Interactions between bilateral clusters of neuroendocrine cells in Aplysia

Abstract

1. Activity of bilateral clusters of electrotonically coupled neuroendocrine cells (the bag cells) was studied using multiple-site intracellular and extracellular recording techniques in isolated parietovisceral ganglia of three species of Aplysia. Bilateral afterdischarges typically began with spike initiation on one side near the neurite terminals along the pleurovisceral connective; propagation of action potentials then proceeded toward the somata with potentiation to full somatic invasion in the ipsilateral bag cell cluster. This activity potentiated across the parietovisceral ganglion until contralateral spikes were initiated at a point near the bag cell somata (designated site A) and compound bag cell activity was then propagated both inward toward the somata and outward toward the circumesophageal ring of head ganglia. This sequence of events, i.e., "in one side, out the other," could occur several times during an afterdischarge, although outward propagation of activity was rarely maintained for more than 20 spikes. Synchrony between clusters was best during these periods of activity. Usually after a few episodes of this sequence, the sites of spike initiation spontaneously shifted to near the neurite terminals of each side and activity was initiated distally and propagated inward. Asychrony between clusters commonly developed when the sites for spike initiation were near the neurite terminals of each side. 2. Waveforms and temporal sequence of recorded events indicate that at least two sites for spike initiation exist within the neuritic tree of each bag cell cluster. These are the distal terminations of the neurites and a proximal site near the somata. Action potentials could be generated at this proximal site spontaneously or when electrotonically driven by contralateral activity. Removal of the bag cell somata did not interfere with bilateral behavior of the bag cell system. The proximal site is, therefore, not somatic. Activity initiated there was always more synchronous and propagated with a higher conduction velocity than activity initiated at the distal ends of the neurites. 3. Experiments were performed with and without the circumesophageal ring of head ganglia intact. Removal of the head ganglia had no effect on bilaterality of or synchrony within the bag cell system. Systematic stimulations and cuts of head ring connectives suggested that the cerebral ganglion may participate in orthodromic activation of the bag cells. 4. Our findings indicate the bag cells of Aplysia are a homogeneous population of neuroendocrine cells with multiple sites for spike initiation. Either cluster can serve as a pacemaker for the other through potentiation and electrotonic activation of the contralateral cluster at proximal sites on the neurites.