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Fish Perform Spatial Pattern Recognition and Abstraction by Exclusive Use of Active Electrolocation

2004; Elsevier BV; Volume: 14; Issue: 9 Linguagem: Inglês

10.1016/j.cub.2004.04.039

1879-0445

Christian Graff, Gwenaël Kaminski, Michael A. Gresty, Théophile Ohlmann,

Fish Ecology and Management Studies

The field generated by the electric organ of weakly electric fish varies with the electrical properties of nearby objects [1Rasnow B The effects of simple objects on the electric field of Apteronotus.J. Comp. Physiol. [A]. 1996; 178: 397-411Google Scholar]. Correspondingly, current fluxes in this field differentially stimulate the electroreceptors in the fish's skin [2Bullock, T.H., and Heiligenberg, W. (1986). Electroreception. (New York: J. Wiley and Sons).Google Scholar]. Thus, resistors are to conductors and insulators as gray is to black and white in optics. Additionally, the capacitances of plants and insect larvae contrast with those of water or stones, giving effects comparable to "coloration" [3Meyer H Behavioral responses of weakly electric fish to complex impedance.J. Comp. Physiol. [A]. 1982; 145: 459-470Crossref Scopus (48) Google Scholar]. Receptors [4von der Emde G Bleckmann H Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish, Gnathonemus petersii.J. Comp. Physiol. [A]. 1992; 171: 683-694Google Scholar] arrayed over a large area of the skin act like a retina upon which the discharge projects "electric images" [5Caputi A Budelli R Grant K Bell C The electric image in weakly electric fish physical images of resistive objects in Gnathonemus petersii.J. Exp. Biol. 1998; 201: 2115-2128PubMed Google Scholar]. By further central processing, the fish also discriminate between objects according to their composition [6Lissmann H.W Machin K.E The mechanism of object location in Gymnarchus niloticus and similar fish.J. Exp. Biol. 1958; 35: 451-486Google Scholar], size, or distance [7von der Emde G Schwarz S Gomez L Budelli R Grant K Electric fish measure distance in the dark.Nature. 1998; 395: 890-894Crossref PubMed Scopus (149) Google Scholar], a procedure termed "electrolocation" [8Lissmann H.W On the function and evolution of electric organs in fish.J. Exp. Biol. 1958; 35: 156-191Google Scholar], analogous to echolocation in bats [9Griffin D.R Echolocation in blind men, bats and radar.Science. 1944; 100: 589-590Crossref PubMed Scopus (74) Google Scholar]. Here we demonstrate that G. petersii and S. macrurus can also recognize 3D orientations and configurations and extract and generalize spatial features solely with their electrical sense. We presented fish with virtual electrical "objects" formed from electrodes set flush in the inner surface of a Y maze with various patterns of external connectivity. With reward and aversion training, the fish could recognize similar electrode configurations and extract a feature, e.g., a vertical connectivity, present in various novel configurations. Previously, shape recognition has only been shown in electrolocating fish when they are in full mechanical contact with solid objects [10von der Emde G Schwartz S Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly-electric fishes (Gnathonemus petersii).Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000; 355: 1143-1146Crossref PubMed Scopus (10) Google Scholar].