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Ultrastructure of pigment-dispersing hormone-immunoreactive neurons in a three-dimensional model of the accessory medulla of the cockroach Leucophaea maderae

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Abstract

Locomotor activity rhythms of the cockroach Leucophaea maderae are orchestrated by two bilaterally symmetric, mutually coupled, circadian pacemakers. They lie in the optic lobes of the brain and are confined to the accessory medulla (AMe), ventro-medially to the medulla. The AMe is innervated by approximately 12 pigment-dispersing hormone (PDH)-immunoreactive anterior medulla neurons (PDHMe), which are circadian pacemaker candidates in the fruitfly and the cockroach. We have developed a three-dimensional computer model of the AMe and associated structures as a framework for neuroanatomical studies. Our greatly improved understanding of this structure in space has allowed us further to subdivide the anterior PDHMe into three subgroups, i.e., large, medium-sized, and small anterior PDHMe. The synaptic connections of two of these subgroups have been examined within subcompartments of the AMe by light and electron microscopy. The large, intensely staining, anterior PDHMe contain medium-sized dense-core vesicles and form input and output synapses with profiles densely filled with clear vesicles primarily in the anterior and shell neuropil of the AMe. The medium-sized anterior PDHMe contain large dense-core vesicles and constitute input and output synapses either with profiles being densely filled with clear vesicles, or with profiles containing granular dense-core vesicles. The small, weakly staining anterior PDHMe belong to a morphological group different from the large and medium-sized PDHMe and cannot be further identified at the electron-microscopic level because of their weak PDH immunoreactivity.

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References

  • Chiang AS, Liu YC, Chiu SL, Hu SH, Huang CY, Hsieh CH (2001) Three-dimensional mapping of brain neuropils in the cockroach, Diploptera punctata. J Comp Neurol 440:1–11

    Article  CAS  PubMed  Google Scholar 

  • Chiba Y, Tomioka K (1987) Insect circadian activity with special reference to the localization of the pacemaker. Zool Sci 4:945–954

    Google Scholar 

  • Dircksen H, Zahnow CA, Gaus G, Keller R, Rao KR, Riem JP (1987) The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean glands: identification by an antiserum against a synthetic PDH. Cell Tissue Res 250:377–387

    CAS  Google Scholar 

  • Fleissner G, Loesel R, Fleissner G, Waterkamp M, Kleiner O, Batschauer A, Homberg U (2001) Candidates for extraocular photoreceptors in the cockroach suggest homology to the lamina and lobula organs in beetles. J Comp Neurol 433:401–414

    Article  CAS  PubMed  Google Scholar 

  • Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383–394

    CAS  PubMed  Google Scholar 

  • Helfrich-Förster C (1995) The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 92:612–616

    PubMed  Google Scholar 

  • Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594

    PubMed  Google Scholar 

  • Helfrich-Förster C, Täuber M, Park JH, Muhlig-Versen M, Schneuwly S, Hofbauer A (2000) Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. J Neurosci 20:3339–3353

    PubMed  Google Scholar 

  • Homberg U, Hildebrand JG (1989) Serotonin immunoreactivity in the optic lobes of the sphinx moth Manduca sexta and colocalization with FMRFamide and SCP immunoreactivity. J Comp Neurol 288:243–253

    CAS  PubMed  Google Scholar 

  • Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266:343–357

    Google Scholar 

  • Homberg U, Reischig T, Stengl M (2003) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591

    Google Scholar 

  • Langford LA, Coggeshall RE (1980) The use of potassium ferricyanide in neural fixation. Anat Rec 197:297–303

    CAS  PubMed  Google Scholar 

  • Loesel R, Homberg U (1999) Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae. Brain Res 842:408–418

    Article  CAS  PubMed  Google Scholar 

  • Loesel R, Homberg U (2001) Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol 439:193–207

    Article  CAS  PubMed  Google Scholar 

  • Nishiitsutsuji-Uwo J, Pittendrigh CS (1968a) Central nervous system control of circadian rhythmicity in the cockroach. III. The pathway of light signals that entrain the rhythm. Z Vergl Physiol 58:1–13

    Google Scholar 

  • Nishiitsutsuji-Uwo J, Pittendrigh CS (1968b) Central nervous system control of circadian rhytmicity in the cockroach. II. The optic lobes, locus of the driving oscillator? Z Vergl Physiol 58:14–46

    Google Scholar 

  • Page TL (1982) Transplantation of the cockroach circadian pacemaker. Science 216:73–75

    Google Scholar 

  • Page TL (1983a) Effects of optic-tract regeneration on internal coupling in the circadian system of the cockroach. J Comp Physiol [A] 153:353–363

    Google Scholar 

  • Page TL (1983b) Regeneration of the optic tracts and circadian pacemaker activity in the cockroach Leucophaea maderae. J Comp Physiol [A] 152:231–240

    Google Scholar 

  • Page TL (1984) Neuronal organization of a circadian clock in the cockroach Leucophaea maderae. In: Page TL (ed) Ciba foundation symposium 104. Photoperiodic regulation of insect and molluscan hormones. Pitman, London, pp 115–135

  • Page TL (1987) Serotonin phase-shifts the circadian rhythm of locomotor activity in the cockroach. J Biol Rhythms 2:23–34

    CAS  PubMed  Google Scholar 

  • Page TL, Caldarola PC, Pittendrigh CS (1977) Mutual entrainment of bilaterally distributed circadian pacemakers. Proc Natl Acad Sci USA 74:1277–1281

    CAS  PubMed  Google Scholar 

  • Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, Hall JC (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA 97:3608–3613

    Article  CAS  PubMed  Google Scholar 

  • Peters A, Palay SL (1996) The morphology of synapses. J Neurocytol 25:687–700

    CAS  PubMed  Google Scholar 

  • Petri B, Stengl M (1997) Pigment-dispersing hormone shifts the phase of the circadian pacemaker of the cockroach Leucophaea maderae. J Neurosci 17:4087–4093

    CAS  PubMed  Google Scholar 

  • Petri B, Stengl M (1999) Presumptive insect circadian pacemakers in vitro: immunocytochemical characterization of cultured pigment-dispersing hormone-immunoreactive neurons of Leucophaea maderae. Cell Tissue Res 296:635–643

    Article  CAS  PubMed  Google Scholar 

  • Petri B, Stengl M, Würden S, Homberg U (1995) Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae. Cell Tissue Res 282:3–19

    CAS  PubMed  Google Scholar 

  • Petri B, Homberg U, Loesel R, Stengl M (2002) Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205:1459–1469

    CAS  PubMed  Google Scholar 

  • Rein K, Zockler M, Mader MT, Grubel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231

    Google Scholar 

  • Reischig T, Stengl M (1996) Morphology and pigment-dispersing hormone immunocytochemistry of the accessory medulla, the presumptive circadian pacemaker of the cockroach Leucophaea maderae: a light- and electron-microscopic study. Cell Tissue Res 285:305–319

    Article  Google Scholar 

  • Reischig T, Stengl M (2002) Optic lobe commissures in a three-dimensional brain model of the cockroach Leucophaea maderae: a search for the circadian coupling pathways. J Comp Neurol 443:388–400

    Article  PubMed  Google Scholar 

  • Reischig T, Stengl M (2003) Ectopic transplantation of the accessory medulla restores circadian locomotor rhythms in arrhythmic cockroaches (Leucophaea maderae). J Exp Biol 206:1877–1886

    Article  PubMed  Google Scholar 

  • Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99:791–802

    CAS  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    CAS  Google Scholar 

  • Richardson KC, Jarett I, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323

    CAS  Google Scholar 

  • Roberts SK (1965) Photoreception and entrainment of cockroach activity rhythms. Science 148:958–959

    Google Scholar 

  • Roberts SK (1974) Circadian rhythms in cockroaches: effects of optic lobe lesions. J Comp Physiol 88:21–30

    Google Scholar 

  • Romeis B (1989) Mikroskopische Technik, 16. edn. Urban und Schwarzenberg, Munich

  • Sokolove PG (1975) Localization of the cockroach optic lobe circadian pacemaker with microlesions. Brain Res 87:13–21

    Google Scholar 

  • Stanewsky R (2002) Clock mechanisms in Drosophila. Cell Tissue Res 309:11–26

    Article  CAS  PubMed  Google Scholar 

  • Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol [A] 175:203–213

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry, 2nd edn. Wiley, New York

  • Taghert PH, Hewes RS, Park JH, O’Brien MA, Han M, Peck ME (2001) Multiple amidated neuropeptides are required for normal circadian locomotor rhythms in Drosophila. J Neurosci 21:6673–6686

    CAS  PubMed  Google Scholar 

  • Veenstra JA, Hagedorn HH (1993) Sensitive enzyme immunoessay for Manduca allatotropin and the existence of an allatotropin-immunoreactive peptide in Periplaneta americana. Arch Insect Biochem Physiol 23:99–109

    CAS  Google Scholar 

  • Westfall JA (1987) Ultrastructure of invertebrate synapses. In: Ali MA (ed) Nervous systems in invertebrates. Plenum, New York, pp 3–28

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Acknowledgements

We are very grateful to Dr. H. Dircksen (University of Bonn, Germany) for providing the anti-β-PDH antiserum.

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Authors and Affiliations

  1. Department of Biology, Institute of Animal Physiology, Philipps University Marburg, Karl von Frisch Strasse, 35032, Marburg, Germany

    Thomas Reischig & Monika Stengl

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  1. Thomas Reischig
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  2. Monika Stengl
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Correspondence to Monika Stengl.

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This work was supported by Deutsche Forschungsgemeinschaft (DFG) grants STE 531/7-1, 2, 3, and Human Science Frontier

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Reischig, T., Stengl, M. Ultrastructure of pigment-dispersing hormone-immunoreactive neurons in a three-dimensional model of the accessory medulla of the cockroach Leucophaea maderae . Cell Tissue Res 314, 421–435 (2003). https://doi.org/10.1007/s00441-003-0772-7

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  • DOI: https://doi.org/10.1007/s00441-003-0772-7

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