Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish

Abstract

As part of an attempt to understand the spinal control of the segmented axial musculature in goldfish, commissural spinal interneurons that are electrotonically coupled to the Mauthner axon (M-axon) were studied with intracellular recording and staining to examine their morphology, segmental relationships, and functional role. Prior studies suggested that these cells might mediate the crossed inhibition that blocks excitation of motoneurons on one side of the body during an escape bend to the opposite side. Simultaneous intracellular recordings from a M-axon, a commissural interneuron coupled to it, and a presumed primary motoneuron show that: (1) the interneurons produce monosynaptic, CI⁻-dependent IPSPs in contralateral motoneurons, (2) the interneurons are responsible for the short latency, crossed spinal inhibition in the M-cell network, and (3) more than one interneuron terminates on each postsynaptic cell. Reconstructions of interneurons from wholemounts show that they form a fairly homogeneous morphological class of cells. Each one is unipolar, with an axon that crosses the cord and then usually bifurcates into a short, thin ascending branch and a thicker, longer descending one. Neighboring interneurons have overlapping terminal arbors consistent with the physiological data showing convergence of interneurons onto the same postsynaptic cell. The interneurons showed little relationship with body segments as denned by ventral roots. Their axons usually straddled segmental boundaries, with terminals typically occupying parts of two adjacent segments. Thus the functional unit of these cells is probably not a segment or a complete group of segments, but instead includes only parts of two adjacent segments. The presence of interneurons like these suggests that the overt peripheral segmentation of trunk musculature is not necessarily reflected in the organization of neurons that control those segments. A consideration of some functional characteristics of the activation of overlapping, serially repeated arrays of interneurons by descending pathways leads to the conclusion that the high conduction velocity of the M-axon, and the large size and short longitudinal extent of the axons of the inhibitory interneurons promote a strong, brief inhibition that is appropriate for the production of an escape turn that has a rapid bend to one side.