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The distribution of neurones immunoreactive for β-tyrosine hydroxylase, dopamine and serotonin in the ventral nerve cord of the cricket, Gryllus bimaculatus

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Abstract

The cellular localization of the biogenic amines dopamine and serotonin was investigated in the ventral nerve cord of the cricket, Gryllus bimaculatus, using antisera raised against dopamine, β-tyrosine hydroxylase and serotonin. Dopamine-(n<-70) and serotonin-immunoreactive (n<-120) neurones showed a segmental arrangement in the ventral nerve cord. Some neuromeres, however, did not contain dopamine-immunoreactive cell bodies. The small number of stained cells allowed complete identification of brain and thoracic cells, including intersegmentally projecting axons and terminal arborizations. Dopamine-like immunostaining was found primarily in plurisegmental interneurones with axons descending to the soma-ipsilateral hemispheres of the thoracic and abdominal ganglia. In contrast, serotonin-immunostaining occurred predominantly in interneurones projecting via soma-contralaterally ascending axons to the thorax and brain. In addition, serotonin-immunoreactivity was also present in efferent cells and afferent elements. Serotonin-immunoreactive, but no dopamine-immunoreactive, varicose fibres were observed on the surface of some peripheral nerves. Varicose endings of both dopamine-and serotonin-immunoreactive neurones occurred in each neuromere and showed overlapping neuropilar projections in dorsal and medial regions of the thoracic ganglia. Ventral associative neuropiles lacked dopamine-like immunostaining but were innervated by serotonin-immunoreactive elements. A colocalization of the two amines was not observed. The topographic representation of neurone types immunoreactive for serotonin and dopamine is discussed with respect to possible modulatory functions of these biogenic amines in the central nervous system of the cricket.

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References

  • Agricola H, Hertel W, Penzlin H (1988) Octopamin—Neurotransmitter, Neuromodulator, Neurohormon. Zool Jb Physiol 92:1–45

    Google Scholar 

  • Ali DW, Orchard I, Lange AB (1993) The aminergic control of locust (Locusta migratoria) salivary glands: evidence for dopaminergic and serotonergic innervation. J Insect Physiol 39:623–632

    Google Scholar 

  • Bach-y-Rita P (1993) Neurotransmission in the brain by diffusion through extracelluar fluid: a review. Neuroreport 4:343–350

    Google Scholar 

  • Baines RA, Tyrer NM, Downer RGH (1990) Serotonergic innervation of the locust mandibular closer muscle modulates contractions through the elevation of cyclic adenosine monophosphate. J Comp Neurol 294:623–633

    Google Scholar 

  • Bicker G, Menzel M (1989) Chemical codes for the control of behaviour in arthropods. Nature 337:33–39

    Google Scholar 

  • Bishop CA, O'Shea M (1983) Serotonin immunoreactive neurons in the central nervous sytem of an insect (Periplaneta americana). J Neurobiol 14:251–269

    Google Scholar 

  • Bloom FE (1981) A comparison of serotonergic and noradrenergic neurotransmission in mammalian CNS. In: Jacobs BL, Gelperin A (eds) Serotonin neurotransmission and behavior. MIT Press, Cambridge, Mass. pp 403–419

    Google Scholar 

  • Bräunig P (1987) The satellite nervous system—an extensive neurohemal network in the locust. J Comp Physiol [A] 160:69–77

    Google Scholar 

  • Brookhart GL, Edgecomb RS, Murdock LL (1987) Amphetamine and reserpine deplete brain biogenic amines and alter blowfly feeding behavior. J Neurochem 48:1307–1315

    Google Scholar 

  • Budnik V, White K (1988) Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 268:400–413

    Google Scholar 

  • Casagrand JL, Ritzmann RE (1992) Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach. J Neurobiol 23:644–655

    Google Scholar 

  • Claassen DE, Kammer AE (1986) Effects of octopamine, dopamine and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. J Neurobiol 17:1–14

    Google Scholar 

  • Consolazione A, Cuello A (1982) CNS serotonin pathways. In: Osborne NN (ed) Biology of serotonergic transmission. Wiley, Chichester, pp 29–62

    Google Scholar 

  • Consolazione A, Milstein C, Wright B, Cuello A (1981) Immunocytochemical detection of serotonin with monoclonal antibodies. J Histochem Cytochem 29:1425–1430

    Google Scholar 

  • Davis JPL, Pitman RM (1991) Characterization of receptors mediating the actions of dopamine on an identified inhibitory motoneurone of the cockroach. J Exp Biol 155:203–217

    Google Scholar 

  • Davis NT (1987) Neurosecretory neurons and their projections to the serotonin neurohemal system of the cockroach Periplaneta americana (L.) and identification of mandibular and maxillary motor neurons associated with this system. J Comp Neurol 259:604–621

    Google Scholar 

  • Distler P (1990) Synaptic connections of dopamine-immunoreactive neurons in the antennal lobes of Periplaneta americana. Colocalization with GABA-like immunoreactivity. Histochemistry 93:401–408

    Google Scholar 

  • Elekes K, Hustert R, Geffard M (1987) Serotonin-immunoreactive and dopamine-immunoreactive neurones in the terminal ganglion of the cricket, Acheta domestica: light-and electron-microscopic immunocytochemistry. Cell Tissue Res 250: 167–180

    Google Scholar 

  • Erber J, Kloppenburg P, Schneider A (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073–1083

    Google Scholar 

  • Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

    Google Scholar 

  • Evans PD, Green KL (1990) The action of dopamine receptor antagonists on the secretory response of the cockroach salivary gland in vitro. Comp Biochem Physiol [C] 97:283–286

    Google Scholar 

  • Gifford AN, Nicholson RA, Pitman RM (1991) The dopamine and 5-hydroxytryptamine content of locust and cockroach salivary glands. J Exp Biol 161:405–414

    Google Scholar 

  • Goldstein RS, Camhi JM (1991) Different effects of the biogenic amines dopamine, serotonin and octopamine on the thoracic and abdominal portions of the escape circuit in the cockroach. J Comp Physiol [A] 168:103–112

    Google Scholar 

  • Gonzales A, Smeets WJAJ (1991) Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltii. J Comp Neurol 303:457–477

    Google Scholar 

  • Gras H, Hörner M (1992) Wind-evoked escape running of the cricket, Gryllus bimaculatus. I. Behavioural analysis. J Exp Biol 171:189–214

    Google Scholar 

  • Grillner S, Brodin L, Sigvard K, Dale N (1986) On the spinal network generating locomotion in the lamprey. In: Grillner S, Stein PSG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion. MacMillan, London, pp 335–352

    Google Scholar 

  • Haeften T van, Schooneveld H (1992) Serotonin-like immunoreactivity in the ventral nerve cord of the Colorado potato beetle, Leptinotarsa decemlineata: identification of five different neuron classes. Cell Tissue Res 270:405–413

    Google Scholar 

  • Harris-Warrick RM, Flamm RE, Johnson BR, Katz PS (1989) Modulation of neural circuits in Crustacea. Am Zool 29:1305–1320

    Google Scholar 

  • Hardt M, Agricola H (1991) Serotonin-like immunoreactivity within the cricket prothoracic auditory pathway. In: Elsner N, Penzlin H (eds) Synapse-Transmission-Modulation. Proceedings of the 19th Göttingen Neurobiology Conference. Thieme, Stuttgart New York, p 135

    Google Scholar 

  • Hörner M (1992) Wind-evoked escape running of the cricket, Gryllus bimaculatus. II. Neurophysiological analysis. J Exp Biol 171:215–245

    Google Scholar 

  • Hörner M, Gras H, Schürmann FW (1989) Modulation of wind sensitivity in thoracic interneurons during cricket escape behavior. Naturwissenschaften 76:534–536

    Google Scholar 

  • Hörner M, Helle J, Pauls M, Spörhase-Eichmann U, Schürmann FW (1994) The topography of histamine-, dopamine-and serotonin-immunoreactive neurones in the ventral nerve cord of the cricket, Gryllus bimaculatus. Verh Dtsch Zool Ges 87: 135

    Google Scholar 

  • Homberg U, Hildebrand JGH (1989) Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258:1–24

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of the avidin-biotincomplex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    Google Scholar 

  • Huff R, Furst A, Mahowald AP (1989) Drosophila embryonic neuroblasts in culture: autonomous differentiation of neural specific neurotransmitters. Dev Biol 134:146–157

    Google Scholar 

  • Hustert R, Topel U (1986) Location and major postembryonic changes of identified 5-HT-immunoreactive neurones in the terminal ganglion of the cricket (Acheta domesticus). Cell Tissue Res 245:615–621

    Google Scholar 

  • Johnson SE, Murphy RK (1985) The afferent projection of mesothoracic bristle hairs in the cricket, Acheta domesticus. J Comp Physiol [A] 156:369–379

    Google Scholar 

  • Kien J, Fletcher WA, Altman JS, Ramirez JM, Roth U (1990) Organisation of intersegmental interneurons in the suboesophageal ganglion of Schistocerca gregaria (Forskål) and Locusta migratoria migratorioides (Reiche and Fairmaire) (Acrididae, Orthoptera). J Insect Morphol Embryol 19:35–60

    Google Scholar 

  • Klemm N (1972) Monoamine-containing nervous fibers in foregut and salivary gland of the desert locust, Schistocerca gregaria Forskål (Insecta, Acrididae). Comp Biochem Physiol [A] 43:207–211

    Google Scholar 

  • Klemm N (1974) Vergleichend-histochemische Untersuchungen über die Verteilung monoaminhaltiger Strukturen im Oberschlundganglion von Angehörigen verschiedener Insekten-Ordnungen. Entomol Germ 1:21–49

    Google Scholar 

  • Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169

    Google Scholar 

  • Klemm N (1983) Detection of serotonin containing neurons in the insect nervous system by antibodies to 5-HT. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin, Heidelberg, New York, pp 302–316

    Google Scholar 

  • Knowles F, Bern HA (1966) The function of neurosecretion in endocrine regulation. Nature 210:271

    Google Scholar 

  • Kravitz EA (1989) Hormonal control of behavior: amines as gainsetting elements that bias behavioral output in lobsters. Am Zool 30:595–608

    Google Scholar 

  • Lutz EM, Tyrer NM (1988) Immunocytochemical localization of serotonin and choline acetyltransferase in sensory neurones of the locust. J Comp Neurol 267:335–342

    Google Scholar 

  • Menzel R, Wittstock S, Sugawa M (1989) Chemical codes of learning and memory in honey bees. In: Sqirre LR, Lindenlaub E (eds) The biology of memory. Schattauer, Stuttgart New York, pp 335–355

    Google Scholar 

  • Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res 234:655–677

    Google Scholar 

  • Michelsen DB (1988) Catecholamines affect storage and retrieval of conditioned odor stimuli in honey bees. Comp Biochem Physiol [C] 91:479–482

    Google Scholar 

  • Milton GWA, Verhaert PDEM, Downer RGH (1991) Immunofluorescent localization of dopamine-like and leucine-encephalin-like neurons in the supraoesophageal ganglia of the American cockroach, Periplaneta americana. Tissue Cell 23:331–340

    Google Scholar 

  • Murphy RK (1981) The structure and development of a somatotopic map in crickets: the cercal afferent projection. Dev Biol 88:236–246

    Google Scholar 

  • Nässel DR (1987) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85

    Google Scholar 

  • Nässel DR, Elekes K (1984) Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect; Calliphora erythrocephala. Neurosci Lett 48:203–210

    Google Scholar 

  • Nässel DR, Elekes K (1985) Serotonergic terminals in the neural sheath of the blowfly nervous system: ultrastructural immunocytochemistry and 5,7-dihydroxytryptamine labelling. Neuroscience 15:293–307

    Google Scholar 

  • Nässel DR, Elekes K (1992) Aminergic neurons in the brain of blowflies and Drosophila: dopamine-and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res 267:147–167

    Google Scholar 

  • Nässel DR, Elekes K, Johansson KUI (1988) Dopamine-immunoreactive neurons in the blowfly visual system: light and electron microscopic immunocytochemistry. J Chem Neuroanat 1:311–325

    Google Scholar 

  • Nagao T, Tanimura T (1988) Distribution of biogenic amines in the cricket central nervous system. Analyt Biochem 171:33–40

    Google Scholar 

  • Nyhof-Young J, Orchard I (1990) Tyrosine hydroxylase-like immunoreactivity in the brain of the fifth instar Rhodnius prolixus Stål (Hemiptera Reduviidae). J Comp Neurol 302:322–329

    Google Scholar 

  • Orchard I, Lange AB, Brown BB (1992) Tyrosine hydroxylase-like immunoreactivity in the ventral nerve cord of the locust (Locusta migratoria) including neurones innervating the salivary glands. J Insect Physiol 38:19–27

    Google Scholar 

  • Orchard I, Ramirez J M, Lange A B (1993) A multifunctional role for octopamine in locust flight. Annu Rev Entomol 38:227–249

    Google Scholar 

  • Panov AA (1966) Correlation in the ontogenetic development of the central nervous system in the house cricket Gryllus domesticus L. (Orthoptera, Grylloidea). Entomol Rev 45:179–185

    Google Scholar 

  • Panov AA (1980) Demonstration of neurosecretory cells in the insect nervous system. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques: insect nervous system. Springer, Berlin Heidelberg, New York, pp 25–50

    Google Scholar 

  • Raabe M (1982) Insect neurohormones. Plenum Press, New York, London

    Google Scholar 

  • Roeder T (1994) Biogenic amines and their receptors in insects. Comp Biochem Physiol [C] 107:1–12

    Google Scholar 

  • Schachtner J, Bräunig P (1993) The activity pattern of identified neurosecretory cells during feeding behaviour in the locust. J Exp Biol 185:287–303

    Google Scholar 

  • Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43–58

    Google Scholar 

  • Schildberger K, Hörner M (1988) The function of auditory neurons in cricket phonotaxis. I. The influence of hyperpolarization of identified neurons in sound localization. J Comp Physiol [A] 163:621–631

    Google Scholar 

  • Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurones in the brain of the honeybee. J Comp Neurol 225:570–580

    Google Scholar 

  • Schürmann FW, Woermann J (1986) On the distribution of serotonin and GABA in the brain of crickets. Verh Dtsch Zool Ges 79:295

    Google Scholar 

  • Schürmann FW, Elekes K, Geffard M (1989) Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 254:399–410

    Google Scholar 

  • Skiebe P, Corette BJ, Wiese K (1990) Evidence that histamine is the inhibitory transmitter of the auditory interneuron ONI of crickets. Neurosci Lett 116:361–366

    Google Scholar 

  • Spörhase-Eichmann U, Schürmann FW (1988) Serotonin-immunoreactivity in the central nervous system of the cricket Gryllus bimaculatus. In: Elsner N, Barth FG, (eds) Sense organs. Proceedings of the 16th Göttingen Neurobiology Conference Thieme, Stuttgart New York, p 298

    Google Scholar 

  • Spörhase-Eichmann U, Gras H, Schürmann FW (1987) Patterns of serotonin immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. I. Ganglia of the ventral nerve cord. Cell Tissue Res 249:601–614

    Google Scholar 

  • Spörhase-Eichmann U, Hanssen M, Schürmann FW (1989) GABA-immunoreactive neurons in the prothoracic ganglion of the cricket Gryllus bimaculatus. In: Elsner N, Singer W (eds) Dynamics and plasticity in neuronal systems. Proceedings of the 17th Göttingen Neurobiology Conference. Thieme, Stuttgart New York, p 55

    Google Scholar 

  • Spörhase-Eichmann U, Vullings HGB, Buijs RM, Hörner M, Schürmann FW (1992) Octopamine-immunoreactive neurons in the central nervous system of the cricket, Gryllus bimaculatus. Cell Tissue Res 268:287–304

    Google Scholar 

  • Steinbusch HWM, Tilders FJH (1987) Immunocytochemical techniques for light microscopical localization of dopamine, noradrenaline, adrenaline, serotonin and histamine in the central nervous system. In: Steinbusch HWM (ed) Monoaminergic neurons: light microscopy and ultrastructure. Wiley, Chichester, pp 125–166

    Google Scholar 

  • Steinbusch HWM, Vliet SP van, Bol JGJM, Vente J de (1991) Development and application of antibodies to primary (DA, LDOPA) and secondary (cGMP) messengers: a technical report. In: Calas A and Eugène D (eds) Neurocytochemical methods. NATO ASI series H 58. Springer, Berlin Heidelberg New York, pp 1–27

    Google Scholar 

  • Sternberger LA (1986) Immunocytochemistry, 3rd edn. Wiley, New York

    Google Scholar 

  • Stevenson PA, Spörhase-Eichmann U (1995) Localization of octopaminergic neurones in insects. Comp Biochem Physiol (in press)

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

    Google Scholar 

  • Taghert PH, Bastiani M, 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 

  • 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 

  • Tyrer NM, Turner JD, Altman JS (1984) Identifiable neurons in the locust central nervous system that react with antibodies to serotonin. J Comp Neurol 227:313–330

    Google Scholar 

  • Venus B, Helle J, Schürmann FW (1992) Dopaminergic neurons in the ventral nerve cord of the cricket Gryllus bimaculatus. In: Elsner N, Richter DW (eds) Rhythmogenesis in neurons and networks. Proceedings of the 20th Göttingen Neurobiology Conference. Thieme, Stuttgart New York, p 493

    Google Scholar 

  • Viellemaringe J, Cailley-Lescure H, Bensch C, Girardie J (1981) Etude en histofluorescence des cellules aminergiques dans le système nerveux central du criquet migrateur. J Physiol (Paris) 77:989–995

    Google Scholar 

  • Watson AHD (1992) The distribution of dopamine-like immunoreactivity in the thoracic and abdominal ganglia of the locust (Schistocerca gregaria). Cell Tissue Res 270:113–124

    Google Scholar 

  • Wendt B, Homberg U (1992) Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321:387–403

    Google Scholar 

  • Wigglesworth VB (1957) The use of osmium in the fixation of tissues. Proc R Soc Lond [Biol] 147:185–199

    Google Scholar 

  • Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool 176:67–86

    Google Scholar 

  • Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket, Gryllus campestris L. J Comp Physiol 146:161–173

    Google Scholar 

  • Wohlers DW, Huber F (1985) Topographical organization of the auditory pathway within the prothoracic ganglion of the cricket Gryllus campestris L. Cell Tissue Res 239:555–565

    Google Scholar 

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  1. Zoologisches Institut, Abteilung für Zellbiologie, Universität Göttingen, Berlinerstrasse 28, D-37073, Göttingen, Germany

    Michael Hörner, Ulrike Spörhase-Eichmann, Johannes Helle, Brüne Venus & Friedrich-Wilhelm Schürmann

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  1. Michael Hörner
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  2. Ulrike Spörhase-Eichmann
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Hörner, M., Spörhase-Eichmann, U., Helle, J. et al. The distribution of neurones immunoreactive for β-tyrosine hydroxylase, dopamine and serotonin in the ventral nerve cord of the cricket, Gryllus bimaculatus . Cell Tissue Res 280, 583–604 (1995). https://doi.org/10.1007/BF00318362

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