Lack of specificity in the interactions of cranial sensory and motoneuron axons in vitro

Abstract

During embryogenesis sensory innervation is established quite precisely, but the mechanisms responsible are poorly understood. Whereas sensory neurons that supply muscle appear to require nearby motor axons to reach their target muscles, sensory neurons that supply skin do not. We have investigated the specificity with which sensory axons interact with motor axons, using the avian trigeminal sensory system, where prospective cutaneous and muscle afferents are anatomically separate. To test whether muscle afferents selectively associate with the appropriate motor axons, we co-cultured muscle afferents from the trigeminal mesencephalic nucleus with appropriate trigeminal motoneurons from rhombomeres 2/3 and with inappropriate facial motoneurons from rhombomeres 4/5. To test whether prospective cutaneous and muscle afferents can be distinguished by their interactions with motor axons, we cocultured cutaneous neurons from trigeminal ganglia with trigeminal motoneurons. Dye labeling and time-lapse videomicroscopy revealed no obvious differences between the interactions of muscle afferents with appropriate and inappropriate motor axons or between the interactions of cutaneous and muscle afferents with motor axons. Sensory axons intermixed freely with and crossed over motor axons without fasciculating, regardless of the combination of sensory and motor axons examined. These results suggest that outgrowing sensory neurons may not yet have distinct identities, raising the possibility that sensory innervation patterns are determined more by spatial or temporal constraints on axon growth than by active pathway or target selection. In contrast, motor axons often retracted upon contacting sensory afferents, indicating that there are marked differences between sensory and motor growth cones at the stages studied.