Adult stingrays use their ampullary electroreceptors to detect prey and locate mates, but the response properties and function of their electrosensory system in the pre-adult stages are unknown. We examined the response properties of Atlantic stingray (Dasyatis sabina) electrosensory primary afferent neurons through ontogeny to determine whether encoding of electrosensory information changes with age, and how it relates to the ontogenetic encoding of biologically relevant electric stimuli. We show that during development electrosensory primary afferents increase resting discharge regularity, show an upward shift in best frequency (BF), an increase in neural sensitivity, and a decrease in bandpass. These ontogenetic changes in the response properties of the stingray electrosense are consistent with sensory adaptations to enhance the avoidance of large predators as young, and increase the location of prey and mates as adults.

1.
Andrianov, G.N., G.R. Broun, O.B. Ilyinsky, and V.M. Muraveiko (1984) Frequency characteristics of skate electroreceptive central neurons responding to electric and magnetic stimulation. Neurophysiology, 16: 365–376.
2.
Art, J.J., and R. Fettiplace (1987) Variation of membrane properties in hair cells isolated from the turtle cochlea. J. Physiol. (Lond.), 385: 207–242.
3.
Art, J.J., A.C. Crawford, and R. Fettiplace (1986) Electrical resonance and membrane currents in turtle cochlear hair cells. Hearing Res., 22: 31–36.
4.
Bennett, M.V.L. (1971) Electroreception. In Fish Physiology (Vol. 5) (ed. by W.S. Hoar and D.J. Randall), Academic Press, New York, pp. 493–574.
5.
Blonder, B.I., and W.S. Alevizon (1988) Prey discrimination and electroreception in the stingray Dasyatis sabina. Copeia, 1988: 33–36.
6.
Bratton, B.O., and J.L. Ayers (1987) Observations on the electric discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behavior. Environ. Biol. Fishes, 20: 241–254.
7.
Carpenter, D.O. (1981) Ionic and metabolic bases of neuronal thermosensitivity. Fed. Proc., 40:2808–2813.
8.
Clusin, W.T., and M.V.L. Bennett (1979) The oscillatory responses of skate electroreceptors to small voltage stimuli. J. Gen. Physiol., 69: 121–143.
9.
Cook, D.A. (1994) Temporal patterns of food habits of the Atlantic stingray, Dasyatis sabina (LeSeur 1824), from the Banana River Lagoon, Florida. MS thesis, Florida Institute of Technology, Melbourne, FL.
10.
Crawford, A.C., and R. Fettiplace (1981) An electrical tuning mechanism in turtle cochlear hair cells. J. Physiol. (Lond.), 312: 377–412.
11.
Fettiplace, R. (1987) Electrical tuning of hair cells in the inner ear. Trends Neurosci., 10: 421–425.
12.
Geisler, C.D. (1968) A model of the peripheral auditory system responding to low-frequency tones. Biophys. J., 8: 1–15.
13.
Hudspeth, A.J. (1989) How the ear’s works work. Nature, 341: 397–404.
14.
Kajiura, S.M., and T.C. Tricas (1996) Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray, Dasyatis sabina. J. Exp. Biol., 199: 2297–2306.
15.
Kajiura, S.M., A.P. Sebastian, and T.C. Tricas (2000) Dermal bite wounds as indicators of reproductive seasonality and behavior in the Atlantic stingray, Dasyatis sabina. Environ. Biol. Fishes, 58: 23–31.
16.
Kalmijn, A.J. (1971) The electric sense of sharks and rays. J. Exp. Biol., 55: 371–383.
17.
Kalmijn, A.J. (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In Handbook of Sensory Physiology (Vol. 3) (ed. by A. Fessard), Springer, Berlin, Heidelberg, New York, pp. 147–200.
18.
Kalmijn, A.J. (1982) Electric and magnetic field detection in elasmobranch fishes. Science, 218:916–918.
19.
Kalmijn, A.J. (1988) Detection of weak electric fields. In Sensory Biology of Aquatic Animals (ed. by J. Atema, R.R. Fay, A.N. Popper and W.N. Tavolga), Springer, New York, pp. 151–186.
20.
Lewis, E.R., and A.J. Hudspeth (1983) Voltage-dependent and ion-dependent conductances in solitary vertebrate hair-cells. Nature, 304: 538–541.
21.
Maruska, K.P., E.G. Cowie, and T.C. Tricas (1996) Periodic gonadal activity and protracted mating in elasmobranch fishes. J. Exp. Zool., 276:219–232.
22.
Mikhailenko, N.A. (1971) Biological significance and dynamics of electrical discharges in weak electric fishes of the Black Sea (in Russian). Zool. Zh., 50: 1347–1352.
23.
Montgomery, J.C. (1984) Frequency response characteristics of primary and secondary neurons in the electrosensory neurons in the electrosensory system of the thornback ray. Comp. Biochem. Physiol., 79A: 189–195.
24.
Montgomery, J.C., and J.A. MacDonald (1990) Effects of temperature on the nervous system: implications for behavioral performance. Am. J. Physiol., 259: 191–196.
25.
Mortenson, J., and R.H. Whitaker (1973) Electric discharges in freeswimming female winter skates (Raja ocellata). Am. Zool., 13: 1266.
26.
New, J.G. (1990) Medullary electrosensory processing in the little skate. I. Response characteristics of neurons in the dorsal octavolateralis nucleus. J. Comp. Physiol. A, 167: 285–294.
27.
New, J.G. (1994) Electric organ discharge and electrosensory reafference in skates. Biol. Bull., 187: 64–75.
28.
Noakes, D.L.G., and J.-G.J. Godin (1988) Ontogeny of behavior and concurrent developmental changes in sensory systems in teleost fishes. In Fish Physiology (Vol. 11) (ed. by W.S. Hoar and D.J. Randall), Academic Press, San Diego, CA, pp. 345–395.
29.
Obara, S., and M.V.L. Bennett (1972) Mode of operation of ampullae of Lorenzini of the skate, Raja. J. Gen. Physiol., 60: 534–557.
30.
Pals, N., P. Valentijn, and D. Verwey (1982) Orientation reactions of the dogfish, Scyliorhinus canicula, to local electric fields. Neth. J. Zool., 32: 495–512.
31.
Peters, R.C. and H. P. Evers (1985) Frequency selectivity in the ampullary system of an elasmobranch fish (Scyliorhinus canicula). J. Exp. Biol., 118: 99–109.
32.
Peters, R.C., and S. van Ieperen (1989) Resting discharge and sensitivity of ampullary electroreceptors in Clarias gariepinus related to convergence ratio during ontogeny. Brain Behav. Evol., 34: 43–47.
33.
Ratnam, R., and M.E. Nelson (2000) Nonrenewal statistics of electrosensory afferent spike trains: implications for the detection of weak sensory signals. J. Neurosci., 20: 6672–6683.
34.
Sanchez, D.Y., and H.H. Zakon (1990) The effects of postembryonic receptor cell addition on the response properties of electroreceptive afferents. J. Neurosci., 10: 361–369.
35.
Sisneros, J.A., and T.C. Tricas (2000) Androgen-induced changes in the response dynamics of ampullary electrosensory primary afferent neurons. J. Neurosci., 20: 8586–8595.
36.
Sisneros, J.A., T.C. Tricas, and C.A. Luer (1998) Response properties and biological function of the skate electrosensory system during ontogeny. J. Comp. Physiol. A, 183: 87–99.
37.
Snelson, F.F., Jr., S.E. Williams-Hooper, and T.H. Schmid (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia, 1988: 729–739.
38.
Stein, R. B. (1967) The information capacity of nerve cells using a frequency code. Biophys. J., 7: 797–826.
39.
Stein, R.B. (1970) The role of spike trains in transmitting and distorting sensory signals. In The Neurosciences – Second Study Program (ed. by F.O. Schmitt), Rockefeller University Press, New York, pp. 597–604.
40.
Tricas, T.C. (1982) Bioelectric-mediated predation by swell sharks, Cephaloscyllium ventriosum. Copeia, 1982: 948–952.
41.
Tricas, T.C., and J.G. New (1998) Sensitivity and response dynamics of electrosensory primary afferent neurons to near threshold fields in the round stingray. J. Comp. Physiol. A, 182: 89–101.
42.
Tricas, T.C., S.W. Michael, and J.A. Sisneros (1995) Electrosensory optimization to conspecific phasic signals for mating. Neurosci. Lett., 202: 29–131.
43.
Tricas, T.C., K.P. Maruska, and L.E.L. Rasmussen (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen. Comp. Endocrinol., 118: 209–225.
44.
Viancour, T.A. (1979) Electroreceptors of a weakly electric fish: II. Individually tuned receptor oscillations. J. Comp. Physiol. A, 133: 327–338.
45.
Vischer, H.A. (1995) Electroreceptor development in the electric fish Eigenmannia: a histological and ultrastructural study. J. Comp. Neurol., 360: 81–100.
46.
Wilkens, L.A., D.F. Russell, X. Pei, and C. Gurgens (1997) The paddlefish rostrum functions as an electrosensory antenna in plankton feeding. Proc. R. Soc. Lond. B. Biol. Sci., 264: 1723–1729.
47.
Wourms, J.P. (1977) Reproduction and development in chondrichthyan fishes. Am. Zool., 17: 379–410.
48.
Zakon, H.H. (1984) Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J. Comp. Neurol., 228: 557–570.
49.
Zakon, H.H. (1987) Variation in the mode of receptor cell addition in the electrosensory system of gymnotiform fish. J. Comp. Neurol., 262: 195–214.
50.
Zakon, H.H., and J.H. Meyer (1983) Plasticity of electroreceptor tuning in the weakly electric fish Sternopygus dariensis. J. Comp. Physiol. A, 153: 477–487.
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