Development of synaptic connections between muscle sensory and motor neurons: anatomical evidence that postsynaptic dendrites grow into a preformed sensory neuropil.

Abstract

The anatomical development of muscle sensory arbors and dendrites of brachial motoneurons in the spinal cord of the bullfrog was studied by labeling both types of cells with horseradish peroxidase. Sensory and motoneurons were labeled in tadpoles (stages XV-XVIII) by backfilling the triceps nerve in vivo with HRP throughout the stages in development when functional monosynaptic connections between these cells are first being formed. Individual triceps motoneurons were injected with HRP in other tadpoles at the same developmental stages. By stage XV, triceps sensory afferents already projected to and arborized in the ventral sensory neuropil region of the spinal cord where sensory-motor connections are made. In contrast, the dendrites of triceps motoneurons rarely were present in this region until stage XVI. By stage XVII, triceps dendrites in this region were common and they intermingled with the collaterals of muscle sensory axons. Thus, sensory axons supplying limb muscles grow into the future neuropil region well in advance of the arrival of motoneuronal dendrites. Electrophysiological studies have shown that the connections between triceps sensory and motor neurons are already specific at stage XVII, as soon as monosynaptic potentials between these cells can be detected (Frank and Westerfield: J. Physiol. (Lond.) 343:593-610, '83). The present anatomical results demonstrate that the processes of sensory and motor cells are not in close anatomical proximity before this time; thus the selection of appropriate synaptic partners must occur from the outset.