Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth, Manduca sexta

Abstract

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

Functional differentiation of adult neural circuits from a single embryonic network

“…However, it appears that, in Homarus, the maturation of the adult neural networks involves neither the elimination of certain neuronal elements by programmed cell death (Truman, 1983;Oppenheim, 1991) nor the addition of elements by postembryonic neurogenesis (Thomas et al, 1984), because the final neuronal population in the STG occurs very early and remains stable during the course of subsequent development (Garzino and Reichert, 1994). Growth or regression of some dendritic structures can modify neuronal circuitry during development (Levine and Truman, 1985;Jacobs and Weeks, 1990) and in some adult nervous systems under the influence of steroid hormones (Nottebohm, 1981;Forger and Breedlove, 1987), but such dendritic remodelling has not been examined in the STNS. Developmental alterations in neural network activity may occur at three main levels involving (1) synaptic connections, (2) cellular properties, (3) descending modulatory inputs.…”

Apoptosis of neuronal cells in the brains of postembryonic silkworms Bombyx mori (Lepidoptera: Bombycidae)

“…These changes include the neuronal apoptosis of brains during the transformation of larva to pupa (Truman et al, 1993). Since earlier studies on neuronal apoptosis concentrated on specific neurons of the M. sexta ventral ganglia in primary culture using 20E (Truman, 1983;Truman & Schwartz, 1984;Levine & Truman, 1985;Prugh et al, 1992;Weeks & Davidson, 1994;Streichert & Weeks, 1995;Sandstrom & Weeks, 1996;Streichert et al, 1997;Hoffman & Weeks, 1998;Kraft et al, 1998;Hoffman & Weeks, 2001;Zee & Weeks, 2001;Kinch et al, 2003), it is now important for insect neurobiologists to understand the pattern or mechanism of neuronal apoptosis in the brain during postembryonic development. The silkworm, B. mori, is recognized by entomologists as one of the most easily-reared and widely-used model insects.…”

Dynamic properties of a locomotory muscle of the tobacco hornwormManduca sextaduring strain cycling and simulated natural crawling

“…The muscles driving these activities are small, each consisting of 2-14 fibers, typically 4-6·mm long in an early fifth instar larva. There are about 70 muscles per larval segment layered beneath the soft cuticle to which they are attached (Barth, 1937;Beckel, 1958;Levine and Truman, 1985). Most lie within a single segment and are innervated by a single motoneuron (Levine and Truman, 1985).…”

“…There are about 70 muscles per larval segment layered beneath the soft cuticle to which they are attached (Barth, 1937;Beckel, 1958;Levine and Truman, 1985). Most lie within a single segment and are innervated by a single motoneuron (Levine and Truman, 1985). Nearly all are oriented longitudinally or obliquely, and none circumferentially as in earthworms or other organisms that accomplish motion by peristalsis (Quillin, 1998;Quillin, 2000).…”