Organization of the larval pre-ecdysis motor pattern in the tobacco hornworm, Manduca sexta

Abstract

The tobacco hornworm, Manduca sexta, undergoes several larval molts before transforming into a pupa and then an adult moth. Each molt culminates in ecdysis, when the old cuticle is shed. Prior to each larval ecdysis, the old cuticle is loosened by pre-ecdysis behavior, which consists of rhythmic compressions that are synchronous along the abdomen and on both body sides, and rhythmic retractions of the abdominal prolegs. Both pre-ecdysis and ecdysis behaviors are triggered by a peptide, eclosion hormone. The aim of the present study was to investigate the neural circuitry underlying larval pre-ecdysis behavior. The pre-ecdysis motor pattern was recorded in isolated nerve cords from eclosion hormone-treated larvae, and the effects of connective transections and ionic manipulations were tested. Our results suggest that the larval pre-ecdysis compression motor pattern is coordinated and maintained by interneurons in the terminal abdominal ganglion that ascend the nerve cord without chemical synaptic relays; these interneurons make bilateral, probably monosynaptic, excitatory connections with identified pre-ecdysis motor neurons throughout the abdominal nerve cord. This model of the organization of the larval pre-ecdysis motor pattern should facilitate identification of the relevant interneurons, allowing future investigation of the neural basis of the developmental weakening of the pre-ecdysis motor pattern that accompanies the larval-pupal transformation.

Ecdysis behaviors and circadian rhythm of ecdysis in the stick insect, Carausius morosus

“…These behaviors appear similar to stereotypic motor programs that have been carefully described and quantified in a number of holometabolous insects (e.g. Truman, 1972; Bainbridge and Bownes, 1981; Novicki and Weeks, 1993; Gammie and Truman, 1999; Baker et al, 1999; Zitnan and Adams, 2000; Zitnan et al, 2002; Park et al, 2002; Clark et al, 2004; Kim et al, 2006a, b; Dai and Adams, 2009; Roller et al, 2010; reviewed by Zitnan and Adams, 2012) along with a number of hemimetabolous insects (eg. Bernays, 1972; Carlson, 1977a & b; Hughes, 1980a-d; Truman et al, 1996).…”

“…Weeks and Truman, 1984a, b; Novicki and Weeks, 1993; Shimoide et al, 2013) along with the identification of key regulators (e.g. Horodyski et al, 1989; Zitnan et al, 1996; Ewer et al, 1994) has led to the generation of a model of the neural network regulating ecdysis.…”

9. Nervous System

“…The behavior is controlled by abdominal motoneurons MN-2 and MN-3 which innervate the tergo-pleural and anterior lateral external muscles (Miles & Weeks 1991). A neural network generating the rhythm is located in the terminal abdominal ganglion (Novicki & Weeks 1993) and conveys rhythmic input to all abdominal motoneurons MN-2 and 3 via a pair of ascending interneurons (Novicki & Weeks 1995).…”

Quantification and analysis of ecdysis in the hornworm, Manduca sexta, using machine vision–based tracking

“…Ecdysis, an essential period at the end of the molt in an insect’s life cycle, facilitates shedding of the old cuticle to allow continued growth and development. It is coordinated by hormonal and neural interactions that regulate activation of various underlying central pattern generator networks (Gammie and Truman 1997; Gammie and Truman 1999; Novicki and Weeks 1993; Zitnan and Adams 2000; reviewed by Ewer and Reynolds 2002). Although a stereotyped behavior, the shedding of the cuticle is fairly complicated and includes a series of distinct patterned motor programs termed pre-ecdysis and ecdysis.…”

“…Pre-ecdysis involves synchronous rhythmic compressions and relaxations along the entire segmented body wall to loosen the cuticle. Ecdysis itself consists of rhythmic anteriorly- directed peristaltic waves that start at the back of the animal and move forward in a wave-like motion, segment by segment (Weeks and Truman 1984; Novicki and Weeks 1993; Zitnan et al 1999). …”