processing demands in electrosensory and mechanosensory lateral line systems , 2002, Journal of Physiology-Paris.

[9]  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.

[10]  W. Harder,et al.  Zur Empfindlichkeit des schwachelektrischen Fisches Gnathonemus petersii (Gthr. 1862) (Mormyriformes, Teleostei) gegenüber elektrischen Feldern , 2004, Zeitschrift für vergleichende Physiologie.

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

[12]  J. E. Lewis,et al.  Neuronal Population Codes and the Perception of Object Distance in Weakly Electric Fish , 2001, The Journal of Neuroscience.

[13]  Gerhard von der Emde,et al.  Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii , 2001, Journal of Comparative Physiology A.

[14]  H. Wagner Bipolar cells in the “grouped retina” of the elephantnose fish (Gnathonemus petersii) , 2007, Visual Neuroscience.

[15]  Wilhelm Harder,et al.  Die Beziehungen zwischen Elektrorezeptoren, Elektrischem Organ, Seitenlinienorganen und Nervensystem bei den Mormyridae (Teleostei, Pisces) , 1968, Zeitschrift für vergleichende Physiologie.

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

[17]  Angel A. Caputi,et al.  Physical basis of distance discrimination in weakly electric fish , 2000 .

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

[19]  Gerhard von der Emde,et al.  The “novelty response” in an electric fish response properties and habituation , 1999, Physiology & Behavior.

[20]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. II. Intra-axonal recordings show initial stages of central processing. , 1990, Journal of neurophysiology.

[21]  Jacob Engelmann,et al.  Sensory and motor effects of etomidate anesthesia. , 2006, Journal of neurophysiology.

[22]  B. Rasnow,et al.  The electric organ discharges of the gymnotiform fishes: I. Apteronotus leptorhynchus , 1996, Journal of Comparative Physiology A.

[23]  Angel A. Caputi,et al.  Contributions of electric fish to the understanding sensory processing by reafferent systems , 2004, Journal of Physiology-Paris.

[24]  J. Bastian,et al.  Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs , 2004, Journal of Comparative Physiology A.

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

[26]  K. Catania,et al.  Tactile Foveation in the Star-Nosed Mole , 2003, Brain, Behavior and Evolution.

[27]  A. Cowey,et al.  Preferential representation of the fovea in the primary visual cortex , 1993, Nature.

[28]  C. Bell,et al.  Behavioral evidence of a latency code for stimulus intensity in mormyrid electric fish , 1995, Journal of Comparative Physiology A.

[29]  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.

[30]  G. von der Emde,et al.  Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish. , 2006, Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology.

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

[32]  A. Caputi,et al.  Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G. carapo , 2003, Journal of Experimental Biology.

[33]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology , 1989, The Journal of comparative neurology.

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

[35]  C. Carr,et al.  Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish , 1982, The Journal of comparative neurology.

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

[37]  A. Cowey,et al.  The overrepresentation of the fovea and adjacent retina in the striate cortex and dorsal lateral geniculate nucleus of the macaque monkey , 1996, Neuroscience.

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

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

[40]  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.

[41]  Peter Moller,et al.  Spectral sensitivity of the weakly discharging electric fish Gnathonemus petersi using its electric organ discharges as the response measure , 1997 .