Cell death during gangliogenesis in the leech: competition leading to the death of PMS neurons has both random and nonrandom components

Abstract

The posteromedial, serotonin-containing (PMS) neurons are found in the ventral aspect of certain anterior segmental ganglia of adult leeches. With one exception, these cells are unpaired in all the ganglia where they are found. During early embryogenesis in Hirudo medicinalis, however, a bilateral pair of PMS neurons appears and differentiates in each of the 21 segmental ganglia (SG1-SG21). Over the next several days, one of the pair dies in SG3-SG21. Examination of the PMS neuron in any one of these segments reveals that either the right or the left cell remains, with equal probability, suggesting that the elimination of one of the pair is a random process. When unpaired PMS neurons are examined in pairs of adjacent ganglia, however, the cells are from opposite sides in the majority of cases (approximately 88%). This observation implies that the death of a PMS neuron in 1 ganglion strongly biases which member of the pair of PMS neurons degenerates in adjacent ganglia. Detailed examination of the sequence of degeneration shows that it begins at several separate loci in the nerve cord. We propose that the mechanism responsible for the death of one of the pair of PMS neurons in a segmental ganglion is competition between these 2 cells for some trophic factor, but that the outcome of this competition is predetermined if one of the PMS neurons in an adjacent ganglion has already begun to degenerate.