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

Abstract

1. At the culmination of each molt, insects shed their old cuticle by a behavior called ecdysis, which generally involves rhythmic peristaltic body movements. We have compared the abdominal peristalsis behaviors produced by the tobacco hornworm,Manduca sexta, during larval-larval molts (‘larval ecdysis’) and at the larval-pupal molt (‘pupal ecdysis’), to see whether the morphological changes during metamorphosis were accompanied by alterations in the motor patterns. 2. At larval ecdysis, caterpillars shed their old cuticle by means of rhythmic peristaltic contractions which run anteriorly along the body, accompanied by coordinated retractions and extensions of the abdominal prolegs (Fig. 2). During the larval-pupal transformation the prolegs are lost, so that at pupal ecdysis the cuticle is shed by peristalsis alone (Fig. 1). 3. Cinematographic analysis of ecdysing larvae and pupae revealed that the peristaltic movements resulted from each abdominal segment being sequentially pulled forward and partially telescoped into the next anterior segment, due to the contraction of intersegmental muscles (ISMs) in the more anterior segment. Despite the marked changes in body morphology which occurred during the larval-pupal transformation, the pattern of the peristaltic contractions produced at larval and pupal ecdysis was the same (Table 1). 4. The neural basis of these behaviors was investigated in semi-intact, deafferented preparations which produced ecdysis motor patterns in response to a peptide hormone, eclosion hormone (EH), which is the normal blood-borne trigger for ecdysis (Fig. 3). The motoneurons which generated the peristaltic motor patterns in larvae and pupae were identified by recording extracellularly from various nerve branches (Figs. 4, 5, 6, 8) and intracellularly from neuronal somata (Figs. 7, 9). 5. The pattern of the motoneuron bursts was the same during both larval and pupal ecdysis (Table 2). The only apparent difference at the two stages was that pupae exhibited a lower level of tonic background motor activity than did larvae (e.g., Figs. 4, 8). 6. Thus, both behavioral and electrophysiological data indicated that the pattern-generating circuitry underlying abdominal peristalsis remained stable during the larval-pupal transformation. In contrast, the loss of the prolegs at pupation and their consequent absence from pupal ecdysis behavior did suggest a possible stage-specific change in the neural circuitry; this possibility is investigated in an accompanying paper (Weeks and Truman 1984).