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The development of GABA-like immunoreactivity in the thoracic ganglia of the locust Schistocerca gregaria

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Summary

The development of GABA-like immunoreactivity was investigated in embryonic and juvenile locusts using an antibody raised against GABA-protein conjugates. GABA-like immunoreactivity was first detectable in the neuropile of embryonic ganglia at 55% development, and in neuronal somata at 62% development. The total number of immunoreactive somata increased between 62% and 85% embryonic development, and followed an anterio-posterior pattern of expression. At 85% development, the number of immunoreactive somata reached adult levels and no change in number was then seen. In embryonic stages and first and second juvenile instars two dorsal and four ventral groups of somata were labeled in all three thoracic ganglia, whilst in later juvenile instars one of the dorsal groups was visible as a separate entity only in the metathoracic ganglion. These early patterns were modified by alterations in the positions of some of the groups during late embryogenesis and during juvenile development to produce the adult pattern. The results show that the development of GABA expression is similar to that of other neurotransmitters. The characteristics of the development of immunoreactivity indicate that some of these immunoreactive clusters may be derived from clonally related neurones. Finally, we demonstrate the presence of immunoreactive somata and processes in embryos, which correspond to those of identified local and intersegmental interneurones studied in the adult.

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Abbreviations

Ab1–3 :

first-third abdominal ganglion

CON :

connective

CI 1–3 :

common inhibitors 1–3

CTC :

tract

DC I–VII :

dorsal commissures I–VII

DIT :

dorsal intermediate tract

DMT :

dorsal median tract

LDT :

lateral dorsal tract

LF :

lateral fibres

o, iLVT :

outer and inner lateral ventral tract

MVT :

median ventral tract

N1–5 :

nerves 1–5

aPT :

anterior perpendicular tract

PT :

perpendicular tract

aRT :

anterior ring tract

R1–5 :

nerve roots 1–5

PVC :

posterior ventral commissure

SMC :

supra-median commissure

T3 :

metathoracic neuromere

TT :

T tract

aVAC :

anterior ventral association centre

VC I :

ventral commissure I

d,vVCII :

dorsal and ventral parts of ventral commissure II

VF :

ventral fibres

VIT :

ventral intermediate tract

VLT :

ventral lateral tract

VMT :

ventral median tract

(d,v)LAG :

(dorsal and ventral) lateral anterior group

LDG :

lateral dorsal group

LVG :

lateral ventral group

MDG :

medial dorsal group

MPG :

medial posterior group

MVG :

medial ventral group

References

  • Baden V (1936) Embryology of the nervous system in the grasshopper, Melanoplus differentialis. J Morphol 60:159–190

    Google Scholar 

  • Bate CM, Grunewald EB (1980) Embryogenesis of an insect nervous system. II. A second class of neuronal precursor cells and the origin of the intersegmental connectives. J Embryol Exp Morphol 61:317–330

    Google Scholar 

  • Bate M, Goodman CS, Spitzer NC (1981) Embryonic development of identified neurons: Segment-specific differences in the H cell homologues. J Neurosci 1:103–106

    Google Scholar 

  • Bentley D, Toroian-Raymond A (1981) Embryonic and postembryonic morphogenesis of a grasshopper interneuron. J Comp Neurol 201:507–518

    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 61:47–74

    Google Scholar 

  • Burrows M, Siegler MVS (1982) Spiking local interneurons mediate local reflexes. Science 217:650–652

    Google Scholar 

  • Coulombe J, Bronner-Fraser M (1986) Choline acetyltransferase immunoreactivity in embryonic neurons of the quail ciliary ganglion. Soc Neurosci Abstr 12:1008

    Google Scholar 

  • Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. 1. Developmental and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205

    Google Scholar 

  • Emson PC, Burrows M, Fonnum F (1974) Levels of glutamate decarboxylase, choline acetyl transferase and acetylcholine esterase in identified motor neurones of the locust. J Neurobiol 5:33–42

    Google Scholar 

  • Goodman CS (1982) Embryonic development of identified neurons in the grasshopper. In: Spitzer NC (ed) Neuronal Development. Plenum Press, London, pp 171–212

    Google Scholar 

  • Goodman CS, Spitzer NC (1979) Embryonic development of identified neurones: Differentiation from neuroblast to neurone. Nature 280:208–214

    Google Scholar 

  • Goodman CS, Spitzer NC (1980) Embryonic development of neurotransmitter receptors in grasshoppers. In: Satelle DB (ed) Receptors for Neurotransmitters, Hormones and Pheromones in Insects. Elsevier, North Holland, pp 195–207

  • Goodman CS, Spitzer NC (1981a) The mature electrical properties of identified neurones in grasshopper embryos. J Physiol 313:369–384

    Google Scholar 

  • Goodman CS, Spitzer NC (1981b) The development of electrical properties of identified neurones in grasshopper embryos. J Physiol 313:385–403

    Google Scholar 

  • Goodman CS, O'Shea M, McCaman R, Spitzer NC (1979) Embryonic development of identified neurons: Temporal pattern of morphological and biochemical differentiation. Science 204:1219–1222

    Google Scholar 

  • Goodman CS, Bate M, Spitzer NC (1981) Embryonic development of identified neurons: origin and transformation of the H cell. J Neurosci 1:94–102

    Google Scholar 

  • Kerkut GA, Pitman RM, Walker RJ (1969a) Iontophoretic application of acetylcholine and GABA onto insect central neurones. Comp Biochem Physiol 31:611–633

    Google Scholar 

  • Kerkut GA, Pitman RM, Walker RJ (1969b) Sensitivity of neurones in the insect central nervous system to iontophoretically applied acetylcholine or GABA. Nature 222:1075–1076

    Google Scholar 

  • Keshishian H, O'Shea M (1985a) the distribution of a peptide neurotransmitter in the postembryonic grasshopper central nervous system. J Neurosci 5:922–1004

    Google Scholar 

  • Kesheshian H, O'Shea M (1985b) The acquisition and expression of a peptidergic phenotype in the grasshopper embryo. J Neurosci 5:1005–1015

    Google Scholar 

  • Laurent G (1987a) Parallel effects of joint receptors on motor neurones and intersegmental interneurones in the locust. J Comp Physiol 160:341–353

    Google Scholar 

  • Laurent G (1987b) The morphology of a population of thoracic intersegmental interneurones in the locust. J Comp Neurol 256:412–429

    Google Scholar 

  • Laurent G, Burrows M, Watson AHD (1987) The role of intersegmental interneurones in the transfer of mechanosensory information between local centres in the locust. Physiol Soc [London], Sept

  • LeDouarin N, Renaud D, Teillet M, LeDouarin G (1975) Cholinergic differentiation of presumptive adrenergic neuroblasts in interspecific chimeras after hetertopic transplantations. Proc Natl Acad Sci USA 72:728–732

    Google Scholar 

  • Patterson PH, Chun LLY (1977) The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurones. Dev Biol 56:263–280

    Google Scholar 

  • Pitman RM, Kerkut GM (1970) Comparison of the actions of iontophoretically applied acetylcholine and gamma aminobutyric acid with the EPSP and IPSP in cockroach central neurones. Comp Gen Pharmacol 1:221–230

    Google Scholar 

  • Segula P, Geffard M, Buijs R, Le Moal M (1984) Antibodies against gamma-aminobutyric acid: specificity studies and immunocytochemical results. Proc Natl Acad Sci USA 81:3888–3892

    Google Scholar 

  • Shankland M (1981) Development of a sensory afferent projection in the grasshopper embryo I. Growth of peripheral pioneer axons within the central nervous system. J Embryol Exp Morphol 64:169–185

    Google Scholar 

  • Shankland M, Goodman CS (1982) Development of the dendritic branching pattern of the medial giant interneuron in the grasshopper embryo. Dev Biol 92:489–506

    Google Scholar 

  • Siegler MVS, Burrows M (1984) The morphology of two groups of spiking local internurons in the metathoracic ganglion of the locust. J Comp Neurol 224:463–482

    Google Scholar 

  • Sternberger LA (1974) Immunocytochemistry. 2nd. edn, Prentice Hall Inc. New Jersey

    Google Scholar 

  • Taghert PH, Goodman CS (1984) Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. J Neurosci 4:989–1000

    Google Scholar 

  • Tyrer NM, Gregory GE (1982) A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Philos Trans R Soc Lond [Biol] 297:91–123

    Google Scholar 

  • Usherwood PNR, Cull-Candy SG (1975) Pharmacology of somatic nerve-muscle synapses. In Usherwood PNR (ed) Insect muscle. Academic Press, London, pp 207–280

    Google Scholar 

  • Usherwood PNR, Grundfest H (1965) Peripheral inhibition in skeletal muscle of insects, J Neurophysiol 28:497–518

    Google Scholar 

  • Watson AHD (1986) The distribution of GABA-like immunoreactivity in the thoracic nervous system of the locust Schistocerca gregaria. Cell Tissue Res 246:331–341

    Google Scholar 

  • Watson AHD, Burrows M (1987) Immunocytochemical and pharmacological evidence for GABAergic spiking local interneurons in the locust. J Neurosci 7:1741–1751

    Google Scholar 

  • Watson AHD, Pflüger H-J (1987) The distribution of GABA-like immunoreactivity in relation to ganglion structure in the abdominal nerve cord of the locust (Schistocerca gregaria). Cell Tissue Res 249:391–402

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Cambridge, Cambridge, UK

    D. A. O'Dell & B. L. Watkins

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  1. D. A. O'Dell
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  2. B. L. Watkins
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O'Dell, D.A., Watkins, B.L. The development of GABA-like immunoreactivity in the thoracic ganglia of the locust Schistocerca gregaria . Cell Tissue Res. 254, 635–646 (1988). https://doi.org/10.1007/BF00226514

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  • DOI: https://doi.org/10.1007/BF00226514

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