1. We have previously shown that Xenopus spinal motoneurons make both chemical and electrical synapses with neighboring motoneurons. Because motoneurons are active during swimming, these synapses would be expected to contribute excitation to their neighbors. The significance of central motoneuron to motoneuron synapses was therefore investigated by analyzing the composition of the fast on-cycle excitation underlying spiking activity during fictive swimming in spinal motoneurons. To accomplish this we developed a method for very local application of drugs around a caudal recorded neuron while still being able to evoke and record essentially unaltered fictive swimming rostrally. 2. Intracellular recordings were made from spinal motoneurons during fictive swimming. Bicuculline (40 microM) and strychnine (2 microM) were used continuously to block inhibitory potentials locally around the motoneurons. The amplitude and duration of the fast excitation underlying spiking activity was measured before and during local applications of excitatory antagonists. 3. The nicotinic antagonists d-tubocurarine (10 microM) and dihydro-beta-erythroidine (10 microM) reduced the amplitude of this excitation by approximately 20%. Nicotinic antagonists also reduced the duration of this fast on-cycle excitation. The kainate/alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM) reduced the amplitude (by approximately 30%) but not the duration of the on-cycle excitation. In the presence of 100 microM Cd2+, which blocks all chemically mediated transmission, a considerable amount (50%) of on-cycle excitation remained. 4. These results suggest that 20% of the on-cycle excitation comes from activation of nicotinic receptors by naturally released acetylcholine (ACh), presumably from other motoneurons.(ABSTRACT TRUNCATED AT 250 WORDS)