Abstract
An antiserum raised against the peptide, culetachykinin II, immunocytochemically detected a group of neurosecretory cells in the first flagellar segment of the antennae of both males and females of the mosquito, Culex salinarius. This is the first insect species in which neurosecretory cells have been found in the antennae. The ultrastructure of these antennal neurosecretory cells (ANC) is described, as well as their relationship to other neurons in the antennae and antennal lobe of the mosquito. These tachykinin-reactive cells contain relatively small (140–220 nm) elementary neurosecretory granules. Not only do the ANC have axons that terminate on specific glomeruli of the deutocerebrum, but these neurons also have collaterals that form neurohemal terminals in the receptor lymph channels of the dendrites of the sensory neurons. Thus, the ANC not only influence higher centers of the brain that interpret signals from the antennal sensillae, but also modulate the response of the sensory receptors. To our knowledge, this is the first report of neurosecretory cells directly affecting the signal reception of sensory neurons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abernathy R. L., Teal P. E., Meredith J. A., and Nachman R. J. (1966) Induction of pheromone production in a moth by topical application of a pseudopeptide mimic of a pheromonotropic neuropeptide. Proc. Natl. Acad. Sci. USA 93, 12,621–12,625.
Axel R. (1995) The molecular logic of smell. Sci. Amer. 273, 154–159.
Blackburn M. B., Kingan T. C., Raina A. K., and Ma M. C. (1992) Colocalization and differential expression of PBAN-and FMRFamide-like immunoreactivity in the subesophageal ganglion of Helicoverpa zea (Lepidoptera:Noctuidae) during development. Arch. Insect Biochem. Physiol. 21, 225–238.
Bowen M. F. (1991) The sensory physiology of hostseeking behavior in mosquitoes. Ann. Rev. Entomol. 36, 139–158.
Hildebrand J. G. and Sheperd G. M. (1997) Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Ann. Rev. Neurosci. 20, 595–631.
Humason G. L. (1962) Animal Tissue Techniques. W. H. Freeman, San Francisco, CA.
Jones J. C. (1977) The Circulatory System of Insects. Charles C. Thomas, Springfield, IL.
Kalt M. R. and Tandler B. (1971) A study of fixation of early amphibian embryos for electron microscopy. J. Ultrastruct. Res. 36, 633.
Keil T. A. and Steinbrecht R. A. (1994) Mechanosensitive and olfactory sensilla of insects, in Insect Ultrastructure, vol. 2 (King, R. and Akai, H., eds.), Plenum, New York, pp. 477–516.
Lundquist C. T., Clottens F. L., Holman G. M., Riehm J. P., Bonkale W., and Nassel D. R. (1994) Locustatachykinin immunoreactivity in the blowfly central nervous system and intestine. J. Comp. Neurol. 341, 225–240.
Maggio J. E. (1988) Tachykinins. Ann. Rev. Neurosci. 11, 13–28.
McIver S. B. (1982) Sensilla of mosquitoes (Diptera:Culicidae). J. Med. Entomol. 19, 489–535.
Meola S. M., Wright M. S., Holman G. M., and Thompson J. M. (1991) Localization of leucomyosuppressin-like peptides in the central nervous system of the stable fly with immunocytochemistry. J. Med. Entomol. 28, 712–718.
Meola S. M., Clottens F. L., Holman G. M., Nachman R. J., Nichols R., Schoofs L., et al. (1998) Isolation and immunocytochemical characterization of three tachykinin-related peptides from the mosquito, Culex salinarius. Neurochem. Res. 22, 189–202.
Mollenhauser H. H. (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol. 39, 111.
Nassel D. R. (1999) Tachykinin-related peptides in invertebrates: a review. Peptides 20, 141–158.
Reynolds E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208.
Rosay P., Colas J. F., and Maroteaux L. (1995) Dual organization of the Drosophila neuropeptide receptor NKD gene promoter. Mech. Dev. 51, 329–339.
Schoonveld H. (1991) Peptidergic nerve cells deliver multiple messengers for optimizing neuroendocrine coordination in the Colorado potato beetle. Proc. Exper. Appl. Entomol. N.E.V. Amsterdam. 2, 86–91.
Todd J. L. and Baker T. C. (1997) The cutting edge of insect olfaction. Am. Entomol. 43, 174–182.
Tveten M. S. and Meola R. M. (1988) Autogeny in Culex salinarius from Texas, Florida and New Jersey. J Amer. Mosquito Cont. Assoc. 4, 436–441.
Vassar R., Chao S. K., Sitcheran R., Nunez J. M., and Vosshall L. B. (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981–991.
Zacharuk R. Y. (1985) Antennae and sensilla, in Comprehensive Insect Physiology Biochemistry and Pharmacology (Kerkut, G. A. and Gilbert, L. L., eds.), Pergamon, Oxford, UK, pp. 1–69.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Meola, S.M., Sittertz-Bhatkar, H., Pendleton, M.W. et al. Ultrastructural analysis of neurosecretory cells in the antennae of the mosquito, Culex salinarius (Diptera: Culicidae). J Mol Neurosci 14, 17–25 (2000). https://doi.org/10.1385/JMN:14:1-2:017
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1385/JMN:14:1-2:017