Abstract
The electric sense of mormyrids is often regarded as an adaptation to conditions unfavourable for vision and in these fish it has become the dominant sense for active orientation and communication tasks. With this sense, fish can detect and distinguish the electrical properties of the close environment, measure distance, perceive the 3-D shape of objects and discriminate objects according to distance or size and shape, irrespective of conductivity, thus showing a degree of abstraction regarding the interpretation of sensory stimuli. The physical properties of images projected on the sensory surface by the fish’s own discharge reveal a “Mexican hat” opposing centre-surround profile. It is likely that computation of the image amplitude to slope ratio is used to measure distance, while peak width and slope give measures of shape and contrast. Modelling has been used to explore how the images of multiple objects superimpose in a complex manner. While electric images are by nature distributed, or ‘blurred” behavioural strategies orienting sensory surfaces and the neural architecture of sensory processing networks both contribute to resolving potential ambiguities. Rostral amplification is produced by current funnelling in the head and chin appendage regions, where high density electroreceptor distributions constitute foveal regions. Central magnification of electroreceptive pathways from these regions particularly favours the detection of capacitive properties intrinsic to potential living prey. Swimming movements alter the amplitude and contrast of pre-receptor object-images but image modulation is normalised by central gain-control mechanisms that maintain excitatory and inhibitory balance, removing the contrast-ambiguity introduced by self-motion in much the same way that contrast gain-control is achieved in vision.
Similar content being viewed by others
References
Adelman TL, Bialek W, Olberg RM (2003) The information content of receptive fields. Neuron 40: 823–33
Assad C (1997) Electric field maps and boundary element simulations of electrolocation in weakly electric fish. Electrical Engineering, California Institute of Technology, Pasadena
Azzopardi P, Cowey A (1993) Preferential representation of the fovea in the primary visual cortex. Nature 361: 719–21
Babineau D, Longtin A, Lewis JE (2006) Modelling the field of weakly electric fish. J Exp Biol 209: 3636–651
Babineau D, Lewis JE, Longtin A (2007) Spatial acuity and prey detection in weakly electric fish. PLoS Comput Biol 3: e38
Bacelo J (2007) Sensory processing in the Electrosensory Lobe of the weakly electric fish Gnathonemus petersii. THESE DE DOCTORAT DE L’UNIVERSITE PARIS 6, Pierre et Marie Curie. Paris 6, Paris, p 167
Bacelo J, Grant K (2001) Electrosensory and trigeminal innervation of the Schnauzenorgan in Gnathonemus petersii. In: 6th international congress of neuroethology, Bonn/Germany, p 225
Baldi P, Heiligenberg W (1988) How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers. Un Ensemble de courbes qui font monter une droite. Biol Cybern 59: 313–18
Bastian J (1975) Receptive fields of cerebellar cells receiving exteroceptive input in a ymnotid fish. J Neurophysiol 38: 285–00
Bastian J (1981a) Electrolocation: I. How the electroreceptors of Apteronotus albifrons code for moving objects and other electric stimuli. J Comp Physiol A 144: 465–79
Bastian J (1981b) Electrolocation: II. The effects of moving objects and other electric stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J Comp Physiol A 144: 481–94
Bastian J (1995) Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs. J Comp Physiol A 176: 63–3
Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22: 4577–590
Bell CC (1981) An efference copy which is modified by reafferent input. Science 214(4519): 450–53
Bell CC (1990) Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. II. Intra-axonal recordings show initial stages of central processing. J Neurophysiol 63: 303–18
Bell CC (2001) Memory-based expectations in electrosensory systems. Curr Opin Neurobiol 11: 481–87
Bell CC, Zakon H, Finger TE (1989) Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology. J Comp Neurol 286: 391–07
Bell CC, Bodznick D, Montgomery JC, Bastian J (1997a) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50: 17–1
Bell CC, Caputi A, Grant K (1997b) Physiology and plasticity of morphologically identified cells in the mormyrid electrosensory lobe. J Neurosci 17: 6409–423
Budelli R, Caputi AA (2000) The electric image in weakly electric fish: perception of objects of complex impedance. J Exp Biol 203(Pt 3): 481–92
Caputi AA (2004) Contributions of electric fish to the understanding of sensory processing by reafferent systems. J Physiol Paris 98: 81–7
Caputi AA, Budelli R (2006) Peripheral electrosensory imaging by weakly electric fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192(6): 587–00
Caputi AA, Budelli R, Grant K, Bell CC (1998) The electric image in weakly electric fish: physical images of resistive objects in Gnathonemus petersii. J Exp Biol 201(Pt 14): 2115–128
Catania KC (1999) A nose that looks like a hand and acts like an eye: the unusual mechanosensory system of the star-nosed mole. J Comp Physiol A 185: 367–72
Catania KC, Kaas JH (1997) Somatosensory fovea in the star-nosed mole: behavioral use of the star in relation to innervation patterns and cortical representation. J Comp Neurol 387: 215–33
Castelló ME, Caputi AA, Trujillo-Cenóz O (1998) Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo. J Comp Neurol 401: 549–63
Castelló ME, Aguilera PA, Trujillo-Cenoz O, Caputi AA (2000) Electroreception in Gymnotus carapo: Pre-receptional mechanisms and distribution of electroreceptor types. J Exp Biol 203: 3279–287
Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature 423: 77–1
Chen L, House JL, Krahe R, Nelson ME (2005) Modeling signal and background components of electrosensory scenes. J comp Physiol A 191: 331–45
Ciali S, Gordon J, Moller P (1997) Spectral sensitivity of the weakly discharging electric fish Gnathonemus petersii using its electric organ discharges as the response measure. J Fish Biology 50: 1074–087
Ćurčić B, van Netten SM (2006) Source location encoding in the fish lateral line canal. J Exp Biol 209: 1548–559
Douglas RH, Eva J, Guttridge N (1988) Size constancy in goldfish (Carassius auratus). Behav Brain Res 30: 37–2
Egelhaaf M, Boddeker N, Kern R, Kretzberg J, Lindemann JP, Warzecha AK (2003) Visually guided orientation in flies: case studies in computational neuroethology. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189: 401–09
Gomez L, Budelli R, Grant K, Caputi AA (2004) Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system. J Exp Biol 207: 2443–2453
Goulet J, Engelmann J, Chagnaud B, Franosch JM, Suttner MD, van Hemmen JL (2007) Object localization through the lateral line system of fish: theory and experiment. J Com Physiol A 194(1): 1–7
Harder W, Schief A, Uhlemann H (1967) Zur empfindlichkeit des schwachelektrischen Fisches Gnathonemus petersii (Mormyriformes; Teleostei) gegenüber elektrischen Feldern. Z Vergl Physiol 54: 89–08
Heiligenberg W (1973) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87: 137–64
Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish. In: Aneuroethologicalapproach. Braitenberg V(eds) Studies of brain function. Springer Verlag, Berlin, pp 1–5
Hollmann M, von der Emde G (2004) Two electrical foveae in the skin of the weakly electric fish, Gnathonemus persii (Teleostei). 97 Jahresversammlung der Deutschen Zoologischen Gesellschaft, Rostock, p P14
Hollmann M, von der Emde G (2007) Electrofoveal regions on the skin of a weakly electric fish. 8th Int Congress of Neuroethology, Vancouver, Canada
Jeffress LA (1948) A place theory of sound localization. J Comp Physiol Psychol 41: 35–9
Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A(eds) Handbook of sensory physiology. Springer, Berlin, pp 148–00
Karmeier K, van Hateren JH, Kern R, Egelhaaf M (2006) Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons. J Neurophysiol 96: 1602–614
Landsberger M, von der Emde G (2007) Relevance of a peculiar retina type for visual detection in the weakly electric elephantnose fish. In: Eigth international conference of neuroethology, Vancouver/Canada, p PO37
Leibowitz HW (1971) Sensory, learned, and cognitive mechanisms of size perception. Ann NY Acad Sci 188: 47–0
Lewis JE, Maler L (2001) Neuronal population codes and the perception of object distance in weakly electric fish. J Neurosci 21: 2842–850
Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35: 156–91
Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35: 451–86
McCreery DB (1977) Spatial organization of receptive fields of lateral lemniscus neurons of the lateral line lobe of the catfish Ictalurus nebulosus. J Comp Physiol A 113: 341–53
Migliaro A, Caputi AA, Budelli R (2005) Theoretical analysis of pre-receptor image conditioning in weakly electric fish. PLoS Comp Biol 1: 123–31
Mountcastle V, Darian-Smith I (1974) Neuronal mechanisms in somesthesia. CV Mosby Company, Mosby
Pereira ASF, Centurión V, Caputi AA (2005) Contextual effects of small environments on the electric images of objects and their brain evoked responses in weakly electric fish. J Exp Biol 208: 961–72
Petkov N, Subramanian E (2007) Motion detection, noise reduction, texture suppression, and contour enhancement by spatiotemporal Gabor filters with surround inhibition. Biol Cybern doi:10.1007/s00422-007-0182-0
Pusch R, von der Emde G, Hollmann M, Bacelo J, Nöbel S, Grant K, Engelmann J (2008) Active Sensing in a Mormyrid Fish — Electric Images and Peripheral Modifications of the Signal Carrier give Evidence of Dual Foveation. J Exp Biol 211: 921–34
Quinet P (1971) Etude systematique des organes sensoriels de la peau des Mormyriformes (Pisces, Mormyriformes). Ann Mus R Afr Cent Tervuren (Belg) Ser 8(190): 1–7
Rasnow B (1996) The effects of simple objects on the electric field of Apteronotus. J Com Physiol A 178: 397–11
Ratcliff F (1965) Mach bands: quantitative studies on neuronal structures in the retina. Holden Day, San Francisco
Rother D (2003) Simulación de Imágenes Eléctricas en Peces Eléctricos de Descarga Débil. Simulación de Imágenes Eléctricas en Peces Eléctricos de Descarga Débil. Universidad de la República, Montevideo, p 93
Rother D, Migliaro A, Canetti R, Gomez L, Caputi A, Budelli R (2003) Electric images of two low resistance objects in weakly electric fish. Biosystems 71: 169–77
Sachdev RN, Catania KC (2002) Receptive fields and response properties of neurons in the star-nosed mole’s somatosensory fovea. J Neurophysiol 87: 2602–611
Sawtell NB, Williams A, Roberts PD, von der Emde G, Bell CC (2006) Effects of sensing behavior on a latency code. J Neurosci 26: 8221–234
Schuster S, Amtsfeld S (2002) Template-matching describes visual pattern-recognition tasks in the weakly electric fish Gnathonemus petersii. J Exp Biol 205: 549–57
Schwarz S, von der Emde G (2001) Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii. J Comp Physiol A 186: 1185–197
Sherman SM (1979) Functional-significance of X and Y cells in normal and visually deprived cats. Trends Neurosci 2: 192–95
Sicardi EA, Caputi AA, Budelli R (2000) Physical basis of distance discrimination in weakly electric fish. Physica A 86–3
Szabo T, Hagiwara S (1967) A latency change mechanism involved in sensory coding of electric fish (mormyrids). Physiol Behav 2: 331–35
von der Emde G (2006) Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192(6): 601–12
von der Emde G, Ronacher B (1994) Perception of electric properties of objects in electrolocating weakly electric fish: two-dimensional similarity scaling reveals a City-Block metric. J Comp Physiol A 175: 801–12
von der Emde G, Fetz S (2007) Distance, shape and more: Recognition of object features during active electrolocation in a weakly electric fish. J Exp Biology 210: 3082–095
von der Emde G, Schwarz S, Gomez L, Budelli R, Grant K (1998) Electric fish measure distance in the dark. Nature 395: 890–94
Wagner HJ (2007) Bipolar Cells in the “Grouped Retina” of the Elephantnose Fish (Gnathonemus petersii). Vis Neurosci 24(3): 355–62
Author information
Authors and Affiliations
Corresponding author
Additional information
J. Engelmann and J. Bacelo contributed equally to this study.
Rights and permissions
About this article
Cite this article
Engelmann, J., Bacelo, J., Metzen, M. et al. Electric imaging through active electrolocation: implication for the analysis of complex scenes. Biol Cybern 98, 519–539 (2008). https://doi.org/10.1007/s00422-008-0213-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-008-0213-5