During metamorphosis in the hawkmoth Manduca sexfa, muscles of the abdominal body wall undergo a reorganization. Many die at the end of larval life and are replaced in the adult by newly generated muscles. We have identified several of the motoneurons innervating these muscles and followed them through metamorphosis.The morphology of larval motoneurons is correlated with their target location. Those with medial targets have bilateral dendritic fields, whereas those with lateral targets have dendrites restricted to one side of the segmental ganglion. Some motoneurons innervate the same muscle in all stages of life, but the majority lose their larval targets following entry into the pupal stage. Although some of the latter group also die at this time, most survive to innervate a new adult target. These "respecified" motoneurons undergo a period of dramatic dendritic growth during metamorphosis.The results demonstrate that these identified neurons are capable, under the appropriate conditions of existing in more than one stable morphology.Typically the development of the nervous system does not end with the completion of embryogenesis. A postembryonic phase of development is often required to allow fine tuning of sensory (Hubel et al., 1977) and motor (Brown et al., 1976) systems. Even functioning systems may be modified as animals acquire new behavior as they mature (Nottebohm, 1981). The discrete larval, pupal, and adult stages of the holometabolous insects each have their own characteristic morphology and behavior. Their nervous systems must undergo an extensive reorganization in order to direct the behavior of these radically different stages as the animal progresses through its life history.In some instances this reorganization during metamorphosis involves the generation of new neurons by retained embryonic neuroblasts (Edwards, 1969). This is particularly true with regard to the major sensory processing areas of the insect brain (Nordlander and Edwards, 1969a, b, 1970; Meinertzhagen, 1973; White and Kankel, 1978; Matsumoto and Hildebrand, 1981), which receive inputs from a large number of imaginal disc-derived sensory neurons. However, the generation of new neurons is not the only strategy employed by

During insect metamorphosis many larval neurons persist but are modified to serve new behavioral roles at later stages of life. For example, certain larval mechanosensory neurons expand their central arborizations during pupal development and evoke a different behavioral response, the gin trap reflex. The role of the insect steroid hormone, 20-hydroxyecdysone (20-HE) in this developmental change was investigated by removing the normal source of the hormone, followed by topical application of 20-HE to the peripheral somata of the sensory neurons. In prepupal animals that were ligated between the abdomen and thorax to remove the source of ecdysteroids the sensory neurons retained a larval arborization pattern. Topical application of 20-HE to the peripheral sensory neuron somata caused the treated neurons to undergo terminal arbor expansion within the CNS. The treated sensory neurons were not able to evoke the normal pupal behavioral response, but instead caused a larval-like reflex response. In a previous study, sensory neurons that were treated peripherally with a juvenile hormone analog during the commitment peak of ecdysteroids were shown to retain a larval arborization pattern at pupation and to not evoke the gin trap reflex (Levine et al., 1986). Within 4 d of pupation, however, these neurons belatedly developed expanded terminal arbors and evoked the pupal reflex. In the present study, similarly treated animals were ligated at pupation to block the surge in ecdysteroids that normally occurs at this time. This treatment prevented both the delayed expansion and the reflex, whereas topical 20-HE application induced growth and allowed the treated sensory neurons to evoke the gin trap reflex. It is concluded that both 20-HE and juvenile hormone act directly on the cell bodies of the sensory neurons to regulate the growth of their central processes. This growth is necessary but not sufficient for the development of the gin trap reflex, suggesting that other steroid-dependent changes must also occur within the CNS. Thus, as in the vertebrates, steroid hormones direct important developmental events within the insect nervous system.

By discrete manipulation of the endocrine cues that control insect metamorphosis, it has been possible to examine the mechanisms governing the growth of neural processes during development. During the transition from larva to pupa in the hawkmoth, Manduca sexta, identified sensory neurons reorganize their central projections to evoke a new behavior--the gintrap reflex. Topical application of a juvenile hormone analog to the peripheral cell bodies of these sensory neurons during a critical period of development caused them to retain their larval commitment rather than undergo pupal development with the rest of the animal. The sensory neurons retained the larval arborization pattern within the pupal CNS and were unable to evoke the gin-trap reflex. Thus, the hormonal environment of the cell body is critical for controlling growth and synapse formation by distant axonal processes.

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During metamorphosis insects undergo dramatic changes in both form and behaviour. Cell birth and death, as well as neurone respecification all contribute to the overall reorganization of the nervous system. Within the visual and chemosensory processing areas of the insect brain large numbers of newly-generated adult neurones are incorporated into the larval nervous system. In the abdominal ganglia, however, identified larval neurones are retained to assume a new adult role. This respecification of motor neurone function involves not only the acquisition of a new target muscle, but also the reorganization of dendritic morphology, and alterations in the interconnections between neurones. For example, an identified abdominal motor neurone in the hawkmoth, Manduca sexta, grows new dendritic processes and changes its synaptic relationship with an abdominal stretch receptor such that an interaction that was inhibitory during larval life, becomes excitatory in the adult. In another example, identified sensory neurones that evoke a larval flexion behaviour, later participate in the defense gin trap reflex that is characteristic of the pupa. In both instances the formation of new pathways is a two-step process in that the new circuits do not become behaviourally relevant as they are formed, but instead are activated abruptly at the appropriate time. For the gin trap reflex an identified peptide hormone is responsible for activating the circuit.