Skip to main content
Log in

Acetylcholinesterase activity in antennal receptor neurons of the sphinx moth Manduca sexta

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

We have used a cytochemical technique to investigate the distribution of acetylcholinesterase (AChE) activity in the antenna of the sphinx moth Manduca sexta. High levels of echothiophate-insensitive (presumably intracellular) AChE activity were found in six different types of antennal receptors localized in specific regions of the three antennal segments of the adult moth. Mechanosensory organs in the scape and pedicel, the Böhm bristles and Johnston's organ, are innervated by AChE-positive neurons. In each annulus of the antennal flagellum, AChE-positive neurons are associated with six sensilla chaetica and a peg organ, probably a sensillum styloconicum. At least 112 receptor neurons (8–10 per annulus) innervating the intersegmental membranes between the 14 distalmost annuli also exhibit high levels of echothiophate-resistant AChE. In addition, each annulus has more than 30 AChE-positive somata in the epidermis of the scale-covered (back) side of the flagellum, and 4 AChE-positive somata reside within the first annulus of the flagellum. Since none of the olfactory receptor neurons show a high level of echothiophateresistant AChE activity, and all known mechanoreceptors are AChE-positive, apparently “intracellular” AChE activity in the antenna correlates well with mechanosensory functions and is consistent with the idea that these cells employ acetylcholine as a neurotransmitter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 67:69–139

    Google Scholar 

  • Altner H, Schaller-Selzer L, Wohlrab I (1983) Poreless sensilla with inflexible sockets. A comparative study of a fundamental type of insect sensilla probably comprising thermo- and hygroreceptors. Cell Tissue Res 234:279–307

    Google Scholar 

  • Arbas EA (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159:849–857

    Google Scholar 

  • Becker D (1978) Elektrophysiologische Untersuchungen zur Feuchterezeption durch die styloconischen Sensillen bei Mamestra brassicae L. (Lepidoptera, Noctuidae). Doctoral Dissertation, Regensburg, FRG

  • Bell RA, Joachim FA (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373

    Google Scholar 

  • Boeckh J, Kaissling K-E, Schneider D (1965) Insect olfactory receptors. Cold Spring Harbor Symp Quant Biol 30:26–280

    Google Scholar 

  • Böhm LK (1911) Die antennalen Sinnesorgane der Lepidopteren. Arb Zool Inst Wien 14:219–246

    Google Scholar 

  • Brimijoin S, Skau K, Wiermaa MJ (1978) On the origin and fate of external external acetylcholinesterase in peripheral nerve. J Physiol 285:143–158

    Google Scholar 

  • Camazine SM, Hildebrand JG (1979) Central projections of antennal sensory neurons in mature and developing Manduca sexta. Soc Neurosci Abstr 5:492

    Google Scholar 

  • Christensen TA, Hildebrand JG (1984) Functional anatomy and physiology of male-specific pheromone-processing interneurons in the brain of Manduca sexta. Soc Neurosci Abstr 10:862

    Google Scholar 

  • Gewecke M (1972a) Antennen und Stirn-Scheitelhaare von Locusta migratoria L. als Luftströmungs-Sinnesorgane bei der Flugsteuerung. J Comp Physiol 80:57–94

    Google Scholar 

  • Gewecke M (1972b) Bewegungsmechanismus und Gelenkrezeptoren der Antennen von Locusta migratoria L. (Insecta, Orthoptera). Z Morphol Ökol Tiere 71:128–149

    Google Scholar 

  • Haug T (1985) Ultrastructure of the dendritic outer segments of sensory cells in poreless (‘no-pore’) sensilla of insects. A cryofixation study. Cell Tissue Res 242:313–322

    Google Scholar 

  • Hildebrand JG (1980) Development of putative acetylcholine receptors in normal and deafferented antennal lobes during metamorphosis of Manduca sexta. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland, Amsterdam, pp 209–220

    Google Scholar 

  • Hildebrand JG, Hall LM, Osmond BC (1979) Distribution of binding sites for 125I-labeled α-bungarotoxin in normal and deafferented antennal lobes of Manduca sexta. Proc Natl Acad Sci USA 76:499–503

    Google Scholar 

  • Hoskins S, Hildebrand JG (1983) Neurotransmitter histochemistry of neurons in the antennal lobes of Manduca sexta. Soc Neurosci Abstr 9:216

    Google Scholar 

  • Kaissling K-E (1987) RH Wright lectures on insect olfaction. Colbow K (ed) Simon Fraser University, Burnaby, BC, Canada

    Google Scholar 

  • Kaissling K-E, Thorson J (1980) Insect olfactory sensilla: structural, chemical and electrical aspects of the functional, organization. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland, Amsterdam, pp 261–282

    Google Scholar 

  • Kaissling K-E, Hildebrand JG, Tumlinson JH (1989) Pheromone receptor cells in the male moth Manduca sexta. Arch Insect Biochem Physiol 10:273–279

    Google Scholar 

  • Karnovsky MJ, Roots L (1964) A “direct-coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12:219–221

    Google Scholar 

  • Keil TA (1989) Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta. Tissue Cell 21:139–151

    Google Scholar 

  • Keil TA, Steinbrecht RA (1984) Mechanosensitive and olfactory sensilla of insects. In: King RC, Akai H (eds) Insect ultrastructure, vol 2. Plenum, New York, pp 477–516

    Google Scholar 

  • Kreissl S, Bicker G (1989) Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71–84

    Google Scholar 

  • Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne. (Apis mellifica L). Z Vergl Physiol 48:587–623

    Google Scholar 

  • Larink O (1976) Entwicklung und Feinstruktur der Schuppen bei Lepismatiden und Machiliden (Insecta, Zygentoma und Archaeognatha). Zool Jb Ant 95:252–293

    Google Scholar 

  • Lee K, Strausfeld N J (1990) Structure, distribution, and number of surface sensilla and their receptor cells on the olfactory appendage of the male moth Manduca sexta. J Neurocytol 19:519–538

    Google Scholar 

  • Levey AI, Wainer BH, Mufson EJ, Mesulam MM (1983) Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 9:9–22

    Google Scholar 

  • Lundberg JM, Hökfelt T, Schulzberg M, Uvnaes-Wallensten K, Köhler C, Laid LI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: Evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Google Scholar 

  • Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond [Biol] 298:309–354

    Google Scholar 

  • McIver SB (1985) Mechanoreception. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 6. Pergamon Press, Oxford, pp 71–132

    Google Scholar 

  • Mesulam M-M, Geula C (1988) Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp Neurol 275:216–240

    Google Scholar 

  • Prescott DJ, Hildebrand JG, Sanes JR, Jewett S (1977) Biochemical and developmental studies of acetylcholine metabolism in the central nervous system of the moth Manduca sexta. Comp Biochem Physiol 56C:77–84

    Google Scholar 

  • Robinson PM (1971) The demonstration of acetylcholinesterase in autonomic axons with the electron microscope. Prog Brain Res 34:357–370

    Google Scholar 

  • Sanes JR, Hildebrand JG (1975) Nerves in the antenna of pupal Manduca sexta Johanssen (Lepidoptera: Sphingidae). W Roux' Archiv 178:71–78

    Google Scholar 

  • Sanes JR, Hildebrand JG (1976a) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51:282–299

    Google Scholar 

  • Sanes JR, Hildebrand JG (1976b) Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300–319

    Google Scholar 

  • Sanes JR, Hildebrand JG (1967c) Acetylcholine and its metabolic enzymes in developing antennae of the moth, Manduca sexta. Dev Biol 52:105–120

    Google Scholar 

  • Sanes JR, Prescott DJ, Hildebrand JG (1977) Cholinergic neurochemical development of normal and deafferented antennal lobes in the brain of the moth, Manduca sexta, during metamorphosis. Brain Res 119:389–402

    Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 8:103–122

    Google Scholar 

  • Schneider D, Kaissling K-E (1957) Ber Bau der Antenne des Seidenspinners Bombyx mori L. II. Sensillen, cuticulare Bildungen und innerer Bau. Zool Jb Abt Ant Ont Tiere 76:223–250

    Google Scholar 

  • Schweitzer ES, Sanes JE, Hildebrand JG (1976) Ontogeny of electroantennogram responses in the moth Manduca sexta. J Insect Physiol 22:955–960

    Google Scholar 

  • Silver A (1974) The biology of cholinesterase. North-Holland, Amsterdam

    Google Scholar 

  • Stenbrecht RA (1984) Arthropoda: chemo-, thermo-, and hygroreceptors. In: Bereiter-Hahn J, Matoltsy A, Richards KS (eds) Biology of the integument, vol 1. Springer, Berlin, pp 523–553

    Google Scholar 

  • Steinbrecht RA, Kittmann R (1986) Funktionelle Morphologie eines elektrophysiologisch identifizerten Hygrorezeptors beim Seidenspinner, Bombyx mori. Verh Dtsch Zool Ges 79:111

    Google Scholar 

  • Tago H, Kimura H, Maeda T (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem 34:1431–1438

    Google Scholar 

  • Tichy H (1979) Hygro- and thermoreceptive triad in antennal sensillum of the stick insect, Carausius morosus. J Comp Physiol 132:149–152

    Google Scholar 

  • Tolbert LP, Matsumoto SG, Hilbebrand JG (1983) Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158–1175

    Google Scholar 

  • Toutant J-P (1989) Insect acetylcholinesterase: catalytic properties, tissues distribution and molecular forms. Prog Neurobiol 32:423–446

    Google Scholar 

  • Vande Berg J (1971) Fine structural studies of Johnston's organ in the tobacco hornworm moth, Manduca sexta (Johannson). J Morphol 133:439–456

    Google Scholar 

  • Waldow U (1970) Elektrophysiologische Untersuchungen an Feuchte-, Trocken- und Kälterezeptoren auf der Antenne der Wanderheuschrecke Locusta. Z Vergl Physiol 69:249–283

    Google Scholar 

  • Waldrop B, Hildebrand JG (1989) Physiology and pharmacology of acetylcholinergic responses of interneurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 164:433–441

    Google Scholar 

  • Wallace B (1981) Distribution of AChE in cholinergic and noncholinergic neurons. Brain Res 219:190–195

    Google Scholar 

  • Wallace B, Gillon JW (1982) Characterization of acetylcholinesterase in individual neurons in the leech central nervous system. J Neurosci 2:1106–1118

    Google Scholar 

  • Yokohari F (1981) The sensillum capitulum, an antennal hygro- and thermoreceptive sensillum of the cockroach Periplaneta americana L. Cell Tissue Res 216:525–543

    Google Scholar 

  • Yokohari F, Tateda H (1976) Moist and dry hygroreceptors for relative humidity of the cockroach, Periplaneta americana L. J Comp Physiol 106:137–152

    Google Scholar 

  • Zacharuk RY (1985) Antennae and sensilla. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 6. Pergamon, Oxford, pp 1–69

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stengl, M., Homberg, U. & Hildebrand, J.G. Acetylcholinesterase activity in antennal receptor neurons of the sphinx moth Manduca sexta . Cell Tissue Res 262, 245–252 (1990). https://doi.org/10.1007/BF00309879

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00309879

Key words

Navigation