Formation of specific monosynaptic connections between muscle spindle afferents and motoneurons in the mouse

Abstract

In adult vertebrates, sensory neurons innervating stretch-sensitive muscle spindles make monosynaptic excitatory connections with specific subsets of motoneurons in the spinal cord. Spindle afferents (la fibers) make the strongest connections with motoneurons supplying the same (homonymous) muscle but make few or no connections with motoneurons supplying antagonistic or functionally unrelated muscles. In lower vertebrates these connections are specific from the time they first are formed, but there is comparatively little information about how these reflex connections form in mammals. We therefore studied the pattern of these synaptic connections during postnatal development in mice. Intracellular recordings were made from identified hindlimb motoneurons in an isolated spinal cord preparation, and monosynaptic inputs from la fibers in identified hindlimb muscle nerves were measured at different times during the first postnatal week. The pattern of connections was specific throughout this period, la fibers made strong connections with homonymous motoneurons but only weak connections with antagonistic motoneurons at every time point examined, from P0 through P7. Even when muscle nerves were stimulated at only 0.1 Hz, the pattern of connections was still highly specific, arguing against a special subpopulation of labile inappropriate connections. The absence of appreciable rearrangements in the pattern of these connections during the first postnatal week is, therefore, analogous to the situation in lower vertebrates, suggesting that mechanisms responsible for establishing this specificity have been conserved during evolution.