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Sensory innervation of the spiracular muscle in the tsetse fly (Glossina morsitans) and the larva of the waxmoth (Galleria mellonella)
J. Insect Physiol., 1966, Vol. 12, pp. 1451 to 1454. Pwgamon Press Ltd.
Printed in Great Britain
SENSORY INNERVATION OF THE SPIRACULAR MUSCLE IN THE TSETSE FLY (GLOSSINA &fORSITANS) AND THE LARVA OF THE WAXMOTH
GALLERIA
MELLONELLA)
L. H. FINLAYSON Department of Zoology and Comparative Physiology, University of Birmingham (R&wed
28 Muy 1966)
Abstract-In the tsetse fly a multipolar neurone situated in the vicinity of the spiracle sends one of its processes to the spiracular muscle. In the larva of the waxmoth a multipolar neurone lies in a similar position. INTRODUCTION
A NUMBER of authors have discussed the possibility
of a receptor sensitive to carbon dioxide and oxygen being situated in the vicinity of the spiracle in insects (e.g. CASE, 1956; BECKEL, 1958; BUCK, 1962). BECKEL and SCHNEIDERMAN(1957) showed, by extreme surgical techniques, that the totally denervated spiracular muscle of Hyalophora cemopia, or even a few fibres remaining after the bulk of the muscle had been dissected away, would respond directly to carbon dioxide and oxygen. However, in Hyalophora, as in all insects, the spiracular muscle is normally innervated and it is generally assumed that it is under the influence of the central nervous system. SCHNEIDERMAN(1956) made the observation that the denervated spiracular muscle is less responsive to carbon dioxide or oxygen than the innervated muscle. He also made the suggestion, based on experimental evidence, that there were separate receptors for carbon dioxide and oxygen. No such receptors have been identified, but Whitten postulated that one of the lateral group of peripheral neurones in cyclorrhaphorous larvae (WHITTEN, 1963 ; OSBORNE, 1963 ; FINLAYSON, 1966) might be a carbon dioxide receptor. This neurone sends a process to the spiracular trachea which in the larva is not respiratory in function. RESULTS
Methylene blue preparations of adult tsetse flies showed several neurones in the vicinity of the spiracle (FINLAYSON, 1966) and closer study revealed that one of them (Figs. l-5) sends a process to the spiracular muscle. The cell body of this neurone lies in the main segmental nerve that runs to the dorsal body wall passing through the cluster of tracheae near their origin in the spiracular atrium. A homologous neurone has been identified at every spiracle of the abdomen (the thoracic spiracles were not investigated in this study). The precise position of the cell 1451
14.52
L. H. FINLAYSON
body varies from segment to segment. As Figs. 1 and 2 show, the cell body tends to lie nearer to the spiracular muscle in the more posterior segments. At least four processes emerge from the cell body (Fig. 1). Two processes run towards the central nervous system; one is presumably the axon. One or possibly two processes continue in the main nerve to an unknown destination, and one process runs in the spiracular nerve to the spiracular muscle, At the end of the spiracular nerve there are one or two terminations, each consisting of a tangle of fine nerve processes (Figs. 1, 2). In addition, there are one or more processes running along
FIG. 1. Innervation of spiracular muscle of right side of third abdominal segment of Glossina adult by two nerve processes coming from the direction of the central nervous system and one process from the spiracular neurone. The closer bow of the spiracle is shown as a broken line below the muscle.
FIG. 2. A-Sixth
Spiracular neurone and innervation of spiracular muscle in Gloss&a adult. abdominal segment, right side. B-Second abdominal segment, right side.
THESPIRACULAR MUSCLEOF TSETSE FLY ANDWAXMOTHLARVA
1453
the muscle. At some spiracles (Fig. 2) there is a ramifying process that passes beyond the spiracular muscle to innervate other muscles nearby. In the waxmoth larva (Fig. 6) less detail has been observed so far but a neurone lies in the same position relative to the spiracle and it seems likely that it also innervates the spiracular muscle. DISCUSSION
Up to date the only function that has been demonstrated by experimental methods for neurones of the type described in this paper is mechanoreception (FINLAYSON and LOWENSTEIN, 1958; LOWENSTEIN and FINLAYSON, 1960) and it is possible that the spiracular neurone is also a mechanoreceptor. The neurone that innervates the spiracular trachea of the larva, and which WHITTEN (1963) suggests may be a gas receptor, may be the same cell as the spiracular neurone, but as there are other neurones nearby it is not yet certain that they are the same cell. As in many peripheral multipolar neurones (OSBORNE, 1963; WHITTEN, 1963; FINLAYSON, 1966) the processes of the spiracular neurone run in different directions and must innervate different structures. It is becoming increasingly obvious that sensory neurones of this type in insects must be capable of transmitting separately to the central nervous system information received from different dendrites, otherwise their morphology and topography would be inexplicable. HUGHES (1965) postulated a similar necessity of functional subdivision of interneurones in the central nervous system of insects and OSBORNE (personal communication) has obtained evidence from electron microscopy that supports HUGHES’S (1965) hypothesis. Acknowledgements-1 am grateful to Dr. R. J. PHELPSand Miss ROSEMARYELLIS of the Agricultural Research Council of Central Africa for kindly sending tsetse puparia from Rhodesia.
REFERENCES BECKELW. E. (1958) The morphology, histology and physiology of the spiracular regulatory apparatus of Hyalophora cecropia (L.) (Lepidoptera). Proc. 10th int. Congr. Ent. 2, 87-115. BECKELW. E. and SCHNEIDERMAN H. A. (1957) The insect spiracle as an independent effector. Science, N.Y. 126, 352-353. BUCK J. (1962) Some physical aspects of insect respiration. A. Rev. Ent. 7, 27-56. CASEJ. F. (1956) Carbon dioxide and oxygen effects on the spiracles of flies. Pkysiol. Ziiol. 29, 163-171. FINLAYSONL. H. (1966) In preparation. FINLAYSONL. H. and LOWENSTEIN0. E. (1958) The structure and function of abdominal stretch receptors in insects. Proc. R. Sot. (B) 148, 433-449. HUGHESG. M. (1965) Neuronal pathways in the insect central nervous system. In The Physiology of the Insect Central Nervous System. pp. 79-l 12. Academic Press, London. LOWENSTEIN0. E. and FINLAYSONL. H. (1960) The response of the abdominal stretch receptor of an insect to phasic stimulation. Comp. Biochem. Physiol. 1, 55-61.
1454
L. H. FINLAYSON
OSBORNE M. P. (1963) The sensory neurones and sensilla in the abdomen and thorax of the
blowfly larva.
Quart. J. micr. Sci. 104, 227-241. Spiracular control of discontinuous respiration in insects. Nature, Lond. 177, 1169-l 171. WHITTEN J. M. (1963) Observations on the cyclorrhaphan larval peripheral nervous system: muscle and tracheal receptor organs and independent peripheral Type II neurons associated with the lateral segmental nerves. Ann. ent. Sot. Am. 56, 755-763. SCHNEIDERMAN H. A. (1956)
Printed in Great Britain
SENSORY INNERVATION OF THE SPIRACULAR MUSCLE IN THE TSETSE FLY (GLOSSINA &fORSITANS) AND THE LARVA OF THE WAXMOTH
GALLERIA
MELLONELLA)
L. H. FINLAYSON Department of Zoology and Comparative Physiology, University of Birmingham (R&wed
28 Muy 1966)
Abstract-In the tsetse fly a multipolar neurone situated in the vicinity of the spiracle sends one of its processes to the spiracular muscle. In the larva of the waxmoth a multipolar neurone lies in a similar position. INTRODUCTION
A NUMBER of authors have discussed the possibility
of a receptor sensitive to carbon dioxide and oxygen being situated in the vicinity of the spiracle in insects (e.g. CASE, 1956; BECKEL, 1958; BUCK, 1962). BECKEL and SCHNEIDERMAN(1957) showed, by extreme surgical techniques, that the totally denervated spiracular muscle of Hyalophora cemopia, or even a few fibres remaining after the bulk of the muscle had been dissected away, would respond directly to carbon dioxide and oxygen. However, in Hyalophora, as in all insects, the spiracular muscle is normally innervated and it is generally assumed that it is under the influence of the central nervous system. SCHNEIDERMAN(1956) made the observation that the denervated spiracular muscle is less responsive to carbon dioxide or oxygen than the innervated muscle. He also made the suggestion, based on experimental evidence, that there were separate receptors for carbon dioxide and oxygen. No such receptors have been identified, but Whitten postulated that one of the lateral group of peripheral neurones in cyclorrhaphorous larvae (WHITTEN, 1963 ; OSBORNE, 1963 ; FINLAYSON, 1966) might be a carbon dioxide receptor. This neurone sends a process to the spiracular trachea which in the larva is not respiratory in function. RESULTS
Methylene blue preparations of adult tsetse flies showed several neurones in the vicinity of the spiracle (FINLAYSON, 1966) and closer study revealed that one of them (Figs. l-5) sends a process to the spiracular muscle. The cell body of this neurone lies in the main segmental nerve that runs to the dorsal body wall passing through the cluster of tracheae near their origin in the spiracular atrium. A homologous neurone has been identified at every spiracle of the abdomen (the thoracic spiracles were not investigated in this study). The precise position of the cell 1451
14.52
L. H. FINLAYSON
body varies from segment to segment. As Figs. 1 and 2 show, the cell body tends to lie nearer to the spiracular muscle in the more posterior segments. At least four processes emerge from the cell body (Fig. 1). Two processes run towards the central nervous system; one is presumably the axon. One or possibly two processes continue in the main nerve to an unknown destination, and one process runs in the spiracular nerve to the spiracular muscle, At the end of the spiracular nerve there are one or two terminations, each consisting of a tangle of fine nerve processes (Figs. 1, 2). In addition, there are one or more processes running along
FIG. 1. Innervation of spiracular muscle of right side of third abdominal segment of Glossina adult by two nerve processes coming from the direction of the central nervous system and one process from the spiracular neurone. The closer bow of the spiracle is shown as a broken line below the muscle.
FIG. 2. A-Sixth
Spiracular neurone and innervation of spiracular muscle in Gloss&a adult. abdominal segment, right side. B-Second abdominal segment, right side.
THESPIRACULAR MUSCLEOF TSETSE FLY ANDWAXMOTHLARVA
1453
the muscle. At some spiracles (Fig. 2) there is a ramifying process that passes beyond the spiracular muscle to innervate other muscles nearby. In the waxmoth larva (Fig. 6) less detail has been observed so far but a neurone lies in the same position relative to the spiracle and it seems likely that it also innervates the spiracular muscle. DISCUSSION
Up to date the only function that has been demonstrated by experimental methods for neurones of the type described in this paper is mechanoreception (FINLAYSON and LOWENSTEIN, 1958; LOWENSTEIN and FINLAYSON, 1960) and it is possible that the spiracular neurone is also a mechanoreceptor. The neurone that innervates the spiracular trachea of the larva, and which WHITTEN (1963) suggests may be a gas receptor, may be the same cell as the spiracular neurone, but as there are other neurones nearby it is not yet certain that they are the same cell. As in many peripheral multipolar neurones (OSBORNE, 1963; WHITTEN, 1963; FINLAYSON, 1966) the processes of the spiracular neurone run in different directions and must innervate different structures. It is becoming increasingly obvious that sensory neurones of this type in insects must be capable of transmitting separately to the central nervous system information received from different dendrites, otherwise their morphology and topography would be inexplicable. HUGHES (1965) postulated a similar necessity of functional subdivision of interneurones in the central nervous system of insects and OSBORNE (personal communication) has obtained evidence from electron microscopy that supports HUGHES’S (1965) hypothesis. Acknowledgements-1 am grateful to Dr. R. J. PHELPSand Miss ROSEMARYELLIS of the Agricultural Research Council of Central Africa for kindly sending tsetse puparia from Rhodesia.
REFERENCES BECKELW. E. (1958) The morphology, histology and physiology of the spiracular regulatory apparatus of Hyalophora cecropia (L.) (Lepidoptera). Proc. 10th int. Congr. Ent. 2, 87-115. BECKELW. E. and SCHNEIDERMAN H. A. (1957) The insect spiracle as an independent effector. Science, N.Y. 126, 352-353. BUCK J. (1962) Some physical aspects of insect respiration. A. Rev. Ent. 7, 27-56. CASEJ. F. (1956) Carbon dioxide and oxygen effects on the spiracles of flies. Pkysiol. Ziiol. 29, 163-171. FINLAYSONL. H. (1966) In preparation. FINLAYSONL. H. and LOWENSTEIN0. E. (1958) The structure and function of abdominal stretch receptors in insects. Proc. R. Sot. (B) 148, 433-449. HUGHESG. M. (1965) Neuronal pathways in the insect central nervous system. In The Physiology of the Insect Central Nervous System. pp. 79-l 12. Academic Press, London. LOWENSTEIN0. E. and FINLAYSONL. H. (1960) The response of the abdominal stretch receptor of an insect to phasic stimulation. Comp. Biochem. Physiol. 1, 55-61.
1454
L. H. FINLAYSON
OSBORNE M. P. (1963) The sensory neurones and sensilla in the abdomen and thorax of the
blowfly larva.
Quart. J. micr. Sci. 104, 227-241. Spiracular control of discontinuous respiration in insects. Nature, Lond. 177, 1169-l 171. WHITTEN J. M. (1963) Observations on the cyclorrhaphan larval peripheral nervous system: muscle and tracheal receptor organs and independent peripheral Type II neurons associated with the lateral segmental nerves. Ann. ent. Sot. Am. 56, 755-763. SCHNEIDERMAN H. A. (1956)