Modeling an electrosensory landscape

sensors, and the physical distribution of sensors can play a crucial role in a system’s functioning. For instance, the differences detected between two auditory organs lead an animal to locate a sound’s source (Rayleigh, 1877; Durlach and Colburn, 1978). A predator must use sensory input to determine its prey’s distance and heading as precisely as possible. The geometry of sensor location can greatly affect this task. Research into the auditory system of predators such as the barn owl, for example, has revealed that bilateral asymmetry in the auditory system – one ear is higher than the other – facilitates prey capture (Volman and Konishi, 1990). Elasmobranchs can use an electrical sense to locate prey, even in the absence of other cues (Kalmijn, 1966, 1982). Although detailed observations have been made (Kalmijn, 1971, 1982, 1997), a quantitative model for the way in which elasmobranchs ‘see’ their local electrical landscape has yet to emerge. Here, a mathematical model is used to link quantitatively the physical geometry and movement of an elasmobranch to its resulting neural input. Some marine elasmobranchs are sensitive to electric fields of less than 5 nV cm–1, and they possess hundreds of electrically sensitive organs known as the ampullae of Lorenzini (Kalmijn, 1971; Bennett, 1971). The ampullae are small, innervated bulbs, and these are connected to the aqueous environment by narrow canals terminated by pores. Both the ampullae and the canals are filled with an ion-rich jelly with electrical properties approximating those of sea water (Waltman, 1966). A single canal/ampulla system shows a maximum sensory response when an electric field (voltage gradient) is applied parallel to the canal (Murray, 1962). The ampullae are not sensitive to absolutely static electric fields. Instead, they are sensitive to changes in the electric field that occur in the range 0.1–10 Hz, relevant biological frequencies for prey swimming movements or even gill movements (Montgomery, 1984; Tricas et al., 1995). Since the strength of even a static field emanating from stationary prey will necessarily drop off quickly with distance, a predator approaching the prey will perceive a changing electric field. The relative motion between the observer and the source is the key aspect for the underlying electrodynamics. Voltages within an ampulla are amplified by ion-channelmediated interactions between the apical and basal membranes of the ampullary sensing cells (Lu and Fishman, 1994). Sudden voltage changes in the ampullae have been shown to modify firing patterns in the afferent nerves (Murray, 1962; Montgomery, 1984; Wissing et al., 1988; Lu and Fishman, 999 The Journal of Experimental Biology 205, 999–1007 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 JEB3809