Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion

Abstract

Cell Tr1, a trigger neuron found in the subesophageal ganglion of the leech,Hirudo medicinalis, is part of a network of subesophageal ganglion neurons which control swimming activity, and makes apparently direct connections to swiminitiating interneurons (SIIs; cells 204 and 205). In this study, we investigated the role of SIIs in swim initiation by cell Tr1. We also examined how brief Tr1 activity controls swim initiation at the levels of the SIIs and of the oscillator neurons. We found: In shortened nerve cord preparations consisting of the head ganglion (supra- and subesophageal ganglia) through segmental ganglia 11 or 12, the effectiveness of swim initiation by Tr1 stimulation was highly correlated with the concurrent injection of depolarizing or hyperpolarizing current into a single cell 204. Tr1 stimulation causes sustained excitation in SIIs, serotonin-containing interneurons and Retzius cells, independent of whether or not swimming is initiated. A short, depolarizing current pulse injected simultaneously into as many as three 204 cells does not replicate the sustained excitation evoked in these cells by Tr1 stimulation. An oscillator neuron, cell 208, is inhibited when Tr1 stimulation fails to elicit swimming, but receives excitatory input from Tr1 otherwise. In another oscillator neuron, cell 115, stimulation of Tr1 suppressed an unidentified source of inhibitory synaptic potentials only on trials which resulted in swim initiation. We conclude that Tr1 stimulation triggers swimming by activating a long-lasting ramp depolarization in the SIIs which, in turn, provide excitatory drive to the swim oscillator. Moreover, Tr1 initiates swimming only when inhibitory inputs to the swim oscillator are suppressed. Thus the brain controls both excitatory and inhibitory descending signals which function to regulate swimming activity in the isolated nerve cord of the leech.