Neural control of leg movements in a metamorphic insect: Sensory and motor elements of the larval thoracic legs in Manduca sexta

Abstract

During the metamorphosis of the hawkmoth Manduca sexta the larval thoracic legs degenerate to be replaced in the adult by legs of very different form and function. This change must be accompanied by a reorganization of the neural circuits controlling leg movements. As an initial step in the study of this reorganization we describe here the sensory and motor elements of this circuitry in the larval stage of life. Sensory neurons innervating mechanoreceptive hairs on the thoracic surface were stained individually with cobalt. Those innervating hairs on the general thoracic surface project topographically into two ventral regions of the segmental ganglia. Sensory neurons innervating leg sensilla also map topographically to the more ventral of these regions but in addition have arborizations in a midlateral region. The density of branching within this lateral “leg neuropil” is greatest for sensory neurons from sensilla on the more distal leg segments. Leg motor neurons were identified with intracellular recording and cobalt injection techniques. Those innervating muscles controlling distal leg segments have dense dendritic arbors in the lateral “leg neuropil,” while motor neurons controlling more proximal segments and muscles of the ventral body wall have extensive arborizations in a dorsomedial region of the ganglion. In general, flexor motor neurons are excited by medial and inhibited by lateral leg sensilla, while the opposite is true of extensors. Distal segment motor neurons respond most strongly to sensory neurons from distal segments, thus suggesting some interaction within the lateral “leg neuropil.” Thus, in the larval nervous system a highly ordered array of of sensory and motor elements underlies the specific behavioral responses of the legs to tactile stimulation.