Synaptic interactions between a muscle-associated proprioceptor and body wall muscle motor neurons in larval and adult Manduca sexta

1. Synaptic remodeling of a proprioceptive circuit during metamorphosis of the insect, Manduca sexta, is described. The stretch receptor organ is a muscle-associated proprioceptor that is innervated by a single sensory neuron. It inserts dorsolaterally in the abdomen in parallel with the intersegmental muscles of each abdominal segment. The synaptic input from the stretch receptor sensory neuron to select abdominal internal (intersegmental) and external muscle motor neurons was characterized in both the larva and adult. 2. In the larva, the sensory neuron provides excitatory synaptic input to motor neurons that innervate muscles ipsilateral to the stretch receptor organ in the body wall; the strongest excitatory synaptic input is to motor neurons that innervate targets in close proximity to the stretch receptor organ. The sensory neuron also provides excitatory synaptic input to motor neurons that innervate contralateral, dorsal targets. However, it inhibits, apparently through a polysynaptic pathway, motor neurons innervating contralateral, lateral, and ventral targets. 3. The synaptic input to intersegmental muscle motor neurons from the stretch receptor sensory neuron changes during metamorphosis. In contrast to the larva, all motor neurons recorded in the adult (both ipsilateral and contralateral) were excited by the sensory neuron. As in the larva, the adult sensory neuron provides the strongest excitatory synaptic input to motor neurons innervating targets in close proximity to the stretch receptor organ. 4. The proprioceptive input to the body wall muscle motor neurons was evaluated to determine whether the pathway is monosynaptic, as has been described in other systems. Spike-triggered signal averaging and synaptic latency measurements suggested that the strongest excitatory synaptic input to motor neurons involves a monosynaptic pathway.