Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis

Abstract

During the metamorphosis of holometabolous insects, the larval nervous system is restructured to provide the circuitry needed by the developing adult. Prominent new centers in the brain, the antennal lobes, arise to receive olfactory afferent axons from the developing adult antennae and provide an excellent system in which to study the development of synapses in a central nervous system. We have examined the anatomy and physiology of developing synapses in the antennal lobes of the moth Manduca sexta during the 18 days of metamorphic adult development. On day 5, the neuropil of the newly emerging antennal lobe condenses into distinct glomeruli, in which intercellular junctional complexes have already begun to form. Although some junctions have associated synaptic vesicles, most complexes are desmosome-like until day 9, when the number of synaptic complexes begins to increase. Early synapses are characterized by membrane-associated densities in at least two abutting cellular processes and a small number of synaptic vesicles clustered near the membrane of one process. As adult development proceeds, the membrane-associated densities become denser and more extensive, and the number of synaptic vesicles in the clusters increases. At day 14 synapses appear ultrastructurally mature, and almost all junctions in the neuropil can be identified as synaptic. Not until day 9 do antennal lobe neurons begin to respond postsynaptically when the antennal nerve is stimulated electrically, suggesting that the earliest synapses observed in the electron microscope may not be made by antennal nerve axons. At first the postsynaptic responses are graded and fatigue rapidly. By day 11, the antennal lobe neurons respond with action potentials, but the fatigability does not decline to adult levels until day 13. Filling of antennal lobe neurons with cobalt reveals that the arborizations of both local interneurons and output neurons continue to mature morphologically until about day 13. Previous work (Schweitzer,

Cholinergic Nerve Terminals in the Central Nervous System of Insects

“…These are as follows: 1) Excitatory postsynaptic potentials (EPSPs) recorded from a GI follow every presynaptic spike with a constant latency of 1.4 ms, which is too long to be attributed to electrical transmis-tained by observation of FHSN-GI contacts throughout embryogenesis (16). This sequence is similar to those described for cultured vertebrate neurons (22) and synapses in the antenna1 lobe of the moth Manduca sexta (26). In all cases, initial filopodial adhesion, mediated by desmosome-like contacts, is followed by accumulation of synaptic vesicles and formation of presynaptic membrane density.…”

Development of depolarization‐induced calcium transients in insect glial cells is dependent on the presence of afferent axons

“…Verapamil-sensitive VACCs have been shown in the glial cells of leech ganglia in situ Deitmer, 1992, 1997;Lohr and Deitmer, 1999 Tucker et al, 2000), serious cell injury probably can be excluded. Rather, the size of the increase in [Ca 2ϩ ] i may exceed the capacity of the (Schweitzer et al, 1976;Tolbert et al, 1983). The time constant of the [Ca 2ϩ ] i recovery of approximately 30 s is in the same range as found for the leech giant glial cell (Nett and Deitmer, 1998).…”

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

“…In contrast to phase II, in phase III, which lasts about 8 days up to adult eclosion, only little synaptogenesis occurs. During this last phase, the glomeruli grow in size between 40 and 130% (Huetteroth and Schachtner, 2005), probably because of the increasing neurite diameters, and the synaptic wiring in the glomeruli is thought to undergo further refinement and maturation (Tolbert et al, 1983;Tolbert, 1989;Dubuque et al, 2001). None of the neurons of the ALs undergo programmed cell death during phases I to III (Schachtner et al, 2004a), and, as all neurons of the ALs are born early in AL development , the neuronal composition of the ALs does not change throughout formation of the ALs.…”