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Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain

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Abstract

In honeybees (Apis mellifera), the biogenic amine octopamine has been shown to play a role in associative and non-associative learning and in the division of labour in the hive. Immunohistochemical studies indicate that the ventral unpaired median (VUM) neurones in the suboesophageal ganglion (SOG) are putatively octopaminergic and therefore might be involved in the octopaminergic modulation of behaviour. In contrast to our knowledge about the behavioural effects of octopamine, only one neurone (VUMmx1) has been related to a behavioural effect (the reward function during olfactory learning). In this study, we have investigated suboesophageal VUM neurones with fluorescent dye-tracing techniques and intracellular recordings combined with intracellular staining. Ten different VUM neurones have been found including six VUM neurones innervating neuropile regions of the brain and the SOG exclusively (central VUM neurones) and four VUM neurones with axons in peripheral nerves (peripheral VUM neurones). The central VUM neurones innervate the antennal lobes, the protocerebral lobes (including the lateral horn) and the mushroom body calyces. Of these, a novel mandibular VUM neurone, VUMmd1, exhibits the same branching pattern in the brain as VUMmx1 and responds to sucrose and odours in a similar way. The peripheral VUM neurones innervate the antennal and the mandibular nerves. In addition, we describe one labial unpaired median neurone with a dorsal cell body, DUMlb1. The possible homology between the honeybee VUM neurones and the unpaired median neurones in other insects is discussed.

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Abbreviations

DUM neurone:

dorsal unpaired median neurone

EPSPs:

excitatory post-synaptic potentials

l-ACT:

lateral antenno-cerebralis tract

LbMT:

labial midline tract

mACT:

median antenno-cerebralis tract

MdMT:

mandibular midline tract

MT:

midline tract

MxMT:

maxillary midline tract

octopamine-IR:

octopamine-immunoreactive

PL:

protocerebral lobe

PTG:

prothoracic ganglion

SOG:

suboesophageal ganglion

US:

unconditioned stimulus

VUM neurone:

ventral unpaired median neurone

References

  • Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurones in the honeybee, Apis mellifera. J Comp Neurol 437:363–383

    Article  PubMed  CAS  Google Scholar 

  • Allgäuer C, Honegger H (1993) The antennal motor system of crickets: modulation of muscle contractions by a common inhibitor, DUM neurones, and proctolin. J Comp Physiol [A] 173:485–494

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bitterman M, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119

    Article  PubMed  CAS  Google Scholar 

  • Bossing T, Technau G (1994) The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling. Development 120:1895–1906

    PubMed  CAS  Google Scholar 

  • Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege H-C, Menzel R (2006) A three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol (in press)

  • Braun G, Bicker G (1992) Habituation of an appetitive reflex in the honeybee. J Neurophysiol 67:588–598

    PubMed  CAS  Google Scholar 

  • Bräunig P (1988) Identification of a single prothoracic “dorsal unpaired median” (DUM) neurone supplying locust mouthpart nerves. J Comp Physiol [A] 163:835–840

    Article  Google Scholar 

  • Bräunig P (1990) The morphology of suboesophageal ganglion cells innervating the nervus corporis cardiaci II of the locust. Cell Tissue Res 260:95–108

    Article  Google Scholar 

  • Bräunig P (1991) Suboesophageal DUM neurones innervate the principal neuropiles of the locust brain. Philos Trans R Soc Lond Biol 332:221–240

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bräunig P, Eder M (1998) Locust dorsal unpaired medain (DUM) neurones directly innervate and modulate hindleg proprioreceptors. J Exp Biol 201:3333–3338

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bräunig P, Allgäuer C, Honegger H (1990) Suboesophageal DUM neurones are part of the antennal motor system of locusts and crickets. Experientia 46:259–261

    Article  Google Scholar 

  • Breuer T (1994) Seitenspezifische Sensitisierung und klassische Konditionierung bei der Honigbiene, Apis mellifera. Diploma thesis, FU Berlin

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

    Article  PubMed  CAS  Google Scholar 

  • Duch C, Mentel T, Pflüger H-J (1999) Distribution and activation of different types of octopaminergic DUM neurones in the locust. J Comp Neurol 403:119–134

    Article  PubMed  CAS  Google Scholar 

  • Ehmer B, Gronenberg W (1997) Proprioreceptors and fast antennal reflexes in the ant Odontomachus (Formicidae, Ponerinae). Cell Tissue Res 290:153–165

    Article  PubMed  CAS  Google Scholar 

  • Ellerkmann E (1994) Neuroneale Kontrolle und Modulation der Antennenbewegung bei der Honigbiene. PhD thesis, TU Berlin

  • Erber J, Pribbenow B, Kisch J, Faensen D (2000) Operant conditioning of antennal muscle activity in the honey bee (Apis mellifera L.). J Comp Physiol [A] 186:557–565

    Article  CAS  Google Scholar 

  • Farooqui T, Robinson K, Vaessin H, Smith B (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23:5370–5380

    PubMed  CAS  Google Scholar 

  • Frambach I, Rössler W, Winkler M, Schürmann F (2004) F-actin at identified synapses in the mushroom body neuropil of the insect brain. J Comp Neurol 475:303–314

    Article  PubMed  CAS  Google Scholar 

  • Ganeshina O, Menzel R (2001) GABA-immunoreactive neurones in the mushroom bodies of the honeybee; an electron microscopic study. J Comp Neurol 437:335–349

    Article  PubMed  CAS  Google Scholar 

  • Goodman L, Fletcher W, Guy R, Mobbs P, Pomfrett C (1987) Motion sensitive descending interneurones, ocellar LD neurones and neck motoneurones in the bee: a neural substrate for visual course control in Apis mellifera. In: Menzel R (ed) Neurobiology of the honeybee. Springer, Berlin Heidelberg New York, pp 158–171

    Google Scholar 

  • Griss C, Rowell C (1986) Three descending interneurones reporting deviation from course in the locust. I. Anatomy. J Comp Physiol [A] 158:765–774

    Article  CAS  Google Scholar 

  • Hammer M (1987) Elektrophysiologische und anatomische Charakterisierung von Motoneuronen und Interneuronen im Unterschlundganglion der Honigbiene, Apis mellifera. Diploma thesis, FU Berlin

  • Hammer M (1991) Analyse der funktionellen Rolle des Neurones VUMmx1 bei der klassischen Konditionierung des Rüsselreflexes der Biene. PhD thesis, FU Berlin

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

    Article  Google Scholar 

  • Hammer M (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci 20:245–251

    Article  PubMed  CAS  Google Scholar 

  • Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617–1630

    PubMed  CAS  Google Scholar 

  • Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156

    PubMed  CAS  Google Scholar 

  • Hammer M, Braun G, Mauelshagen J (1994) Food-induced arousal and nonassociative learning in honeybees: dependence of sensitization on the application site and duration of food stimulation. Behav Neural Biol 62:210–223

    Article  PubMed  CAS  Google Scholar 

  • Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209

    Article  PubMed  CAS  Google Scholar 

  • Honegger H, Allgäuer C, Klepsch U, Welker J (1990) Morphology of antennal motoneurones in the brains of two crickets, Gryllus bimaculatus and Gryllus campestris. J Comp Neurol 291:256–268

    Article  PubMed  CAS  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 

  • Ibbotson M (1991a) A motion-sensitive visual descending neurone in Apis mellifera monitoring translatory flowfields in the horizontal plane. J Exp Biol 157:573–577

    Google Scholar 

  • Ibbotson M (1991b) Wide-field motion-sensitive neurones tuned to horizontal movement in the honeybee, Apis mellifera. J Comp Physiol [A] 168:91–102

    Article  Google Scholar 

  • Ibbotson M, Goodman L (1990) Response characteristics of four wide-field motion-sensitive descending interneurones in Apis mellifera. J Exp Biol 148:255–279

    Google Scholar 

  • Jia X, Siegler M (2002) Midline lineages in grasshopper produce neuroneal siblings with asymmetric expression of engrailed. Development 129:5181–5193

    PubMed  CAS  Google Scholar 

  • Kanzaki R, Arbas E, Hildebrand J (1991) Physiology and morphology of descending neurones in pheromone-processing olfactory pathways in the male moth Manduca sexta. J Comp Physiol [A] 169:1–14

    CAS  Google Scholar 

  • Kent K, Hildebrand J (1987) Cephalic sensory pathways in the central nervous system of larval Manduca sexta (Lepidoptera: Sphingidae). Philos Trans R Soc Lond Biol 315:1–36

    PubMed  CAS  Google Scholar 

  • Kloppenburg P (1995) Anatomy of the antennal motoneurones in the brain of the honeybee (Apis mellifera). J Comp Neurol 363:333–343

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lafon-Cazal M, Bockaert J (1985) Pharmacological characterization of octopamine sensitive adenylate cyclase in the flight muscle of Locusta migratoria L. Eur J Pharmacol 119:53–59

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Menzel R, Bitterman ME (1983) Learning by honey bees in an unnatural situation. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology: roots and growing points. Springer, Berlin Heidelberg New York, pp 206–215

    Google Scholar 

  • Menzel R, Müller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404

    Article  PubMed  CAS  Google Scholar 

  • Menzel R, Heyne A, Gerber B, Fiala A (1999) Pharmacological dissociation between the reinforcing, sensitizing and response releasing functions of reward in honeybee classical conditioning. Behav Neurosci 113:744–754

    Article  PubMed  CAS  Google Scholar 

  • Mobbs P (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond Biol 298:309–354

    Google Scholar 

  • Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V (1995) Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356:275–287

    Article  PubMed  CAS  Google Scholar 

  • Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol [A] 188:359–370

    Article  Google Scholar 

  • Nambu J, Lewis J, Crews S (1993) The development and function of the Drosophila CNS midline cells. Comp Biochem Physiol [A 104:399–409

    Article  CAS  Google Scholar 

  • Nässel D, Högmo O, Hallberg E (1984) Antennal receptors in the blowfly Calliphora erythrocephala. I. The gigantic central projection of the pedicellar campaniform sensillum. J Morphol 180:159–169

    Article  Google Scholar 

  • Nishikawa M, Yokohari F, Ishibashi T (1995) Central projections of the antennal cold receptor neurones and hygroreceptor neurones of the cockroach Periplaneta americana. J Comp Neurol 361:165–176

    Article  PubMed  CAS  Google Scholar 

  • Orchard I, Lange A (1985) Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol 16:171–181

    Article  PubMed  CAS  Google Scholar 

  • O’Shea M, Rowell C, Williams J (1974) The anatomy of a locust visual interneurone; the descending contralateral movement detector. J Exp Biol 60:1–12

    Google Scholar 

  • Pankiw T, Page R (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J Comp Physiol [A] 189:675–684

    Article  CAS  Google Scholar 

  • Pareto A (1972) Die zentrale Verteilung der Fühlerafferenz bei Arbeiterinnen der Honigbiene, Apis mellifera. Z Zellforsch 131:109–140

    Article  PubMed  CAS  Google Scholar 

  • Pflüger H-J, Watson A (1988) Structure and distribution of dorsal unpaired median (DUM) neurones in the abdominal nerve cord of male and female locusts. J Comp Neurol 268:329–345

    Article  PubMed  Google Scholar 

  • Pribbenow B, Erber J (1996) Modulation of antennal scanning in the honeybee by sucrose stimuli, serotonin, and octopamine: behaviour and electrophysiology. Neurobiol Learn Mem 66:109–120

    Article  PubMed  CAS  Google Scholar 

  • Rehder V (1987) Zur Struktur und Funktion des Unterschlundganglions der Honigbiene, Apis mellifera. PhD thesis, FU Berlin

  • Rehder V (1988) A neuroanatomical map of the suboesophageal and the prothoracic ganglion of the honeybee (Apis mellifera). Proc R Soc Lond (Biol) 235:179–202

    Article  Google Scholar 

  • Rehder V (1989) Sensory pathways and motoneurones of the proboscisreflex in the suboesophageal ganglion of the honey bee. J Comp Neurol 279:499–513

    Article  PubMed  CAS  Google Scholar 

  • Rillich J, Stevenson P, Schildberger K (2001) The mandibular motor system of the cricket. Thieme, Stuttgart

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rohlfing T, Brandt R, Maurer CR, Menzel R (2001) Bee brains, b-splines and computational democracy: generating an average shape atlas. In: Proceedings of the IEEE Workshop on Mathematical Methods in Biomedical Image Analysis, MMBIA 2001, Kauai, Hawaii

  • Rybak J, Jennett A, Brandt R, Malun D (2001) Cellular localization of octopamine-like immunoreactivity in the honeybee brain. Sixth International Congress of Neuroethology, July 29-August 3, University of Bonn, abstract no. 339

  • Sandoz J-C, Hammer M, Menzel R (2002) Side-specificity of olfactory learning in the honeybee: US input side. Learn Mem 9:337–348

    Article  PubMed  Google Scholar 

  • Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136:545–553

    Article  PubMed  CAS  Google Scholar 

  • Scheiner R, Kuritz-Kaiser A, Menzel R, Erber J (2005) Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees. Learn Mem 12:626–635

    Article  PubMed  Google Scholar 

  • Schmid A, Chiba A, Doe C (1999) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653–4689

    PubMed  CAS  Google Scholar 

  • Schröter U, Malun D (2000) Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, Apis mellifera.J Comp Neurol 422:229–245

    Article  PubMed  Google Scholar 

  • Schröter U, Menzel R (2003) A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract.J Comp Neurol 465:168–178

    Article  PubMed  Google Scholar 

  • Schulz D, Robinson G (2001) Octopamine influences division of labor in honeybee colonies. J Comp Physiol [A] 187:53–61

    Article  CAS  Google Scholar 

  • Schulz D, Barron A, Robinson G (2002) A role for octopamine in honey bee division of labor. Brain Behav Evol 60:350–359

    Article  PubMed  Google Scholar 

  • Smid H, Bleeker M, Loon J van, Vet L (2003) Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell Tissue Res 312:237–248

    PubMed  Google Scholar 

  • Stern M, Thompson K, Zhou P, Watson D, Midgley J, Gewecke M, Bacon J (1995) Octopaminergic neurones in the locust brain: morphological, biochemical and electrophysiological characterization of potent modulators of the visual system. J Comp Physiol [A] 177:611–625

    CAS  Google Scholar 

  • Stevenson P (1999) Colocalisation of taurine- with transmitter-immunoreactivities in the nervous system of the migratory locust. J Comp Neurol 404:86–96

    Article  PubMed  CAS  Google Scholar 

  • Stevenson P, Meuser S (1997) Octopaminergic innervation and modulation of a locust flight steering muscle. J Exp Biol 200:633–642

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stevenson P, 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 

  • Strausfeld N, Bacon J (1983) Multimodal convergence in the central nervous system of dipterous insects. Fortschr Zool 28:47–76

    Google Scholar 

  • Suzuki H (1975) Antennal movements induced by odour and central projection of the antennal neurones in the honey-bee. J Insect Physiol 21:831–847

    Article  Google Scholar 

  • Thompson K, Siegler M (1991) Anatomy and physiology of spiking local and intersegmental interneurones in the median neuroblast lineage of the grasshopper. J Comp Neurol 305:659–675

    Article  PubMed  CAS  Google Scholar 

  • Thompson K, Siegler M (1993) Development of segment specificity in identified lineages of the grasshopper CNS. J Neurosci 13:3309–3318

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yasuyama K, Meinertzhagen I, Schürmann F (2003) Synaptic connections of cholinergic antennal lobe relay neurones innervating the lateral horn neuropile in the brain of Drosophila melanogaster. J Comp Neurol 466:299–315

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Drs. Michael Ibbotson and Jürgen Rybak for helpful comments on the manuscript and to Dr. Jürgen Rybak for his contributions to the improvement of the figures. We also thank Malte Westerhoff for his cooperation regarding the development of important Amira tools for the three-dimensional reconstruction of single neurones, and Mary Wurm for her help with the English.

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Correspondence to Randolf Menzel.

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This work was supported by the DFG ME 365/24-2.

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Schröter, U., Malun, D. & Menzel, R. Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327, 647–667 (2007). https://doi.org/10.1007/s00441-006-0197-1

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