Abstract
Weakly electric fishes use active electrolocation to orient in their environment at night. They emit an electric organ discharge (EOD) with a specialized organ in their tail and sense this signal with epidermal electroreceptors. Objects in the vicinity of the fish locally alter the transepidermal current flow evoked by the EOD and thereby project an “electrical image” on the fish’s skin. By analyzing this image, the fish can detect and three-dimensionally localize objects and also can determine some of their properties, such as the object’s electrical impedance, its shape, and maybe also its size. During electrolocation, peak amplitude and waveform of the local EOD inform the fish about the object’s complex impedance. Object distance is determined by measuring the slope of the electric image, while the determination of object shape and size requires some complex neural calculation of spatial-temporal image parameters.
Mormyrids possess a special type of electroreceptor organs for active electrolocation, called mormyromasts. Each of these organs contains two types of receptor cells, both of which respond to signal amplitude changes, and one also responds to signal waveform. Primary receptor afferents project to the electrosensory lateral line lobe (ELL) forming two somatotopic maps of the body surface. The ELL also receives input originating from the command nucleus in the medulla, which initiates each discharge of the electric organ. The dynamic interaction of this electric organ corollary discharge with the input provided by the primary afferents is essential for the extraction of information about the electric image and thus about the object. During initial processing in ELL, basic features of the electric image are extracted by the projection of a plastic copy of the peripheral electric image onto the ELL maps. The spatial-temporal relationships of the voltage distributions on the fish’s skin are analyzed in relation to the changes that are occurring constantly during active electrolocation. Little is known about the physiology of higher-order electrosensory structures beyond ELL. A major feature of the electrosensory pathway is extensive feedback from higher to lower centers, which might be responsible for many of the dynamic neural response patterns observed.
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References
Assad, C., Rasnow, B., and Stoddard. P.K. (1999). Electric organ discharges and electric images during electrolocation. J. Exp. Biol. 202:1185–1193.
Bastian, J. (1996). Plasticity in an electrosensory system. I. General features of a dynamic filter. J. Neurophysiol. 76:2483–2496.
Bell, C., Bodznick, D., Montgomery, J., and Bastian, J. (1997a). The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav. Evol. 50:17–31.
Bell, C.C. (1990a). Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. II. Intra-axonal recordings show initial stages of central processing. J. Neurophysiol. 63:303–318.
Bell, C.C. (1990b). Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers. J. Neurophysiol. 63:319–332.
Bell, C.C., and Russell, C.J. (1978). Effect of electric organ discharge on ampullary receptors in a mormyrid. Brain Res. 145:85–96.
Bell, C.C., and Szabo, T. (1986). Electroreception in Mormyrid fish. Central Anatomy. In: Electroreception (Heiligenberg, W., ed.), pp. 375–421. New York: Wiley.
Bell, C.C., and von der Emde, G. (1995). Electric organ corollary discharge pathways in mormyrid fish. II. The medial juxtalobar nucleus. J. Comp. Physiol. A. 177:463–479.
Bell, C.C., Bradbury, I, and Russell, C.J. (1976). The electric organ of a mormyrid as a current and voltage source. J. Comp. Physiol. A. 110:65–88.
Bell, C.C., Caputi, A., and Grant, K. (1997b). Physiology and plasticity of morphologically identified cells in the mormyrid electrosensory lobe. J. Neurosci. 17:6409–6423.
Bell, C.C., Finger, T.E., and Russell, C.J. (1981). Central connections of the posterior lateral line lobe in mormyrid fish. Exp. Brain Res. 42:9–22.
Bell, C.C., Grant, K., and Serrier, J. (1992). Sensory processing and corollary discharge effects in the mormyromast regions of the mormyrid electrosensory lobe. I. Field potentials. J. Neurophysiol. 68:843–858.
Bell, C.C., Libouban, S., and Szabo, T. (1983). Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish. J. Comp. Neurol. 216:327–338.
Bell, C.C., Dunn, K., Hall, C., and Caputi, A. (1995). Electric organ corollary discharge pathways in mormyrid fish. I. The mesencephalic command associated nucleus. J. Comp. Physiol. A. 177:449–462.
Bell, C.C., Han, V.Z., Sugawara, Y., and Grant, K. (1997c). Synaptic plasticity in a cerebellum-like structure depends on a temporal order. Nature 387:278–281.
Bennett, M.V.L., Aljure, E., Nakajima, Y, and Pappas, G.D. (1963). Electrotonic junctions between teleost spinal neurons: Electrophysiology and ultrastructure. Science 141:262–264.
Caputi, A.A., Budelli, R., Grant, K., and Bell, C.C. (1998). The electric image in weakly electric fish: Physical images of resistive objects in Gnathonemus petersii. J. Exp. Biol. 201:2115–2128.
Douglas, R.H., Eva, J., and Guttridge, N. (1988). Size constancy in goldfish (Carassius auratus). Behav. Brain Res. 30:37–42.
Dusenbery, D.B. (1992). Sensory Ecology: How Organisms Acquire and Respond to Information. New York: W.H. Freeman.
Finger, T.E., Bell, C.C., and Russell, C.J. (1981). Electrosensory pathways to the valvula cerebelli in mormyrid fish. Exp. Brain Res. 42:22–33.
Grant, K., Bell, C.C., Clausse, S., and Ravaille, M. (1986). Morphology and physiology of the brainstem nuclei controlling the electric organ discharge in mormyrid fish. J. Comp. Neurol. 245: 514–530.
Hall, C., Bell, C., and Zelick, R. (1995). Behavioral evidence of a latency code for stimulus intensity in mormyrid electric fish. J. Comp. Physiol. A. 177: 29–39.
Han, V.Z., Grant, K., and Bell, C.C. (2000). Rapid activation of GABA ergic interneurons and possible calcium independent GABA release in the mormyrid electrosensory lobe. J. Neurophysiol. 83:1592–1604.
Han, V.Z., Bell, C.C., Grant, K., and Sugawara, Y (1999). The mormyrid electrosensory lobe in vitro: Morphology of cells and circuits. J. Comp. Neurol. 404:359–374.
Harder, W. (1968). Die Beziehungen zwischen Elektrorezeptoren, elektrischen Organen, Seitenlinienorganen und Nervensystem bei den Mormyridae (Teleostei, Pisces). Zeit. Vergl. Physiol. 59:272–318.
Heiligenberg, W. (1973). Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei ). J. Comp. Physiol. 87:137–164.
Hopkins, C.D. (1988). Neuroethology of electric communication. Ann. Rev. Neurosci. 11:497–535.
Hopkins, C.D. (1999). Design features for electric communication. J. Exp. Biol. 202:1217–1228.
Huffman, R.F., and Henson, O.W. (1990). The descending auditory pathway and acousticomotor systems: Connections with the inferior colliculus. Brain Res. Rev. 15:295–323.
Kalmijn, A.J. (1974). The detection of electric fields from inanimate and animate sources other than electric organs. In: Handbook of Sensory Physiology (Fessard, A., ed.), pp. 148–200. Berlin: Springer-Verlag.
Kramer, B. (1990). Electrocommunication in Teleost Fishes: Behavior and Experiments. Berlin: Springer-Verlag.
Lissmann, H.W., and Machin, K.E. (1958). The mechanism of object location in Gymnarchus niloticus and similar fish. J. Exp. Biol. 35:451–486.
Meek, J., Grant, K., Sugawara, Y., Hafmans, T.G.M., Veron, M., and Denizot, J.P. (1996). Interneurons of the ganglionic layer in the mormyrid electrosensory lateral line lobe: Morphology, immunohistochemistry, and synaptology. J. Comp. Neurol. 375:43–65.
Meyer, J.H. (1982). Behavioral responses of weakly electric fish to complex impedances. J. Comp. Physiol. 145:459–470.
Meyer, J.H., and Bell, C.C. (1983). Sensory gating by a corollary discharge mechanism. J. Comp. Physiol. A. 151:401–406.
Mohr, C., and von der Emde, G. (1998). Mapping of the nucleus lateralis (torus semicircularis) of the electrosensory system of Gnathonemus petersii. In: New Neuroethology on the Move (Wehner, R., ed.), Proc. 26th Göttingen Neurobiology Conference 1998, p. 54. Thieme, Stuttgart, New York.
Moller, P. (1995). Electric Fishes: History and Behavior. London: Chapman & Hall.
Montgomery, J.C., and Bodznick, D. (1994). An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish. Neurosci. Lett. 174:145–148.
Nieuwenhuys, R., and Nicholson, C. (1969). A survey of the general morphology, the fiber connections, the possible functional significance of the gigantocerebellum of mormyrid fish. In: Neurobiology of Cerebellar Evolution and Development (Llinas, R., ed.), pp. 107–134. Chicago: American Medical Association.
Niso, R., Serrier, J., and Grant, K. (1989). Mesencephalic control of the bulbar electromotor network in the mormyrid Gnathonemus petersii. Europ. J. Neurosci. Suppl. 2:176.
Peters, R.C., Loos, W.J.G., Bretschneider, F., and Baretta, A.B. (1999). Electroreception in catfish: Patterns from motion. Belgian J. Zool. 129:263–268.
Prechtl, J.C., von der Emde, G., Wolfart, J., Karamürsel, S., Akoev, G.N., Andrianov, Y.N., and Bullock, T.H. (1998). Sensory processing in the pallium of a teleost fish, Gnathonemus petersii. J. Neurosci. 18:7381–7393.
Rasnow, B. (1996). The effects of simple objects on the electric field of Apteronotus. J. Comp. Physiol. A. 178:397–411.
Roberts, P.D., and Bell, C.C. (1999). Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J. Comput. Neurosci. 1–15.
Roberts, P.D., and Bell, C.C. (2000). Computational consequences of temporally asymetric learning rules: II. Sensory image cancelation. J. Comput. Neurosci. (in press).
Russell, C.J., and Bell, C.C. (1978). Neuronal responses to electrosensory input in mormyrid valvula cerebelli. J. Neurophysiol. 41:1495–1510.
Schwan, H.P. (1963). Determination of biological impedances. In: Physical Techniques in Biological Research (Nastuk, W.L., ed.), pp. 323–407. New York: Academic Press.
Schwarz, S., and von der Emde, G. (1999). Object classification by the weakly electric fish, Gnathonemus petersii. In: (Eysel, U., ed.), Göttingen Neurobiology Report, 1999, 27th Göttingen Neurobiology Conference, p. 332. Thieme, Göttingen.
Schwarz, S., and von der Emde, G. (2001). Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii. J. Comp. Physiol. A. 186:1185–1197.
Szabo, T, and Hagiwara, S. (1967). A latency change mechanism involved in sensory coding of electric fish (mormyrids). Physiol. Behav. 2:331–335.
Szabo, T., and Wersäll, J. (1970). Ultrastructure of an electroreceptor (Mormyromast) in a mormyrid fish, Gnathonemus petersii. II. J. Ultrastructure Res. 30:473–490.
Van Essen, D.C., and Gallant, J.L. (1994). Neural mechanisms of form and motion processing in the primate visual system. Neuron 13:1–10.
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 (1998). Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation. J. Comp. Physiol. A. 182: 217–224.
von der Emde, G., and Bell, C.C. (1994). Responses of cells in the mormyrid electrosensory lobe to EODs with distorted waveforms: implications for capacitance detection. J. Comp. Physiol. A. 175: 83–93.
von der Emde, G., and Bell, C.C. (1995). The nucleus prae-eminentialis of mormyrid electric fish: Field potentials, somatotopy and single unit activity. 25th Annual Meeting, Society for Neuroscience, p. 184. San Diego, CA.
von der Emde, G., and Bleckmann, H. (1997). Wave-form tuning of electroreceptor cells in the weakly electric fish, Gnathonemus petersii. J. Comp. Physiol. A. 181:511–524.
von der Emde, G, and Bleckmann, H. (1998). Finding food: Senses involved in foraging for insect larvae in the electric fish, Gnathonemus petersii. J. Exp. Biol. 201:969–980.
von der Emde, G., and 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., and 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., and Zelick, R. (1995). Behavioral detection of electric signal waveform distortion in the weakly electric fish, Gnathonemus petersii. J. Comp. Physiol. A. 177:493–501.
von der Emde, G., Gomez Sena, L., Niso, R., and Grant, K. (2000). The midbrain pre-command nucleus of the mormyrid electromotor network. J. Neurosci. 20:5483–5495.
von der Emde, G., Schwarz, S., Gomez, L., Budelli, R., and Grant, K. (1998). Electric fish measure distance in the dark. Naturwissenschaffen 395: 890–894.
von Holst, E., and Mittelstaedt, H. (1950). Das Reafferenzprinzip. Naturwissenschaffen 37:464–476.
Zakon, H.H. (1987). The electroreceptors: diversity in structure and function. In: Sensory Biology of Aquatic Animals (Tavolga, W.N., ed.), pp. 813–850. Berlin, Heidelberg, New York: Springer-Verlag.
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von der Emde, G., Bell, C.C. (2003). Active Electrolocation and Its Neural Processing in Mormyrid Electric Fishes. In: Collin, S.P., Marshall, N.J. (eds) Sensory Processing in Aquatic Environments. Springer, New York, NY. https://doi.org/10.1007/978-0-387-22628-6_5
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DOI: https://doi.org/10.1007/978-0-387-22628-6_5
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