Summary
The origin and orientation of the heart nerves in Sphinx ligustri and Ephestia kuehniella were investigated by scanning electron microscopy using a special technique which involved pinning the dissected specimens on a stabilizing metal pad. The heart and alary muscles in Sphinx particularly their caudal extremity were also examined by transmission electron microscopy. The alary muscles form an incomplete sheath around the heart with a mainly longitudinal fibre orientation, e.i. antagonistically to the fibres of the heart itself. The heart and alary muscles are multiterminally innervated by branches of the transverse segmental nerves. All branches contain a single electron lucent axon; the thickest branches also possess several neurosecretory axons. Swellings of the segmental nerves may indicate the position of nerve cell bodies. There are no lateral heart nerves. Only one type of neuromuscular junction is abundant in the alary muscles but less frequently found in the heart. The terminals originate from the central axon only. They are capped by glial cells, which interdigitate with the muscle cells. They penetrate into the T-system toward the Z-discs and form a complex intercellular space system. Exocytosis of dense-cored vesicles into this “perisynaptic reticulum” seems likely. Sites of neurohaemal release are distributed along the nerve branches and special nerve endings occur at the level of the ostia. The possible nervous influence upon heart activity is discussed.
Zusammenfassung
Ursprung und Verlauf der Herznerven bei Sphinx ligustri und Ephestia kuehniella wurden unter Verwendung von Präparationsunterlagen aus Bleiblech rasterelektronenmikroskopisch untersucht. Herz und Alarmuskeln von Sphinx ligustri wurden mit besonderer Berücksichtigung des caudalen Herzabschnitts im Transmissionselektronenmikroskop untersucht. Die Alarmuskeln bilden eine unvollständige Hülle um das Herz aus überwiegend längs orientierten Fasern, antagonistisch zum Faserverlauf im Herzmuskel. Herz und Alarmuskeln sind multiterminal über die transversalen Segmentalnerven innerviert, deren größte Zweige ein elektronentransparentes und mehrere neurosekretorische Axone enthalten. Verdickungen der Segmentalnerven enthalten möglicherweise Nervenzellen. Laterale Herznerven wurden nicht gefunden. Synaptische Axonendigungen nur eines Typs sind in den Alarmuskeln häufig, im Herzmuskel seltener. Sie werden nur von dem zentralen Axon aus gebildet. Die neuromuskulären Kontaktstellen sind von Gliazellen bedeckt, die über zahlreiche Ausläufer mit der Muskelzelle verzahnt sind und mit ihr ein “perisynaptisches Retikulum” bilden. Die Gliazellausläufer dringen in das T-System bis zu den Z-Banden vor. Exozytose von Neurosekret-Vesikeln in das perisynaptische Interzellularsystem wird angenommen. Neurohämale Abgabeorte finden sich entlang der Nervenäste und in speziellen Nervenendigungen auf der Höhe der Ostien. Der mögliche Einfluß der Innervierung auf die Herzaktivität wird diskutiert.
Similar content being viewed by others
References
Adams, M.E., Miller, T., Thomson, W.W.: Fine structure of the alary muscles of the cockroach. J. Insect Physiol. 19, 2199–2207 (1973)
Alexandrowicz, J.S.: The innervation of the heart of the cockroach (Periplaneta orientalis). J. comp. Neurol. 41, 291–309 (1926)
Belton, P.: Innervation and neural excitation of ventral muscle fibres of the larva of the waxmoth, Galleria mellonella. J. Insect Physiol. 15, 731–741 (1969)
Bruen, J.P., Ballard R.C.: An intracellular study of myocardial cells of the flesh fly, Sarcophaga bullata. Comp. Biochem. Physiol. 32, 227–237 (1970)
Carlson, A.J.: The physiology of the cardiac nerves in the arthropods. Amer. J. Physiol. 15, 127–135 (1906)
Couteaux, R.: Motor end plate structure. In: The structure and function of muscle. Vol. II (G.H. Bourne, ed.). New York-London: Academic Press 1973
Edwards, G.A., Challice, C.E.: The ultrastructure of the heart of the cockroach Blatella germanica. Ann. ent. Soc. Amer. 53, 369–383 (1960)
Edwards, G.A., Ruska, H., Harven, E. de: Neuromuscular junctions in flight and tymbal muscles of the cicada. J. biophys. biochem. Cytol. 4, 251–255 (1958)
Gerould, J.H.: Structure and action of the heart of Bombyx mori and other insects. Acta zool. (Stockh.) 19, 297–352 (1938)
Glaser, R.W.: The growth of insect blood cells in vitro. Psyche 24, 1–7 (1917)
Heinrich, B.: Nervous control of the heart during thoracic temperature regulation in a Sphinx moth. Science 169, 606–607 (1970)
Hinks, C.F.: Peripheral neurosecretory cells in some Lepidoptera. Canad. J. Zool. 53, 1035–1038 (1975)
Iaguzhinskaia, L.V.: New investigations on the physiology and anatomy of the heart of diptera (Russian). Byull. Mosk. Obshchest. Ispyt. Prir. Otd. Biol. 59, 41–50 (1954)
Johnson, B.: Fine structure of the lateral cardiac nerves of the cockroach Periplaneta americana (L.) J. Insect Physiol. 12, 645–653 (1966)
Jones, D.G.: Synapses and synaptosomes. Morphological aspects. London: Chapman & Hall 1975
Jones, J.C.: The circulatory system of insects. In: The physiology of insecta. Vol. III (M. Rockstein, ed.). London-New York: Academic Press 1964
Ke, O.: Contributions to the anatomy and physiology of the dorsal vessel of the silkworm. Bull. Sci. Fak. Terk. Kjusu Univ. 5, 1–16 (1932)
Kuwana, F.: Morphological studies of the nervous system of the silkworm, Bombyx mori, L. 1. The innervation of the dorsal vessel. Bull. seric. Exp. Stn. Japan 8, 109–120 (1932)
Maloeuf, N.S.R.: The myogenic automatism of the contraction of the heart of insects. Ann. ent. Soc. Amer. 28, 332–337 (1935)
McCann, F.V.: The effect of intracellular current pulses on membrane potentials in the moth heart. Comp. Biochem. Physiol. 17, 599–608 (1966)
McCann, F.V.: Physiology of insect hearts. Ann. Rev. Ent. 15, 173–200 (1970)
McIndoo, N.E.: Innervation of insect hearts. J. comp. Neurol. 83, 141–155 (1945)
Miller, T.A.: Electrophysiology of the insect heart. In: The physiology of insecta. Vol. V (M. Rockstein, ed.). London-New York: Academic Press 1974
Miller, T.A., Rees, D.: Excitatory transmission in insect neuromuscular systems. Amer. Zool. 13, 299–313 (1973)
Miller, T.A., Thomson, W.W.: Ultrastructure of cockroach cardiac innervation. J. Insect Physiol. 14, 1099–1104 (1968)
Moreau, R., Lavenseau, L.: Rôle des organes pulsatiles thoraciques et du coeur pendant l'émergence et l'expansion des ailes des Lépidoptères. J. Insect Physiol. 21, 1531–1534 (1975)
Normann, T.C.: Heart activity and its control in the adult blowfly, Calliphora erythrocephala. J. Insect Physiol. 18, 1793–1810 (1972)
Normann, T.C.: Calcium dependence of neurosecretion by exocytosis. J. exp. Biol. 61, 401–409 (1974)
Opoczynska-Sembratowa, Z.: Recherches sur l'anatomie et l'innervation du coeur de Carausius morosus Brunner. Bull. Acad. pol. Sci., Sér. B, 2, 411–436 (1936)
Osborne, M.P.: The fine structure of the neuromuscular junctions in the segmental muscles of the blowfly larva. J. Insect Physiol. 13, 827–833 (1967)
Osborne, M.P.: Structure and function of neuromuscular junctions and stretch receptors. In: Insect ultrastructure. Vol. 5 (A.C. Neville, ed.). Oxford: Blackwell 1970
Osborne, M.P.: The ultrastructure of nerve-muscle synapses. In: Insect muscle (P.N.R. Usherwood, ed.). London-New York: Academic Press 1975
Queinnec, Y., Campan, R.: Heart beat frequency variations in the moth Mamestra brassicae during ontogeny. J. Insect Physiol. 18, 1739–1744 (1972)
Rehm, E.: Die Innervation der inneren Organe von Apis mellifica. Z. Morph. Ökol. Tiere 36, 89–122 (1939)
Richter, K.: Struktur und Funktion der Herzen wirbelloser Tiere. Zool. Jb., Allg. Zool. Physiol. 77, 477–668 (1973)
Robertis, E.D.P. de: Ultrastructure and cytology of the synaptic region. Science 156, 907–914 (1967)
Sanger, J.W., McCann, F.V.: Ultrastructure of the myocardium of the moth, Hyalophora cecropia. J. Insect Physiol. 14, 1105–1111 (1968a)
Sanger, J. W., McCann, F.V.: Ultrastructure of the moth alary muscles and their attachement to the heart wall. J. Insect Physiol. 14, 1539–1544 (1968b)
Smith, D.S.: Innervation of the fibrillar flight muscle of an insect: Tenebrio molitor (Coleoptera). J. biophys. biochem. Cytol. 3, 447–466 (1960)
Stocker, R.F., Nüesch, H.: Ultrastructural studies on neuromuscular contacts and the formation of junctions in the flight muscle of Antheraea polyphemus (Lep.) Cell Tiss. Res. 159, 245–266 (1975)
Tenney, S.M.: Observations on the physiology of the lepidopteran heart with special reference to reversal of the beat. Physiologia comp. Oekol. 3, 286–306 (1953)
Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)
Wasserthal, L.T.: Herzschlag-Umkehr bei Insekten und die Entwicklung der imaginalen Herzrhythmik. Verh. Dtsch. Zool. Ges. 1974, 67, 95–99 (1975)
Wasserthal, L.T.: Heartbeat reversal and its coordination with accessory pulsatile organs and abdominal movements in Lepidoptera. Experientia (Basel) 32, 577–578 (1976)
Wigglesworth, V.B.: The principles of insect physiology. London: Chapman & Hall 1972
Wilde, J. de: Contribution to the physiology of the heart of insects, with special reference to the alary muscles. Arch. néerl. Physiol. 28, 530–542 (1948)
Zawarzin, A.: Histologische Studien über Insekten. I. Das Herz der Aeschnalarven. Z. wiss. Zool. 97, 481–510 (1911)
Author information
Authors and Affiliations
Additional information
We wish to thank Mrs. Hotzel for her careful technical assistance, Dr. Foelix and the copy editor for the critical revision of the English manuscript. We are indebted to Dr. Noli, Leitz-AMR Wetzlar and Dr. Bijvank for their help at the scanning electron microscopes
The transmission electron microscopic part of this investigation was supported by a research scholarship from the Deutsche Forschungsgemeinschaft
Rights and permissions
About this article
Cite this article
Wasserthal, L.T., Wasserthal, W. Innervation of heart and alary muscles in Sphinx ligustri L. (Lepidoptera). Cell Tissue Res. 184, 467–486 (1977). https://doi.org/10.1007/BF00220970
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00220970