Novel bridge of axon‐like processes of epithelial cells in the aboral sense organ of ctenophores

Abstract

We describe by light and electron microscopy a novel structure in the aboral sense organ (apical organ) of cydippid (Pleurobrachia) and lobate (Mnemiopsis) ctenophores. An elevated bundle of long, thin, microtubule-filled processes arises from the apical ends of two groups of epithelial cells located on opposite sides of the apical organ along the tentacular plane of the body. This bundle of axon-like processes arches over the epithelial floor like a bridge, with branches at both ends running toward opposing pairs of ciliary balancers that are motile pacemakers for the rows of locomotory ciliary comb plates. The bridge in Pleurobrachia is ϳ40 m long and 3-4 m wide and consists of ϳ60 closely packed processes, 0.2-0.8 m thick, containing vesicles and numerous microtubules running parallel to their long axes. There are ϳ30 epithelial cells in each of the two groups giving rise to the bridge and each cell forms a single process, so roughly half of the processes in the bridge must originate from cells on one side and diverge into branches to a pair of balancers on the opposite side of the apical organ. The 150 -200 cilia in each balancer arise from morphologically complex cellular projections with asymmetric lateral extensions directed towards a fork of the bridge. Presynaptic triad structures and vesicles are found in this region but clear examples of synaptic contacts between bridge processes and balancer cells have not yet been traced. Cydippid larvae of Mnemiopsis have a conspicuous bridge along the tentacular plane of the apical organ. Beroid ctenophores that lack tentacles at all stages do not have a bridge. We discuss the possibility that the bridge is an electrical conduction pathway to balancers that coordinates tentacle-evoked swimming responses of ctenophores, such as global ciliary excitation.

Formation of the Statolith in the Ctenophore Mnemiopsis leidyi

“…A surprising finding was that the statolith of Mnemiopsis is not a spherical mass of lithocytes as generally supposed (Hyman, 1940;Horridge, 1971;Barnes, 1980;Tamm, 1982;Pearse et al, 1987;Brusca and Brusca, 1990;Tamm and Tamm, 2002). Aboral views as well as lateral views (Figs.…”

“…As a result, two opposing pairs of closely set balancers are spaced widely apart along the tentacular plane (Fig. 1B, C, E, F) (Tamm, 1982(Tamm, , 2014aTamm and Tamm, 2002). The longer a axis of the statolith and wider spacing of the balancer pairs is thus orthogonal to the expanded sagittal plane of the somewhat flattened body of Mnemiopsis ( Fig.…”

“…Four clefts, or notches, at 45°to the tentacular and sagittal planes mark the locations and insertions of the four balancers. The superellipsoidal shape and orientation of the statolith correspond to the arrangement of the four balancer bases, which arise at the vertices of a rectangle with a length/width ratio of about 3:1, with the longer sides oriented parallel to the tentacular plane (Tamm and Tamm, 2002). As a result, two opposing pairs of closely set balancers are spaced widely apart along the tentacular plane (Fig.…”

Convergent evolution of neural systems in ctenophores

“…This complex controls locomotion, acting as gravity (statocyst) and possible light sensors (Aronova, 1979;Hernandez-Nicaise, 1991;Tamm, 1982). Axon-like processes of epithelial cells in the aboral organ resemble neurons; a fact that might be used to support earlier hypotheses about the possible evolution of nerves from epithelial conduction tissue (Tamm and Tamm, 2002). The impulses originating from primarily mechanosensory cells that bear the balancers reach the comb rows through the ciliary tracts.…”

“…The aboral organ (it is sometimes less correctly named as the apical organ because there is an analogous structure in bilaterian larvae) is the primary sensory 'brain'-type structure located at the aboral pole of the animal. The anatomy of the aboral complex is well described (Aronova, 1974;Aronova, 1975;Aronova et al, 1979;HernandezNicaise, 1991;Tamm, 1982;Tamm and Tamm, 2002). This complex controls locomotion, acting as gravity (statocyst) and possible light sensors (Aronova, 1979;Hernandez-Nicaise, 1991;Tamm, 1982).…”