Synaptic basis of swim initiation in the leech

Summary

• 1. Pairwise intracellular recordings were made from a swim-initiating interneuron (cell 204) and identified motor neurons. No direct connections were found from cell 204 to motor neurons which innervate dorsal and ventral longitudinal muscles. It is the rhythmic activity of these motor neurons which produces body flexions during swimming. The only monosynaptic motor connections made by cell 204 were with ‘flattener’ motor neurons cells 109 and 117, which excite dorsoventral muscles to cause body flattening. During swimming, these motor neurons are active nearly tonically (Fig. 2) and, accordingly, leeches have a strongly flattened body profile.

• 2. Interganglionically, each cell 204 excites both anterior and posterior flattener motor neurons via segmentally repeated, monosynaptic chemical excitatory connections (Figs. 2–5). Intraganglionically, cell 204 excites flattener motor neurons via rectifying electrical connections (Figs. 3, 5). Both inter- and intraganglionically, polysynaptic excitatory connections also link these neurons (Fig. 5). In response to cell 204 activity, flattening behavior has a lower activation threshold than does swimming behavior (Fig. 2). This ensures that body flattening precedes and accompanies swim undulations.

• 3. Pairwise interganglionic recordings were made of cell 204 and four members of the swim central pattern generator (CPG) circuit, the ‘oscillator’ interneurons. During motor pattern resetting caused by passage of current pulses into individual oscillator cells, cell 204's firing pattern was perturbed as well (Fig. 6). However, no synaptic connections were found from oscillator cells to cell 204 (Fig. 7). Furthermore, no synaptic effects of cell 204 onto oscillator cells were observed; cell 204 influenced oscillator cells only insofar as its activity was sufficient to evoke swimming (Fig. 7). This was taken to suggest that cell 204 initiates and modulates swimming by way of synaptic connections with CPG interneurons other than the oscillator cells.

• 4. In some preparations, all cells 204 received tonic, prominent inhibitory postsynaptic potentials (IPSPs) in between swim episodes. Individual IPSPs occurred sequentially in cells 204 in an anterior to posterior progression along the nerve cord. The only other cells in which these IPSPs have been observed are cells 61 and 205, which also have swim-initiating ability. Thus, the IPSPs may be unique to swim-initiating interneurons.