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

Research output: Contribution to journalArticle

136 Citations (Scopus)

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 a 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 showed that antennal sensilla do not begin to be responsive to odors until day 14. Thus the establishment of the synaptic network in the antennal lobe apparently occurs in the absence of functional olfactory input to the system.

Original languageEnglish (US)
Pages (from-to)1158-1175
Number of pages18
JournalJournal of Neuroscience
Volume3
Issue number6
StatePublished - 1983
Externally publishedYes

Fingerprint

Manduca
Moths
Synapses
Synaptic Vesicles
Neurons
Neuropil
Membranes
Axons
Sensilla
Desmosomes
Interneurons
Cobalt
Nervous System
Action Potentials
Fatigue
Insects
Anatomy
Central Nervous System
Electrons
Brain

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. / Tolbert, Leslie P; Matsumoto, S. G.; Hildebrand, John G.

In: Journal of Neuroscience, Vol. 3, No. 6, 1983, p. 1158-1175.

Research output: Contribution to journalArticle

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