Motoneurons supplying the dorsal and ventral parts of the myotome in the lamprey are shown to have different morphological characteristics; furthermore, their pattern of activation during fictive locomotion may differ considerably. Intracellular recordings from motoneurons were performed in an in vitro spinal cord-myotome preparation from segments rostral to the fins. The location of the contracting muscle fibers in the myotome could be observed directly in the dissection microscope during intracellular stimulation of the motoneuron. The motoneurons were injected with Lucifer Yellow, an intracellular dye, and were subsequently reconstructed, sometimes in both a horizontal and a transverse plane. Motoneurons supplying the ventral third of the myotome had a dense, fan-like, dendritic tree and ramifications near the midline. In contrast, motoneurons supplying the dorsal third of the myotome had a more widespread and less dense dendritic tree, with few ramifications near the midline. Some motoneurons supplying the most ventral or dorsal part of the myotome had contralateral dendrites crossing in the ventral commissure and ramifying near contralateral large, reticulospinal Müller fibers. The differences in morphology may indicate that these motoneurons receive different descending inputs. This may be related to the need for an effective control in the dorsoventral plane during righting and steering responses. During fictive locomotion elicited in the isolated spinal cord by bath-applied N-methyl-aspartate, pairs of motoneurons were recorded which subsequently were identified and characterized by intracellular injections of Lucifer Yellow.(ABSTRACT TRUNCATED AT 250 WORDS)