Anatomical and neurochemical consequences of deafferentation in the development of the visual system of the moth Manduca sexta

G. D. Maxwell, John G Hildebrand

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

The primordium of the compound eye of the moth Manduca sexta was removed by surgery within 12 hours after the molt to the pupa. When the operated animals were examined as pharate adults just prior to emergence from the pupal cuticle, no eye tissue was present on the operated side. Histological examination of the brain at successive developmental stages showed that the volume of laminar neuropil on the operated side increased very little after deafferentation while the volume of the control-side laminar neuropil increased more than 20-fold. The impairment of development of the lamina was accompanied by a reduction in the synthesis and storage by the optic lobe of two neurotransmitter candidates, acetylcholine and 5-hydroxytryptamine. The endogenous content of 5-hydroxytryptamine was also reduced in these preparations. Excision of a section of the stemmatal nerve, which connects the primordium of the compound eye to the brain, also arrested the development of the lamina, but in this case the compound eye itself developed apparently normally without making contact with the brain. This finding supports the hypothesis that the centripetal growth of photoreceptor-cell axons normally is contact-guided. Results of neurochemical experiments on retinal tissue argue against the idea that acetylcholine, 5-hydroxytryptamine, or gamma-aminobutyric acid is a likely photoreceptor-cell neurotransmitter. From these and our previous studies of the metamorphosing brain in Manduca we conclude that different classes of neurons in the same central nervous system can exhibit widely different degrees of dependency on their normal innervation for their survival and differentiation.

Original languageEnglish (US)
Pages (from-to)667-680
Number of pages14
JournalJournal of Comparative Neurology
Volume195
Issue number4
StatePublished - 1981
Externally publishedYes

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Manduca
Moths
Serotonin
Photoreceptor Cells
Neuropil
Brain
Acetylcholine
Neurotransmitter Agents
Pupa
gamma-Aminobutyric Acid
Axons
Central Nervous System
Neurons
Growth

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Anatomical and neurochemical consequences of deafferentation in the development of the visual system of the moth Manduca sexta",
abstract = "The primordium of the compound eye of the moth Manduca sexta was removed by surgery within 12 hours after the molt to the pupa. When the operated animals were examined as pharate adults just prior to emergence from the pupal cuticle, no eye tissue was present on the operated side. Histological examination of the brain at successive developmental stages showed that the volume of laminar neuropil on the operated side increased very little after deafferentation while the volume of the control-side laminar neuropil increased more than 20-fold. The impairment of development of the lamina was accompanied by a reduction in the synthesis and storage by the optic lobe of two neurotransmitter candidates, acetylcholine and 5-hydroxytryptamine. The endogenous content of 5-hydroxytryptamine was also reduced in these preparations. Excision of a section of the stemmatal nerve, which connects the primordium of the compound eye to the brain, also arrested the development of the lamina, but in this case the compound eye itself developed apparently normally without making contact with the brain. This finding supports the hypothesis that the centripetal growth of photoreceptor-cell axons normally is contact-guided. Results of neurochemical experiments on retinal tissue argue against the idea that acetylcholine, 5-hydroxytryptamine, or gamma-aminobutyric acid is a likely photoreceptor-cell neurotransmitter. From these and our previous studies of the metamorphosing brain in Manduca we conclude that different classes of neurons in the same central nervous system can exhibit widely different degrees of dependency on their normal innervation for their survival and differentiation.",
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