Abstract
Weakly electric fish react to resistance and capacitance of objects that locally amplify and distort their self-generated Electric Organ Discharge (EOD) received by their skin receptors. The successive-layer structure of tissues gives certain biological materials a kind of electrical anisotropy. A polarized object, for instance, will conduct current differently in one versus the other direction. This diode-like electric anisotropy should make a significant difference to a Mormyrid who emits a directional, biphasic EOD and whose receptors are sensitive to EOD amplitude and distortion changes. The ability of Gnathonemus petersii (Mormyridae) to discriminate polarity was investigated on a virtual object by manipulating changes in a circuit comprised of diodes combined in various ways. The “novelty response,” an increase in the discharge rate in response to perceived changes, was used to assess the fish’s sensitivity. Indeed, G. petersii detects polarized objects and discriminates between polarity directions. However, the diode-like anisotropy entails a voltage threshold. Because voltage decreases with distance, and the EOD comprises opposite phases of different amplitudes, the active spaces of detection and discrimination are different and depend on the object orientation. Electric polarity thus extends the “palette” of dielectric properties used by this fish to evaluate object quality, direction, and distance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- Apl:
-
A circuit with two diodes connected in anti-parallel, i.e., in parallel with one Rev and the other Dir
- Cnd:
-
A pure conductor achieved by a full connection (short circuit) between the two stimulating electrodes
- Dir:
-
A circuit with a diode connected in Direct direction between electrodes, allowing the P-phase current to pass through, and blocking the N-phase current
- EOD:
-
Electric organ discharge
- Ins:
-
A pure insulator, induced by opening the circuit between the two stimulating electrodes
- IPI or inter-pulse interval:
-
Time elapsed between successive discharges, in milliseconds
- N-phase:
-
Second phase along the time axis or the part of the discharge of head-negative polarity (current flowing tail to head around the fish)
- P-phase:
-
First phase along the time axis or the part of the discharge of head-positive polarity (current flowing head to tail)
- Rev:
-
A circuit with a diode connected in Reverse direction between electrodes, blocking the P-phase current and letting the N-phase current through
- RQ or response quotient:
-
An index of responsiveness per trial within a set of trials; post-trigger median IPI obtained in each trial over the pre-trigger, grand median for the set. Expressed in %, the RQ is theoretically equal to 100% in a control trial and decreases with sensitivity
- S− and S+:
-
Respectively, the negative- and positive-poles of the stimulating electrodes
- TTL or transistor-transistor logic:
-
A normalized 5-V electronic signal
References
Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185–1193
Bastian J (1986) Frequency response characteristics of electroreceptors in weakly-electric fish. J Neurophysiol 112:131–156
Bauer R (1974) Electric organ discharge activity of resting and stimulated Gnathonemus petersii (mormyridae). Behaviour 50:306–323
Behari J, Andrabi WH (1981) PN Junction characteristics and photoelectromagnetic effect in bone. Biomaterials 2:23–27
Bell CC (1990) Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers. J Neurophysiol 63:319–332
Bennett MVL, Grundfest H (1961) Studies on the morphology and electrophysiology of electric organs III. Electrophysiology of electric organs in Mormyrids. In: Chagas C, de Carvalho P (eds) Bioelectrogenesis. Elsevier, Amsterdam, pp 113–135
Caputi AA, Budelli R (1995) The electric image in weakly-electric fish. I. A data-based model of waveform generation in Gymnotus carapo. J Comput Neurosci 2:131–147
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 201:2115–2128
Dienfenderfer AJ (1979) Principles of electronic instrumentation. Saunders College Publishing, Philadelphia, pp 110–116
Ghosh D, Manna S, De S, Basu R, Das S, Nandy P (2004) Effect of asymmetric bathing solution on the non-linear I–V characteristics of lipid membranes. Physica A Stat Theor Phys 336:514–520
Graff C (1986) Signaux électriques et comportement social du poisson à faibles décharges Marcusenius macrolepidotus (mormyridae, teleostei). Ph.D. Thesis, University of Paris-Sud, France
Graff C, Kaminski G, Gresty M, Ohlmann T (2004) Fish perform spatial pattern recognition and abstraction by exclusive use of active electrolocation. Curr Biol 14:818–823
Harley HE, Putman EA, Roitblat HL (2003) Bottlenose dolphins perceive object features trough echolocation. Nature 424:667
Heiligenberg W (1977) Principles of electrolocation and jamming avoidance in electric fish. In: Braitenberg V (ed) Studies of brain function, vol 1. Springer, Berlin, pp 1–85
Hopkins CD (1972) Sex differences in electric signaling in an electric fish. Nature 175:1035–1037
Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486
Litel C (1997) Rythmes de décharge de poissons électriques (Mormyridae): aspects structuraux et fonctionnels. Ph.D. Thesis, François Rabelais University, Tours, France
Marszalek PE, Markin VS, Tanaka T, Kawaguchi H, Fernandez JM (1995) The secretory granule matrix-electrolyte interface: a homologue of the p-n rectifying junction. Biophys J 69:1218–1229
Meyer JH (1982) Behavioral responses of weakly electric fish to complex impedances. J Comp Physiol A 145:459–470
Moller P (1995) Electric fishes: history and behavior. Chapman and Hall, London
Nanavati C, Fernandez JM (1993) The secretory granule matrix: a fast-acting smart polymer. Science 259:963–965
Pack AA, Herman LM (1995) Sensory integration in the bottlenose dolphin: immediate recognition of complex shapes across the senses of echolocation and vision. J Acoust Soc Am 96:722–732
Pant HC, Rosenberg B (1971) Semiconducting diode behavior of bimolecular lipid membranes. J Bioenerg Biomembr 2:163–166
Post N, Von der Emde G (1999) The novelty response in an electric fish: response properties and habituation. Physiol Behav 68:115–128
Rasnow B (1996) The effect of simple objects on the electric field of Apteronotus. J Comp Physiol A 178:397–411
Schepers T (2006) Toward an efficient simulation of biomineralization: a computational study of the apatite/collagen system. Genehmigte Dissertation, Vom Fachbereich Chemie der Technischen Universität Darmstadt
Schuster S, Otto N (2002) Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge. J Exp Biol 205:3307–3320
Schwan HP (1963) Determination of biological impedances. In: Nastuk WL (ed) Physical techniques in biological research, vol VI. Academic, New York, pp 323–407
Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocating signals and the evolution of echolocation. J Comp Physiol A 135:61–84
Szabo T, Fessard A (1965) Le fonctionnement des électrorécepteurs étudiés chez les Mormyres. J Physiol Paris 57:343–360
Szabo T, Fessard A (1974) Physiology of electroreceptors. In: Fessard A (ed) Handbook of sensory physiology, vol III/3. Electroreceptors and other specialized receptors in lower vertebrates. Springer, Berlin, pp 59–124
Théry M, Casas J (2002) Predator and prey views of spider camouflage. Nature 415:133
Toerring MJ, Belbenoit P (1979) Motor programmes and electroreception in mormyrid fish. Behav Ecol Sociobiol 4:369–379
Toerring MJ, Moller P (1984) Locomotor and electric displays associated with electrolocation during exploratory behaviour in mormyrid fish. Behav Brain Res 12:291–306
von der Emde G (1990) Discrimination of objects through electrolocation in the weakly electric fish, Gnathonemus petersii. J Comp Physiol A 167:413–421
von der Emde G (1999) Active electrolocation of objects in weakly-electric fish. J Exp Biol 202:1205–1215
von der Emde G, Bleckmann H (1992) Differential responses of two types of electroreceptive afferents to signal distorsions may permit capacitance measurement in a weakly electric fish, Gnathonemus petersii. J Comp Physiol A 171:683–694
von der Emde G, Ringer T (1992) Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I. Discrimination performance. Ethology 91:326–338
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 175:801–812
von der Emde G, Schwarz S (2000) Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii). Philos Trans R Soc Lond B 355:1143–1146
von der Emde G, Schwarz S, Gomez L, Budelli R, Grant K (1998) Electric fish measure distance in the dark. Nature 395:890–894
Acknowledgments
Kevin Gassmann contributed to gathering the behavioral data. Johan Alcindor and Nicolas Vangout helped in recording the signals. Vincent Férotin provided continuous support throughout the work. Bernard Buisson and Gwenaël Kaminski reviewed the typescript, Patrice Kuzniak and Edie Abrams polished the English. We thank them all for their contributions. We thank also three anonymous referees for their gracious suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Avril, A., Graff, C. Active electrolocation of polarized objects by a pulse-discharging electric fish, Gnathonemus petersii . J Comp Physiol A 193, 1221–1234 (2007). https://doi.org/10.1007/s00359-007-0279-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-007-0279-x