Multifunctional features of a gastrodermal sensory cell in Hydra: three-dimensional study

Abstract

Computer-assisted, three-dimensional reconstructions of two gastrodermal sensory cells from transmission electron micrographs of serial sections of Hydra revealed a unipolar morphology with the nucleus near an apical cilium and a simple unbranched axon with a widened terminal. The sensory cells were similar in size and shape to a unipolar sensory cell isolated from macerated gastrodermis and examined with scanning electron microscopy. In thin sections, the cells were characterized by the presence of numerous dense-cored vesicles in the axon and its terminal. A few dense-cored vesicles were aligned at electron-dense synaptic foci in the axon terminal of the sensory cell, which formed an axo-axonal synapse with a nearby centrally located ganglion cell and a neuromuscular synapse with the basal myoneme of a digestive cell. The ganglion cell possessed a perikaryal cilium and a slender axon that extended adjacent to the sensory cell terminal, where it formed an en passant axo-axonal synapse in reciprocal arrangement with that of the sensory cell. In addition, the ganglion cell axon formed a neuromuscular synapse in sequence with the sensory cell axo-axonal synapse. The presence of a large number of neurosecretory-like granules, apical cilium and reciprocal interneuronal and neuromuscular synaptic loci suggests that this gastrodermal sensory cell, characterized ultrastructurally for the first time, represents a third type of multifunctional neuron in Hydra. Thus, Hydra may contain primitive stem-like neurons, which are sensory-motor and also function in both neurosecretion and neurotransmission.