A calcium regenerative potential controlling ciliary reversal is propagated along the length of ctenophore comb plates.

Abstract

A calcium regenerative potential controlling ciliary reversal is propagated along the length of ctenophore comb plates ( Modifications of ciliary and flagellar activity in response to stimuli are controlled by the membrane potential in a variety of protozoan and metazoan cells (1-5). In ciliate protozoa, the best-studied example, depolarizing stimuli activate voltage-sensitive Ca2+ channels located exclusively in the ciliary membrane (6)(7)(8)(9) leading to Ca2+ influx into the cilia and to a graded Ca2+-dependent regenerative response recorded from the cell body (1, 2, 4, 5). The increase in Ca2+ concentration triggers a reorientation of the power stroke (ciliary reversal) (10).The small size of most cilia has prevented direct determination of the distribution of Ca2+ channels along the length of the ciliary membrane. Results of previous studies are consistent with either a uniform or an uneven distribution of ciliary Ca2+ channels (7,8,11).To the best of our knowledge, the site(s) or mechanism(s) of action of Ca2+ within the axoneme also is not known. Calmodulin, a putative ciliary Ca2+ sensor (12-15), has been detected along the entire length of cilia (16,17). In contrast, local application of Ca2+ to reactivated cilia and flagella indicate that the Ca2+-sensitive machinery controlling various motor responses is localized to a specific region of the axoneme (18)(19)(20).In this report we take advantage of the large size of ctenophore comb plate cilia to record electrical activity directly from motile cilia. We show that a graded Ca2+-dependent regenerative potential is initiated near the base of the comb plate and propagates to the tip of the cilia. The regenerative response is correlated with reorientation and reversed beating of the comb plate. The Ca2+ conductance, and hence the Ca2+-sensitive machinery controlling ciliary motor responses, is, therefore, likely to be distributed along the ciliary length. MATERIALS AND METHODSPleurobrachia pileus was collected locally. Split comb-row preparations for electrical recording were made as described (21) (Fig. 1 Extracellular glass recording electrodes (inside tip diameter, 10-15 ,um) were attached to a comb plate by gentle suction, thus splitting the plate longitudinally into a narrow sliver attached to the electrode, and a much wider part which was free to beat (Fig. 1B) Fig. 4).Electrical and motor responses of comb plates were elicited by stimulation of the adjoining ectodermal nerve net with trains of bipolar pulses (5 Hz, 5-40 V, 5 msec) delivered by a suction electrode attached to the body surface (Fig. 1B

Elements of a ‘nervous system’ in sponges

“…Although syncytia are common in animals, their method of formation by fusion during embryogenesis is not seen in other sponges or other animals. Epithelial conduction in the comb plates of ctenophores has similar velocities and is also calcium based (Moss and Tamm, 1987), but travels through cells connected by gap junctions. The temperature dependence of the action potential in glass sponges is thought to reflect an adaptation to deep, cold water.…”

Convergent evolution of neural systems in ctenophores

“…Earlier work on the neurobiology of ctenophores performed by Horridge (Bullock and Horridge, 1965;Horridge, 1965c;Horridge, 1974), Tamm (Moss and Tamm, 1986;Moss and Tamm, 1987;Tamm, 1982;Tamm, 1984;Tamm and Moss, 1985;Tamm and Tamm, 1981;Tamm and Tamm, 1987) and others (Haddock, 2007;Satterlie and Case, 1978) revealed a very complex behavioral repertoire in these marine predators. Nevertheless, we know little about ctenophore neurons because classical nerve stains are particularly unreliable in these animals.…”

Ciliary reorientation is evoked by a rise in calcium level over the entire cilium

“…2c,d). This time course is in contrast to the Ca 2ϩ transient during ciliary reversal of ctenophore comb plates, where multiple site recording showed a simultaneous rise in Calcium Green fluorescence from the base to the tip of the cilia [Tamm and Terasaki, 1994], reflecting propagation of a Ca 2ϩ action potential along the length of comb plate cilia [Moss and Tamm, 1987]. The distribution, activation, and role of the presumed Ca 2ϩ conductance in Didinium ciliary membrane is not known.…”