Omnidirectional Sensory and Motor Volumes in Electric Fish

Abstract

Active sensing organisms, such as bats, dolphins, and weakly electric fish, generate a 3-D space for active sensation by emitting self-generated energy into the environment. For a weakly electric fish, we demonstrate that the electrosensory space for prey detection has an unusual, omnidirectional shape. We compare this sensory volume with the animal's motor volume—the volume swept out by the body over selected time intervals and over the time it takes to come to a stop from typical hunting velocities. We find that the motor volume has a similar omnidirectional shape, which can be attributed to the fish's backward-swimming capabilities and body dynamics. We assessed the electrosensory space for prey detection by analyzing simulated changes in spiking activity of primary electrosensory afferents during empirically measured and synthetic prey capture trials. The animal's motor volume was reconstructed from video recordings of body motion during prey capture behavior. Our results suggest that in weakly electric fish, there is a close connection between the shape of the sensory and motor volumes. We consider three general spatial relationships between 3-D sensory and motor volumes in active and passive-sensing animals, and we examine hypotheses about these relationships in the context of the volumes we quantify for weakly electric fish. We propose that the ratio of the sensory volume to the motor volume provides insight into behavioral control strategies across all animals.

Implications of sensory ecology for species coexistence: biased perception links predator diversity to prey size distribution

“…Examples include eye size that matches the timing of foraging-bouts in ants (Greiner et al 2007), sensitivity to scent profiles of host beetles in closely related necromenic nematodes (Hong and Sommer 2006), olfactory shifts associated with food shifts in Drosophila (Dekker et al 2006), variation in color vision in primate communities (Dominy and Lucas 2001) and even within single primate species (Vogel et al 2007). In weakly electric fish, electrosensory space for prey detection closely matches a species' motor volume (Snyder et al 2007). Information on the underpinnings of these sensory differences is beginning to emerge at the level of genetics (Hong et al 2008), neurotransmitter expression (Park et al 2008) and receptor structure (Greiner et al 2007).…”

Aquatic manoeuvering with counter-propagating waves: a novel locomotive strategy

“…These fish have a higher density of sensory receptors along the top edge of their body [14], which we have previously shown plays an important role in their prey-hunting behaviour [4,5]. For example, our prior research determined that the majority of the detected prey were directly above the body [5].…”

“…The rich locomotor capability of ribbon fin-based propulsion is a remarkable testament to the need for a multi-directional propulsor in an animal with omnidirectional sensing abilities [4]. The phenomenon of counter-propagating waves also provides an approach for generating novel force directions on robotic undulators, an emerging new technology for propelling underwater vehicles [15 -17].…”

“…There are two key capabilities that enable this behaviour. First, the fish can sense objects in all directions around the body [4] through an active sensing system based on self-generated discharges of electricity. Second, the fish propels itself in a manner that facilitates rapid movement in many directions, and rapid changes in direction of movement, such as sub-second reversals in swimming direction [5,6].…”

Variability in Sensory Ecology: Expanding the Bridge Between Physiology and Evolutionary Biology

“…Visual ecology (e.g., Lythgoe 1979;Partridge 1989;Endler 1992;Bowmaker et al 1994;Archer et al 1999;Briscoe and Chittka 2001;Browman and Hawryshyn 2001;Eckert and Zeil 2001;Hart 2001a;Théry and Casas 2002;Land and Nilson 2002;Cronin 2006;Zeil and Hemmi 2006;Rosenthal 2007) and chemical ecology (e.g., Sondheimer et al 1970;Silverstein 1981;Bell and Cardé 1984;Pasteels et al 1983;Hay and Fenical 1988;Duvall et al 1986;Vet and Dicke 1992;Eisner and Meinwald 1995;Koehl et al 2001;Cardé and Millar 2004;Romeo 2005;Müller-Schwarze 2006;Dicke and Takken 2006;Avilla et al 2008;Witzgall et al 2008) have played a central role in the development of sensory ecology into its own field of research. Other key examples of wellstudied sensory systems include echolocation in bats and dolphins (Thomas et al 2002), electroreception in fish (Bullock et al 2005;Arnegard and Carlson 2005;Snyder et al 2007), hearing in frogs and insects (Wilczynski and Ryan 1988;Wiese and Gribakin 1992;Fullard and Yack 1993;Römer 1998;Stumpner and von Helversen 2001;…”