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Ampullary sense organs, peripheral, central and behavioral electroreception in chimeras (Hydrolagus, Holocephali, Chondrichthyes).

Ampullary sense organs are distributed in groups over the head of Hydrolagus colliei with their pores in clusters and innervated by the buccal, hyomandibular and superficial ophthalmic branches of the anterior lateral line nerve. The ampullae contain ciliated sense cells in an alveolate-shaped epithelium, which communicates to the surface through a jelly-filled tube. The sense cells synapse at their bases with the afferent nerve fibers that terminate in the dorsal nucleus of the anterior lateral line lobe of the medulla. The anatomy and ultrastructure support the homology with the ampullae of Lorenzini of elasmobranchs. Single units recorded from the buccal branch of the anterior lateral line nerve are either lateral line or ampullary in character, the former being sensitive only to mechanical stimuli, the latter to both mechanical and to weak electric stimuli. They are also distinguished by the positions of their receptive fields. The electroreceptive units are spontaneously active and are excited by a cathode placed near the opening of their pore and inhibited by an anode. Compound evoked potentials are recorded from beneath the lateral aspect of the tectum in response to weak electric fields in the bath. Each recording locus has a best position and orientation of the electric field. The electric fields are effective if their duration is longer than ca. 2 ms; longer than 10 ms makes no difference until an OFF effect becomes distinct at ca. 50 ms. The reception is tuned to low frequencies but is not sensitive to maintained current (DC). Evoked potentials summating moderate numbers of responses are clear at < 1 microV/cm. Ratfish were conditioned in a ring-shaped tank to reverse the direction of swimming when an electric field was switched ON. The stimulus was a 5 Hz square wave or the onset of a DC of 1-10 microA between a pair of electrodes on the floor of the tank. The fish responded to fields as weak as 0.2 microV/cm. A specialized sense modality for electroreception, similar to that in elasmobranchs and most other groups of nonteleost fishes, except for Myxini and Neopterygii (holosteans), is present in the subclass Holocephali. The notion is supported that this modality and its central as well as peripheral apparatus arose early in the evolution of vertebrates. Only two losses of the whole system need be hypothesized, on this idea, once in the ancestors of the hagfishes and once in the ancestors of the neopterygians, which include the teleosts. Some orders of teleosts then evolved a new system of electroreception independently. The ciliary receptor cells are probably primitive; microvillar sense cells evolved independently.