Neural organization of peptide-activated ecdysis behaviors during the metamorphosis ofManduca sexta

Summary

• 1. In the tobacco hornworm,Manduca sexta, the same peristalsis motor pattern is employed at both larval and pupal ecdysis (Weeks and Truman 1984). However, one prominent difference between the two behaviors is that at larval ecdysis, rhythmic extensions and retractions of the abdominal prolegs are superimposed on the peristalsis pattern. The present experiments investigated the basis of this behavioral change during the larval-pupal transformation.

• 2. Two retractor muscles of the proleg, the principal planta retractor muscle (PPRM) and the accessory planta retractor muscle (APRM) were chosen for study (Fig. 1). PPRM is singly innervated by motoneuron PPR, while APRM is innervated by two morphologically similar motoneurons, both designated APR (Figs. 2, 3). During larval ecdysis these muscles contract rhythmically to produce proleg retractions, and their motoneurons fire synaptically-driven impulse bursts (Fig. 4).

• 3. During the larval-pupal transformation both muscles degenerate and by pupal ecdysis they are gone (Fig. 5). At the same time motoneurons PPR and APR exhibit massive dendritic reductions (Fig. 3). PPR dies two days after pupal ecdysis while APR survives to adulthood.

• 4. Intracellular recordings from APR and PPR during the pupal ecdysis motor pattern in deafferented preparations showed that both motoneurons were synaptically driven to fire rhythmically in the same pattern as was seen during larval ecdysis, despite their lack of target muscles (Fig. 6).

• 5. Thus, not only was the same peristalsis motor pattern generated at both larval and pupal ecdysis, but the proleg motor pattern was conserved as well. The behavioral differences at the two stages, notably the elimination of proleg movements at pupal ecdysis, resulted solely from the elimination of the peripheral proleg musculature and was not accompanied by the removal of central synaptic inputs to the proleg motoneurons.

• 6. To examine the possibility that the proleg motoneurons continued to participate at pupal ecdysis because they made significant synaptic connections onto other neurons (e.g., as members of the central pattern generator circuit), they were stimulated to see if their activity could either influence ongoing motor activity elsewhere in the nerve cord, or could reset the phasing of the ecdysis motor pattern. These results were uniformly negative.