Abstract
Weakly electric fish acquire information about their surroundings by detecting and interpreting the spatial and temporal patterns of electric potential across their skin, caused by perturbations in a self-generated, oscillating electric field. Computational and experimental studies have focused on understanding the electric images due to simple, passive objects. The present study considers electric images of a conspecific fish. It is known that the electric fields of two fish interact to produce beats with spatially varying profiles of amplitude and phase. Such patterns have been shown to be critical for electrosensory-mediated behaviours, such as the jamming avoidance response, but they have yet to be well described. We have created a biophysically realistic model of a wave-type weakly electric fish by using a genetic algorithm to calibrate the parameters to the electric field of a real fish. We use the model to study a pair of fish and compute the electric images of one fish onto the other at three representative phases within a beat cycle. Analysis of the images reveals rostral/caudal and ipsilateral/contralateral patterns of amplitude and phase that have implications for localization of conspecifics (both position and orientation) and communication between conspecifics. We then show how the common stimulation paradigm used to mimic a conspecific during in vivo electrophysiological experiments, based on a transverse arrangement of two electrodes, can be improved in order to more accurately reflect the important qualitative features of naturalistic inputs, as revealed by our model.
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References
Aguilera PA, Castello ME and Caputi A (2001). Electroreception in gymnotus carapo: differences between self-generated and conspecific-generated signal carriers. J Exp Biol 204: 185–98
Assad C (1997) Electric field maps and boundary element simulations of electrolocation in weakly electric fish. Pasadena, CA: California Institute of Technology; University Microfilms Inc, Ann Arbor, MI
Babineau D, Longtin A and Lewis JE (2006). Modeling the electric field of weakly electric fish. J Exp Biol 209: 3636–651
Babineau D, Lewis JE and Longtin A (2007). Spatial acuity and prey detection in weakly electric fish. PLoS Comp Biol 3: e38
Bacher M (1983). A new method for the simulation of electric fields, generated by electric fish and their distortions by objects. Biol Cybern 47: 51–8
Bastian J, Chacron MJ and Maler L (2002). Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22: 4577–590
Bennett M (1971) Electric Organs. In: Fish physiology, Academic Press, New York, pp 347–91
Caputi A and Budelli R (2006). Peripheral electrosensory imaging by weakly electric fish. J Comp Physiol A 192: 587–00
Carlson BA and Kawasaki M (2007). Behavioral responses to jamming and ‘phantom’ jamming stimuli in the weakly electric fish Eigenmannia. J Comp Physiol A 193: 927–41
Chacron MJ, Doiron B, Maler L, Longtin A and 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 and Nelson ME (2005). Modeling signal and background components of electrosensory scenes. J Comp Physiol A 191: 331–45
Chipperfield A, Fleming P (1995) The matlab genetic algorithm toolbox. IEE Colloquium on Applied Control Techniques Using MATLAB 1995/014:10
Crockett D (1986). Agonistic behavior of the weakly electric fish, Gnathonemus petersii. J Comp Physiol 100(1): 3–4
Doiron B, Chacron MJ, Maler L, Longtin A and Bastian J (2003). Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421: 539–43
von der Emde G (1999). Active electrolocation of objects in weakly electric fish. J Exp Biol 202: 1205–215
von der Emde G, Schwarz S, Gomez L, Budelli R and Grant K (1998). Electric fish measure distance in the dark. Nature 395: 890–94
Heiligenberg W (1991). Neural nets in electric fish. MIT Press, Cambridge, MA
Heiligenberg W and Bastian J (1984). The electric sense of weakly electric fish. Ann Rev Physiol 46: 561–83
Heiligenberg W, Baker C and Matsubara J (1978). The jamming avoidance response in Eigenmannia revisited: the structure of a neuronal democracy. J Comp Physiol 127: 267–86
Kramer B and Bauer K (1976). Agonistic behaviour and electric signalling in a mormyrid fish, Gnathonemus pertersii. Behav Ecol Sociobiol 1: 45–1
Lagarias J, Reeds J, Wright M and Wright P (1998). Convergence properties of the nelder-mead simplex method in low dimensions. SIAM Journal of Optimization 9(1): 112–47
Lissmann H and Machin K (1958). The mechanism of object location in gymnarchus niloticus and similar fish. J Exp Biol 35: 451–86
Moller P (1976). Electric signals and schooling behavior in a weakly electric fish, Marcusenius cyprinoides l. (Mormyriformes). Science 193: 697–99
Partridge B, Heiligenberg W and Matsubara J (1981). The neural basis of a sensory filter in the jamming avoidance response: no grandmother cells in sight. J Comp Physiol 145: 153–68
Ramcharitar JU, Tan EW and Fortune ES (2006). Global electrosensory oscillations enhance directional responses of midbrain neurons in Eigenmannia. J Neurophysiol 96: 2319–326
Rasnow B (1996). The effects of simple objects on the electric field of Apteronotus. J Comp Physiol A 178: 397–11
Rasnow B and Bower JM (1996). The electric organ discharges of the gymnotiform fishes: I. Apteronotus leptorhynchus. J Comp Physiol A 178: 383–96
Rasnow B, Assad C and Bower JM (1993). Phase and amplitude maps of the electric organ discharge of the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 172: 481–91
Rose G and Heiligenberg W (1986). Limits of phase and amplitude sensitivity in the torus semicircularis of Eigenmannia. J Comp Physiol A 159: 813–22
Rose G, Kawasaki M and Heiligenberg W (1988). Recognition unit at the top of a neuronal hierarchy? prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously. J Comp Physiol 162: 759–72
Rose GJ and Fortune ES (1999). Mechanisms for generating temporal filters in the electrosensory system. J Exp Biol 202: 1281–289
Rother D, Migliaro A, Canetti R, Gomez L, Caputi A and Budelli R (2003). Electric images of two low resistance objects in weakly electric fish. Biosystems 71: 171–79
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Kelly, M., Babineau, D., Longtin, A. et al. Electric field interactions in pairs of electric fish: modeling and mimicking naturalistic inputs. Biol Cybern 98, 479–490 (2008). https://doi.org/10.1007/s00422-008-0218-0
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DOI: https://doi.org/10.1007/s00422-008-0218-0