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Dendritic projections of different types of octopaminergic unpaired median neurons in the locust metathoracic ganglion

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Abstract

Octopaminergic dorsal unpaired median (DUM) neurons of locust thoracic ganglia are important components of motor networks and are divided into various sub-populations. We have examined individually stained metathoracic DUM neurons, their dendritic projection patterns, and their relationship to specific architectural features of the metathoracic ganglion, such as longitudinal tracts, transverse commissures, and well-defined sensory neuropils. The detailed branching patterns of individually characterized DUM neurons of various types were analyzed in vibratome sections in which architectural features were revealed by using antibodies against tubulin and synapsin. Whereas DUM3,4,5 and DUM5 neurons (the group innervating leg and “non-wing-power” muscles) had many ventral and dorsal branches, DUM1 and DUM3,4 neurons (innervating “wing-power” muscles) branched extensively only in dorsal areas. The structure of DUM3 neurons differed markedly from that of the other DUM neurons examined in that they sent branches into dorsal areas and had differently structured side branches that mostly extended laterally. The differences between the branching patterns of these neurons were quantified by using currently available new reconstruction algorithms. These structural differences between the various classes of DUM neurons corresponded to differences in their function and biophysical properties.

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References

  • Baudoux S, Burrows M (1998) Synaptic activation of efferent neuromodulatory neurones in the locust Schistocerca gregaria. J Exp Biol 201:3339–3354

    PubMed  CAS  Google Scholar 

  • Baudoux S, Duch C, Morris OT (1998) Coupling of efferent neuromodulatory neurons to rhythmical leg motor activity in the locust. J Neurophysiol 79:361–370

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Binder MD (2002) Integration of synaptic and intrinsic dendritic currents in cat spinal motoneurons. Brain Res Brain Res Rev 40:1–8

    Article  PubMed  Google Scholar 

  • Bräunig P (1991) Suboesophageal DUM neurones innervate the principal neuropils of the locust brain. Philos Trans R Soc Lond Biol 322:221–240

    Article  Google Scholar 

  • Bräunig P, Burrows M (2004) Projection patterns of posterior dorsal unpaired median neurons of locust subesophageal ganglion. J Comp Neurol 478:164–175

    Article  PubMed  Google Scholar 

  • Bräunig P, Pflüger H-J (2001) The unpaired median neurons of insects. Adv Insect Physiol 28:185–266

    Google Scholar 

  • Bucher D, Pflüger H-J (2000) Directional sensitivity of an identified wind-sensitive interneuron during the postembryonic development of the locust. J Insect Physiol 46:1545–1556

    Article  PubMed  CAS  Google Scholar 

  • Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, Oxford

    Google Scholar 

  • Burrows M, Pflüger H-J (1995) Action of locust neuromodulatory neurons is coupled to specific motor patterns. J Neurophysiol 74:347–357

    PubMed  CAS  Google Scholar 

  • Cuntz H, Haag J, Borst A (2003) Neural image processing by dendritic networks. Proc Natl Acad Sci USA 100:11082–11085

    Article  PubMed  CAS  Google Scholar 

  • Duch C, Pflüger H-J (1999) DUM neurons in locust flight: a model system for amine mediated peripheral adjustments to the requirements of a central motor program. J Comp Physiol [A] 184:489–499

    Article  CAS  Google Scholar 

  • Eckert M, Rapus J, Nürnberger A, Penzlin H (1992) A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322:1–15

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Evans PD, O’Shea M (1977) An octopaminergic neurone modulates neuromuscular transmission in the locust. Nature 270:257–259

    Article  PubMed  CAS  Google Scholar 

  • Evers JF, Schmitt S, Sibilia M, Duch C (2005) Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J Neurophysiol 93:2331–2342

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Grillner S, Graybiel AM (2006) Microcircuits: the interface between single neurons and global brain function. Dahlem workshop report. MIT Press, Cambridge, USA

    Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    Article  Google Scholar 

  • Heidel E, Pflüger H-J (2006) Differential ion current expression in identified subtypes of locust octopaminergic dorsal unpaired median (DUM-) neurons. Eur J Neurosci 23:1189–1206

    Article  PubMed  CAS  Google Scholar 

  • Heitler WJ, Goodman CS (1978) Multiple sites of spike initiation in a bifurcating locust neurone. J Exp Biol 76:63–84

    Google Scholar 

  • Hoyle G (1978) The dorsal, unpaired, median neurones of the locust metathoracic ganglion. J Neurobiol 9:43–57

    Article  PubMed  CAS  Google Scholar 

  • Hoyle G (1985) Generation of motor activity and control of behaviour: the role of the neuromodulator octopamine and the orchestration hypothesis. In: Kerkut GA, Gilbert L (eds) Comparative insect physiology, biochemistry and pharmacology, vol 5. Pergamon, Toronto, pp 607–621

    Google Scholar 

  • Hoyle G, Dagan D (1978) Physiological characteristics and reflex activation of DUM (octopaminergic) neurons of locust metathoracic ganglion. J Neurobiol 9:59–79

    Article  PubMed  CAS  Google Scholar 

  • Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165

    PubMed  CAS  Google Scholar 

  • Konings PNM, Vullings HG, Geffard M, Buijs RM, Diederen JHB, Jansen WF (1988) Immunocytochemical demonstration of octopamine-immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 251:371–379

    Article  PubMed  CAS  Google Scholar 

  • Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583–595

    Article  PubMed  CAS  Google Scholar 

  • Libersat F, Pflüger H-J (2004) Monoamines and the orchestration of behavior. BioScience 54:17–25

    Article  Google Scholar 

  • Mentel T, Duch C, Stypa H, Müller U, Wegener G, Pflüger H-J (2003) Central modulatory neurons control fuel selection in flight muscle of migratory locust. J Neurosci 23:1109–1113

    PubMed  CAS  Google Scholar 

  • Merritt DJ, Murphey RK (1992) Projections of leg proprioceptors within the CNS of the fly Phormia in relation to generalized insect ganglia. J Comp Neurol 322:16–34

    Article  PubMed  CAS  Google Scholar 

  • Morris OT, Duch C, Stevenson PA (1999) Differential activation of octopaminergic (DUM) neurons via proprioceptors responding to flight muscle contractions in the locust. J Exp Biol 202:3555–3564

    PubMed  Google Scholar 

  • Murphey RK, Possidente DR, Vandervorst P, Ghysen A (1989a) Compartments and the topography of leg afferent projections in Drosophila. J Neurosci 9:3209–3217

    PubMed  CAS  Google Scholar 

  • Murphey RK, Possidente DR, Pollack G, Merritt DJ (1989b) Modality specific axonal projections within the CNS of the flies Phormia and Drosophila. J Comp Neurol 290:185–200

    Article  PubMed  CAS  Google Scholar 

  • Newland PL (1991) Morphology and somatotopic organisation of the central projections of afferents from tactile hairs on the hind leg of the locust. J Comp Neurol 312:493–508

    Article  PubMed  CAS  Google Scholar 

  • Newland PL, Rogers SM, Gaaboub I, Matheson T (2000) Parallel somatotopic maps of gustatory and mechanosensory neurons in the central nervous system of an insect. J Comp Neurol 425:82–96

    Article  PubMed  CAS  Google Scholar 

  • Pflüger H-J, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396

    Article  CAS  Google Scholar 

  • Pflüger HJ, Watson AHD (1995) GABA and glutamate-like immunoreactivity at synapses received by dorsal unpaired median neurones in the abdominal nerve cord of the locust. Cell Tissue Res 280:325–333

    PubMed  Google Scholar 

  • Pflüger H-J, Bräunig P, Hustert R (1988) The organization of mechanosensory neuropils in locust thoracic ganglia. Philos Trans R Soc Lond Biol 321:1–26

    Article  Google Scholar 

  • Pflüger H-J, Duch C, Heidel E (2004) The Ernst Florey Memorial Lecture. Neuromodulatory octopaminergic neurones and their functions during insect motor behaviour. Acta Biol Hung 55:3–12

    Article  PubMed  Google Scholar 

  • Rall W (1962) Theory of physiological properties of dendrites. Ann N Y Acad Sci 96:1071–1092

    Article  PubMed  CAS  Google Scholar 

  • Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30:1169–1193

    PubMed  CAS  Google Scholar 

  • Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533–561

    Article  PubMed  CAS  Google Scholar 

  • Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477

    Article  PubMed  CAS  Google Scholar 

  • Rowell CHF (1971) The orthopteran descending movement detector (DMD) neurons: a characterisation and review. Z Vergl Physiol 73:167–194

    Article  Google Scholar 

  • Schmitt S, Evers JF, Scholz M, Duch C, Obermayer K (2004) New methods for the computer assisted 3D reconstruction of neurons from confocal image stacks. Neuroimage 23:1283–1298

    Article  PubMed  Google Scholar 

  • Sombati S, Hoyle G (1984) Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J Neurobiol 15:481–506

    Article  PubMed  CAS  Google Scholar 

  • Stevenson PA, Kutsch W (1988) Demonstration of functional connectivity of the flight motor system in all stages of the locust. J Comp Physiol [A] 162:247–259

    Article  Google Scholar 

  • Stevenson PA, Pflüger H-J (1994) Colocalization of octopamine and FMRFamide related peptide in identified heart projecting (DUM) neurones in the locust revealed by immunocytochemistry. Brain Res 638:117–125

    Article  PubMed  CAS  Google Scholar 

  • Stevenson PA, Spörhase-Eichmann U (1995) Localization of octopaminergic neurones in insects. Comp Biochem Physiol [A] 110:203–215

    Article  CAS  Google Scholar 

  • Stevenson PA, Pflüger H-J, Eckert M, Rapus J (1992) Octopamine immunoreactive cell populations in the locust thoracic-abdominal nervous system. J Comp Neurol 315:382–397

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Watson AHD (1984) The dorsal unpaired median neurons of the locust metathoracic ganglion: neuronal structure and diversity, and synapse distribution. J Neurocytol 13:303–327

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are indebted to Dr. F. Evers, Cambridge, UK, to Dr. D. Münch, Oslo, Norway, and to Dr. C. Duch, Tempe, USA, for help with the AMIRA program and numerous discussions, and, in particular, to Heike Wolfenberg, Berlin, for expert technical assistance. We are also grateful to Dr. A.H.D. Watson, Cardiff, UK, to Dr. J. Rybak and M. Wurm, Berlin, and to two anonymous referees for valuable suggestions and critical reading of the manuscript.

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Correspondence to Natalia L. Kononenko.

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N.L.K. gratefully acknowledges receipt of a fellowship from the Alexander von Humboldt Foundation, Bonn, Germany, and financial support from the research committee (Forschungskommission) of the Freie Universität Berlin.

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Kononenko, N.L., Pflüger, HJ. Dendritic projections of different types of octopaminergic unpaired median neurons in the locust metathoracic ganglion. Cell Tissue Res 330, 179–195 (2007). https://doi.org/10.1007/s00441-007-0425-3

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