1. Spontaneous and evoked synaptic inputs were recorded in vitro in the axons of lamprey reticulospinal neurones. After isolation of the axon from its somata, synaptic inputs were recorded using microelectrode and whole-cell patch clamp recording techniques. 2. Single stimuli applied to the spinal cord elicited Ca(2+)-dependent synaptic potentials with short latencies in reticulospinal axons. These synaptic inputs are capable of summation and generate sufficient depolarization to raise the membrane potential beyond threshold to initiate action potentials. Action potential initiation in the absence of the cell body indicates that these axons show synaptic integration. 3. Both evoked and spontaneous responses comprise at least two components of synaptic drive: a slow component (rise time of 9.6 +/- 2.1 ms) with a reversal potential of -53 +/- 19 mV and a fast component (rise time as fast as 0.85 ms) with a reversal potential of 0.3 +/- 9.1 mV. The responses are Ca2+ dependent, and are blocked by the substitution of Ba2+ for Ca2+ in the saline solution. 4. The slow component of synaptic input was blocked by the gamma-aminobutyric acidA (GABAA) receptor antagonist bicuculline (5 microM). The fast component was blocked by the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor antagonist 6-cyano-7-nitroqinoxaline-2,3-dione (CNQX; 10 microM) in Ringer solution containing physiological concentrations of Mg2+. Following removal of Mg2+ from the superfusate a further excitatory component was identified that was blocked by application of the N-methyl-D-aspartate (NMDA) receptor antagonist 2-amino-5-phosphonopentanoate (AP5; 100 microM). 5. Comparison of the kinetic properties and the voltage sensitivity of the isolated components of evoked and spontaneous synaptic activity indicate that these responses are mediated by similar synaptic inputs. 6. These results suggest that axons and presynaptic terminals receive excitatory and inhibitory ionotropic receptor-mediated inputs. Summation of these inputs is possible indicating that the axons act as sites of synaptic integration similar to the role previously attributed only to neuronal dendrites and somata.