Differing synaptic strengths between homologous mechanosensory neurons

Leeches have four mechanosensory pressure neurons (P cells) in each midbody ganglion. Within a ganglion, P cells show complex electrical and chemical connections that vary between species. In Hirudo verbana, stimulating one P cell causes a weak depolarization followed by a strong hyperpolarization in the other P cells; however, stimulating a P cell in Erpobdella obscura produces strong depolarizations in the other P cells. In this study, we examined interactions between P cells in the American medicinal leech Macrobdella decora. Not only is Macrobdella more closely related to Hirudo than to Erpobdella, but Hirudo and Macrobdella also have very similar behavioral responses to mechanical stimulation. Despite the phylogenetic relationship and behavioral similarities between the two species, we found that intracellular stimulation of one P cell in Macrobdella causes a depolarization in the other P cells, rather than the hyperpolarization seen in Hirudo. Experiments performed in a high Mg(2+), 0 Ca(2+) saline solution and a high Mg(2+), high Ca(2+) saline solution suggest that the P cells in Macrobdella have a monosynaptic excitatory connection, a polysynaptic inhibitory connection, and a weak electrical coupling, similar to the connections between P cells in Hirudo. The difference in net response of P cells between these two species seems to be based on differences in the strengths of the chemical connections. These results demonstrate that even when behavioral patterns are conserved in closely related species, the underlying neural circuitry is not necessarily tightly constrained.