Neural control of leg movements in a metamorphic insect: persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta.

During metamorphosis of the hawkmoth Manduca sexta, the larval thoracic legs along with their associated sensory organs and muscles degenerate and new adult legs develop. The larval legs are small and relatively simple structures capable of lateral extension and medial flexion allowing them to grasp the substrate as the caterpillar crawls along. By contrast, the adult legs are used for walking with an alternating gait. They are much larger than the larval legs and articulate such that they are capable of movement in several directions. This change in form and function is accompanied by a reorganization of the neural circuits controlling leg movements. In a previous report (Kent and Levine: J. Comp. Neurol. 271:559-576, '88) we described motor neurons innervating the larval prothoracic legs, and here we describe motor neurons innervating the prothoracic legs of the adult. Using a combination of cobalt staining methods and the persistent fluorescent dye Fluoro-Gold, we have found that some, if not all, larval leg motor neurons are retained and innervate the new adult leg muscles. Moreover, we have been able to discover the fate of individual larval leg motor neurons by marking a single larval neuron with Fluoro-Gold and using a second fluorescent dye to double label the same neuron in the adult. Our results suggest that specific larval leg motor neurons innervate corresponding muscles in the adult stage, although their apparent function is significantly different. In addition, the motor neurons undergo significant remodeling of their dendritic branching patterns during metamorphosis, alterations which doubtless contribute to their new roles in adult behavior.