Skip to main content
Log in

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

  • Original Article
  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Abstract

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Altrup U, Peters M (1982) Procedure of intracellular staining of neurons in the snail Helix pomatia. J. Neurosci Methods 5: 161–165

    Google Scholar 

  • Anderson H (1988) Drosophila adhesion molecules and neural development. Trends Neurosci 11 (11):472–475

    Google Scholar 

  • Ball E, Young D (1974) Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker). II. Postembryonic development. Z Zellforsch Microsk Anat 147:313–325

    Google Scholar 

  • Ball EE, Oldfield B, Michel RK (1989) Auditory organ structure, development, and function. In: Huber F, Moore TE, Loher W (eds) Cricket behavior and neurobiology. Cornell University Press, Ithaca London, pp 391–422

    Google Scholar 

  • Bate CM (1976) Pioneer neurons in an insect embryo. Nature 260:54–56

    Google Scholar 

  • Bentley D, Caudy M (1983a) Navigational substrates for peripheral pioneer growth cones: Limb — axis cues, limb segment boundaries, and guidepost neurons. Cold Spring Harbor, Symp Quant Biol 48:573–585

    Google Scholar 

  • Bentley D, Candy M (1983b) Pioneer axons lose directed growth after selective killing of guidepost cells. Nature 304:62–65

    Google Scholar 

  • Bentley D, Keshishian H (1982a) Pathfinding by peripheral pioneer neurons in grasshoppers. Science 218:1082–1088

    Google Scholar 

  • Bentley D, Keshishian H (1982b) Pioneer neurons and pathways in insect appendages. Trends Neurosci 5:354–358

    Google Scholar 

  • Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47–74

    Google Scholar 

  • Berlot J, Goodman CS (1984) Guidance of peripheral pioneer neurons in the grasshopper: adhesive hierarchy of epthelial and neuronal surfaces. Science 223:493–496

    Google Scholar 

  • Bock C (1978) A quick and simple method for preparing soft insect tissues for scanning electron microscopy using carnoy and hexamethyldisilazane. Beitr Elektronenmikroskop Direktabb Oberfl 20:209–214

    Google Scholar 

  • Burns MD (1974) Structure and physiology of the locust femoral organ. J Insect Physiol 20:1319–1339

    Google Scholar 

  • Campbell JI (1961) The anatomy of the nervous system of the mesothorax of Locusta migratoria migratorioides R. & F. Proc Zool Soc London 137:403–432

    Google Scholar 

  • Caudy M, Bentley D (1986) Proximal growth cone morphologies reveal proximal increases in substrate affinity within leg segments of grasshopper embryos. J Neurosci 6 (2):364–379

    Google Scholar 

  • Condic ML, Lefcort F, Bentley D (1989) Selective recognition between embryonic afferent neurons of grasshopper appendages in vitro. Dev Biol 135:221–230

    Google Scholar 

  • Dambach M (1989) Vibrational responses. In: Huber F, Moore TE, Loher W (eds) Cricket behavior and neurobiology. Cornell University Press, Ithaca London, pp 178–197

    Google Scholar 

  • Debaisieux P (1938) Organes scolopidiaux des pattes d'insectes. II. Cellule, 47:79–202

    Google Scholar 

  • Edwards JS, Chen S-W, Berns MW (1981) Cercal sensory development following laser microlesions of embryonic apical cells in Acheta domesticus. J Neurosci 1 (3):250–258

    Google Scholar 

  • Eggers F (1928) Die stiftführenden Sinnesorgane der Orthopteren: Morphologie und Physiologie der chordotonalen und tympanalen Sinnesapparate der Insekten. In: Zoologische Bausteine, vol 2. Verlag Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Eibl E (1978) Morphology of the sense organs in the proximal parts of the tibiae of Gryllus campestris L. and Gryllus bimaculatus DeGeer (Insecta, Ensifera). Zoomorphology 89:85–205

    Google Scholar 

  • Eibl E, Huber F (1979) Central projections of tibial sensory fibres within the three thoracic ganglia of crickets (Gryllus campestris L., Gryllus bimaculatus De Geer). Zoomorphologie 92:1–17

    Google Scholar 

  • Eisen J (1981) Growth cone guidance and pathway formation. Trends Neurosci 11 (8):333–335

    Google Scholar 

  • Friedmann MH (1972a) A light and electron microscopic study of sensory organs and associated structures in the foreleg tibia of the cricket Gryllus assimilis. J Morphol 138:263–328

    Google Scholar 

  • Friedmann MH (1972b)An electron microscopic study of the tympanal organ and associated structures in the foreleg tibia of the cricket Gryllus assimilis. J Morphol 138:329–348

    Google Scholar 

  • Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77–98

    Google Scholar 

  • Goodman CS, Bastiani MJ, Doe CQ, duLac S, Helfand SL, Kuwada JY, Thomas JB (1984) Cell recognition during neuronal development. Science 225:1271–1279

    Google Scholar 

  • Graber V (1876) Die tympanalen Sinnesapparate der Orthopteren. Denkschr Akad Wien Math — Naturwiss Cl 36 (II):1–140

    Google Scholar 

  • Heitler WJ, Burrows M (1977a) The locust jump. I. Motor programme. J Exp Biol 66:203–219

    Google Scholar 

  • Heitler WJ, Burrows M (1977b) The locust jump. II. Neural circuits of the motor programme. J Exp Biol 66:221–241

    Google Scholar 

  • Ho RK, Goodman CS (1982) Peripheral pathways are pioneered by an array of central and peripheral neurons in grasshopper embryos. Nature 297:404–406

    Google Scholar 

  • Jan LY, Jan NJ (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl Acad Sci USA 79:2700–2704

    Google Scholar 

  • Kennedy TE, Serafini T, Torre JR de la, Tessier-Lavigne M (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78:425–435

    Google Scholar 

  • Keshishian H (1980) The origin and morphogenesis of pioneer neurons in the grasshopper metathoracic leg. Dev Biol 80: 388–397

    Google Scholar 

  • Keshishian H, Bentley D (1983a) Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway to the CNS. Dev Biol 96:89–102

    Google Scholar 

  • Keshishian H, Bentley D (1983b) Embryogenesis of peripheral nerve pathways in grasshopper legs. III. Development without pioneer neurons. Dev Biol 96:116–124

    Google Scholar 

  • Klose M, Bentley D (1989) Transient pioneer neurons are essential for formation of an embryonic peripheral nerve. Science 245:982–984

    Google Scholar 

  • Kolodkin AL, Matthes DJ, O'Connor TP, Patel NH, Admon A, Bentley D, Goodman CS (1992) Fasciclin IV: Sequence, expression, and function during growth cone guidance in the grasshopper embryo. Neuron 9:831–845

    Google Scholar 

  • Kutsch W (1989) Formation of the receptor system in the hind limb of the locust embryo. Roux's Arch Dev Biol 198:39–47

    Google Scholar 

  • Kutsch W, Bentley D (1987) Programmed death of peripheral pioneer neurons in the grasshopper embryo. Dev Biol 123: 517–525

    Google Scholar 

  • Kuwada J (1986) Cell recognition by neuronal growth cones in a simple vertebrate embryo. Science 233:740–746

    Google Scholar 

  • Lamborghini JE (1987) Disappearance of Rohon-Beard neurons from the spinal cord of larval Xenopus laevis. J Comp Neurol 264:47–55

    Google Scholar 

  • McConnell SK, Ghosh A, Shatz CJ (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:978–982

    Google Scholar 

  • Meier T, Reichert H (1990) Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21 (4):592–610

    Google Scholar 

  • Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus DeGeer (Saltatoria, Gryllidae). Z Morphol Oekol Tiere 77:285

    Google Scholar 

  • Moulins M (1976) Ultrastructure of chordotonal organs. In: Mill PJ (ed) Structure and function in the invertebrates. John Wiley and Sons, New York

  • Purves D (1986) The trophic theory of neural connections. Trends Neurosci 9:486–489

    Google Scholar 

  • Purves D, Lichtman JW (1985) Principles of neuronal development. Sinauer Associates, Sunderland

    Google Scholar 

  • Rohrer H (1990) The role of growth factors in the control of neurogenesis. Eur J Neurosci 2:1005–1015

    Google Scholar 

  • Rosenbauer KA, Kegel BH (1978) Rasterelektronenmikroskopische Technik. Georg Thieme, Stuttgart

    Google Scholar 

  • Schwabe J (1906) Beiträge zur Morphologie und Histologie der tympanalen Sinnesapparate der Orthopteren. Zoologica (Stuttgart) 20:1–154

    Google Scholar 

  • Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans. UNC-6. Cell 78:409–424

    Google Scholar 

  • Taghert PH, Bastiani MJ, Ho RK, Goodman CS (1982) Guidance of pioneer growth cones: Filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev Biol 94: 391–399

    Google Scholar 

  • Theophilidis G (1986) The femoral chordotonal organs of Decticus albiforans. II. Function. Comp Biochem Physiol A 84 (3):537–543

    Google Scholar 

  • Usherwood PNR, Runion HJ, Campbell JI (1968) Structure and physiology of a chordotonal organ in the locust leg. J Exp Biol 48:305–323

    Google Scholar 

  • Young D (1970) The structure and function of a connective chordotonal organ in the cockroach leg. Philos Trans R Soc London B 256:401–426

    Google Scholar 

  • Young D, Ball E (1974a) Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker). 1. Adult structure. Z Zellforsch Microsk Anat 147:293–312

    Google Scholar 

  • Young D, Ball E (1974b) Structure and development of the tracheal organ in the mesothoracic leg of the cricket Teleogryllus commodus (Walker). Z Zellforsch Microsk Anat 147:325–334

    Google Scholar 

  • Zill N (1985) Plasticity and proprioception in insects. I. Responses and cellular properties of individual receptors of the locust metathoracic femoral chordotonal organ. J Exp Biol 116: 435–461

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klose, M. Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker). Roux's Arch Dev Biol 205, 344–355 (1996). https://doi.org/10.1007/BF00377214

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00377214

Key words

Navigation