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Physiology Paris ELSEVIER Journal of Physiology - Paris 96 (2002) 363-377

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Physiology Paris ELSEVIER Journal of Physiology - Paris 96 (2002) 363-377 Available online at www.sciencedirect.com Journal of Physiology Paris ELSEVIER Journal of Physiology - Paris 96 (2002) 363-377 www.elsevier.com/locate/jphysparis The electric sense of the paddlefish: a passive system for the detection and capture of zooplankton prey Lon A. Wilkensa,*, Michael H. Hofmannb, Winfried Wojteneka aCenter for Neurodynamics, Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121, USA bInstitute of Zoology, University of Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany Abstract Behavioral and electrophysiological experiments have shown that the elongated paddlefish rostrum, with its extensive population of ampullae of Lorenzini, constitutes a passive electrosensory antenna of great sensitivity and spatial resolution. As demonstrated in juvenile paddlefish, the passive electrosense serves a novel function in feeding serving as the primary, if not exclusive sensory modality for the detection and capture of zooplanktonic prey. Ampullary receptors are sensitive to the weak electrical fields of plankton from distances up to 9 cm, and juvenile paddlefish capture plankton individually with great swimming dexterity in the absence of vision or other stimulus signals. Paddlefish also detect and avoid metal obstacles, the electrical signatures of which are a potential hindrance to their feeding and reproductive migrations. The ampullary receptors, their peripheral innervation and central targets in the dorsal octavolateral nucleus, are described. We also describe the ascending and descending neuronal circuitry of the electrosensory system in the brain based on tracer studies using dextran amines. © 2003 Elsevier Ltd. All rights reserved. Keywords: Paddlefish; Ampullae of Lorenzini; Rostrum; Electrosense; Zooplankton 1. Introduction passive electric sense in plankton feeding by the pad- dlefish, evidence that now provides a functional expla- The paddlefish, Polyodon spathula, is distinctive for its nation for the elongated rostrum and its role as an flat, elongated rostrum and large size. Its size can be 'antennal' organ. In addition, we present new informa- accounted for by a feeding strategy shared by a number tion concerning the neural architecture of the electro- of large aquatic 'grazing' animals including baleen sensory system, including peripheral innervation of the whales, the whale shark and basking sharks. All of the ampullary receptors and brain circuitry. aforementioned animals filter feed, straining large quantities of zooplankton from the water column, a rich resource near the bottom of the food chain. The raison 2. Methods d'etre for the rostrum has remained enigmatic, however, although it has long been known to be covered with A brief description is provided for each of the fol- "sensory pores" [18] of unknown function. Over 60 lowing experimental protocols beginning with the years later, and after considerable debate as to their methods used to establish the electrosensory basis of function, these pores were formally characterized as plankton feeding, the premise for our study of the pad- ampullae of Lorenzini [16], similar to the electrosensory dlefish. Detailed descriptions are available in the refer- ampullae of elasmobranchs and other primitive fish. enced literature. The university Institutional Animal Physiological recordings confirmed their electro- Care and Use Committee approved all experiments. sensitivity [29]. However, the association between the eye-catching rostrum, the electric sense, and plankton 2.1. Feeding behavior feeding was not made until more recently [43]. Here we review evidence that establishes a unique role for the These experiments utilize small paddlefish (12-17 cm long) that feed selectively by capturing individual Correpsonding author. plankton. Feeding was characterized by video analysis E-mail address: [email protected] (L.A. Wilkens). of plankton strikes by fish swimming in place in a 0928-4257/03/S - see front matter CD 2003 Elsevier Ltd. All rights reserved, doi: 10.1016/80928-4257(03)00015-9 364 L.A. Wilkens el at. / Journal of Physiology - Paris 96 (2002) 363-377 recirculating laminar stream of water driven by the overlying cartilage, followed by paralysis with curare propeller of a trolling motor [see also 43,44]. Fish were and washout of the anesthetic. Fish were artificially restricted to a viewing chamber with glass sides. Two irrigated by aerated water flowing over the gills. Stimu- IR-sensitive video cameras recorded their movements, lation of the electroreceptors was by a small silver wire one viewing the fish from the side, the other from electrode, serving as the cathode or anode, referenced to beneath via a 45°-angled mirror. Following baseline a large silver plate electrode at the side of the chamber. experiments in the light, all subsequent experiments Alternatively, a dipole electrode with wire tips separated have been performed in the dark using near infrared by 5 mm was used to deliver stimuli. Constant-current light (>880 nm) for illumination. Plankton, admitted to DC, or sinusoidal AC currents at low frequencies were the stream via a plastic tube, were added at a rate to used to modulate the firing of electroreceptor primary offset consumption and to maintain a density of 1-2 per afferents. We also recorded electrical responses to nat- liter. In some experiments we sought to obstruct poten- ural stimuli, i.e. to plankton glued to a thin glass fila- tial chemo- and mechanosensory signals by adding ment and swept over the receptive field by a pen motor concentrated plankton extract to the water, by encap- lever. Responses were recorded and analyzed using sulating live plankton in agarose, blocking the fish's Spike 2 software (CED, Cambridge, UK). nares, and by creating turbulent water flow. Feeding events were analyzed off line from video taped feeding 2.4. Neuroanatomy strikes. After each capture the tape was reversed to align the plankton with the tip of the rostrum. This reference Innervation of the ampullae was studied by clearing frame was digitized and the coordinates of the plankton thin skin samples with 1% H2O2 over night and and rostrum tip were entered into a computer spread- immersing in a solution of 0.5% sudan black in ethylene sheet for analysis. Feeding strikes equivalent to those glycol containing 10% ethanol for 8-24 h. The tissue aimed at plankton could be elicited also by weak electric was rinsed in ethylene glycol (containing 10% ethanol) fields from dipole electrodes placed in the water of a several hours until the excess stain was washed out. The large holding tank (550 1) [46]. Strikes were recorded tissue was then placed on slides and coverslipped with from sets of four fish in response to weak oscillating ethylene glycol. currents at various intensities and frequencies, again Central projections of the electrosensory system were using infrared illumination and an IR-sensitive video studied by means of applying the neuronal tracer bioti- camera. nylated dextran amine (BDA, molecular weight 3000, Molecular Probes, Inc., Eugene, Oregon, USA) into the 2.2. Avoidance behavior lateral line nerves, dorsal octavolateral nucleus, cere- bellum, and mesencephalic tectum. Before surgery, the Paddlefish sensitivity to a static electric field was tips of small insect pins were dipped into a paste made examined by introducing a 2.5-cm diameter aluminum of BDA dissolved in a small amount of distilled water. rod into the path of a fish swimming in circles near the The BDA paste dried on the tip of the pin. For surgery perimeter of a round tank (95-cm diameter) [14]. animals were anesthetized with MS 222 (0.01%, Sigma). Responses were compared to equivalent sized obstacles The skull was opened with a scalpel, reflecting back a of plastic and insulated aluminum, and to controls with piece of cartilage to expose the brain or nerves. The pins no obstacle. Swimming movements were recorded under were inserted into the tissue and the skull was closed infrared illumination using a computerized tracking and sealed with Vetbond Tissue Adhesive (3M, St. Paul, system (Chromotrack 4.02, San Diego, CA) that detec- MN, USA). After surgery fish were revived by perfusing ted a small reflector glued to the tip of the rostrum. The the gills with aerated water until they restarted respira- obstacles were lowered by a robotic manipulator while tory and swimming movements. Three days after sur- the fish was at the opposite side of the tank and an gery, the animal was deeply anesthetized with MS222 avoidance trial was recorded if the fish passed a criter- (0.05%) and transcardially perfused with phosphate ion point about 35 cm from the target. Approach dis- buffer (PB, pH 7.4, 0.1 M) followed by 4% para- tances and collisions were recorded for 20 fish, with 15 formaldehyde in PB (Fisher Scientific Company, New trials for each type of obstacle. Jersey, USA). After fixation the brain was removed from the skull and stored overnight in fixative in a 2.3. Electrophysiology refrigerator. The brains were transferred to PB for two or more hours and embedded in 7.5% gelatin (Fisher) in Electrically mediated responses were recorded from PB. The gelatin block was stored overnight in 4% par- electroreceptor primary afferents in the anterior lateral aformaldehyde in PB before it was cut on a vibratome line nerve (aLLN) at the level of the dorsal ganglion (OTS-4000, Electron Microscopy Sciences, USA). 100 adjacent to the medulla [43]. The brain was exposed μm sections were collected into PB. Sections were under anesthesia (0.01% MS222) by removal of the washed in PB and endogenous peroxidase destroyed by L.A. Wilkens et al. / Journal of Physiology - Paris 96 (2002) 363-377 365 incubation in 0.3% H2O2 for 10 min. Thereafter, the ducted in the dark, shows their position in vertical space sections were incubated with ABC-solution (Vectastain in front of the fish. As evident in this figure, the majority ABC Kit, Vector Laboratories, Inc, Burlingame, CA, of captures were within 20 mm of the rostrum (56%), USA) and stained with diaminobenzidine containing after which capture frequency falls off rapidly.
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