Differentiation of insect sensory neurons in the absence of their normal synaptic targets

Sensory neurons in the antenna of the moth, Manduca sexta, arise and differentiate during the 18 days of metamorphosis from pupa to adult, sending axons to the brain. To assess the trophic dependence of developing antennal neurons on their targets, we studied antennae from surgically debrained animals. If the brain is removed 1 to 45 hr after pupal ecdysis (before and during the period when antennal neurons arise by cell divisions), adult development can be triggered by injection of β-ecdysone; if the brain is removed 50 to 60 hr after pupal ecdysis (before antennal axons contact the brain), metamorphosis proceeds spontaneously. Neurons proliferate normally and differentiate extensively in the antennae of debrained animals. They acquire a characteristic size and shape, elaborate axons and dendrites, migrate to appropriate positions in the sensilla, accumulate components of a neurotransmitter system (acetylcholine, choline acetyltransferase, and acetylcholinesterase), and generate electrical responses to olfactory and mechanical stimuli. Antennal sensory neurons thus differ from a variety of vertebrate neurons, which fail to mature when deprived of their synaptic targets.