The biomechanical and neural control of hydrostatic limb movements in Manduca sexta

Caterpillars are ecologically successful soft-bodied climbers. They are able to grip tightly to foliage using cuticular hooks at the tips of specialized abdominal limbs called prolegs. The neural control of proleg retraction has been examined in some detail but little is known about how prolegs extend and adduct. This is of particular interest because there are no extensor muscles or any obvious mechanisms for directing hydraulic flow into the proleg. In restrained tobacco hornworms (Manduca sexta), adduction can be evoked by stimulating mechanosensory hairs on the medial surface of the proleg. 3-D kinematics show that extension and adduction occur simultaneously through an unfolding of membrane between the pseudo segments. Hemolymph pressure pulses are not necessary to extend the proleg; instead, the pressure at the base of the proleg decreases before adduction and increases before retraction. It is proposed that these pressure changes are caused by muscles that stiffen and relax the body wall during cycles of retraction and adduction. Electromyographic recordings show that relaxation of the principal planta retractor muscle is essential for normal adduction. Extracellular nerve and muscle recordings in reduced preparations show that medial hair stimulation of one proleg can strongly and bilaterally excite motoneurons controlling the ventral internal lateral muscles of all the proleg-bearing segments. Ablation, nerve section and electromyographic experiments show that this muscle is not essential for adduction in restrained larvae but that it is coactive with the retractors and may be responsible for stiffening the body wall during proleg movements.