Skip to main content
SpringerLink
Log in

Differential effects of octopamine and tyramine on the central pattern generator for Manduca flight

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The biogenic amine, octopamine, modulates a variety of aspects of insect motor behavior, including direct action on the flight central pattern generator. A number of recent studies demonstrate that tyramine, the biological precursor of octopamine, also affects invertebrate locomotor behaviors, including insect flight. However, it is not clear whether the central pattern generating networks are directly affected by both amines, octopamine and tyramine. In this study, we tested whether tyramine affected the central pattern generator for flight in the moth, Manduca sexta. Fictive flight was induced in an isolated ventral nerve cord preparation by bath application of the octopamine agonist, chlordimeform, to test potential effects of tyramine on the flight central pattern generator by pharmacological manipulations. The results demonstrate that octopamine but not tyramine is sufficient to induce fictive flight in the isolated ventral nerve cord. During chlordimeform induced fictive flight, bath application of tyramine selectively increases synaptic drive to depressor motoneurons, increases the number of depressor spikes during each cycle and decreases the depressor phase. Conversely, blocking tyramine receptors selectively reduces depressor motoneuron activity, but does not affect cycle by cycle elevator motoneuron spiking. Therefore, octopamine and tyramine exert distinct effects on the flight central pattern generating network.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

CDM:

Chlordimeform

MN1-5:

Motoneurons 1-5

References

  • Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR (2005) Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46:247–260

    Article  PubMed  CAS  Google Scholar 

  • Baier A, Wittek B, Brembs B (2002) Drosophila as a model organism for the neurobiology of aggression. J Exp Biol 205:1233–1240

    PubMed  Google Scholar 

  • Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48(1):13–38

    Article  PubMed  CAS  Google Scholar 

  • Blenau W, Baumann A (2003) Aminergic signal transduction in invertebrates: focus on tyramine and octopamine receptors. Recent Res Dev Neurochem 6:225–240

    CAS  Google Scholar 

  • Bozic J, Woodring J (1998) Variations of brain biogenic amines in mature honeybees and induction of recruitment behavior. Comp Biochem Physiol A 120:737–744

    Article  Google Scholar 

  • Brembs B, Christiansen F, Pflueger HJ, Duch C (2007) Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J Neurosci 27(41):11122–11131

    Article  PubMed  CAS  Google Scholar 

  • Buhl E, Schildberger K, Stevenson PA (2008) A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J Exp Biol 211:2346–2357

    Article  PubMed  CAS  Google Scholar 

  • Cazzamali G, Klaerke DA, Grimmelikhuijzen CJP (2005) A new family of insect tyramine receptors. Biochem Biophys Res Commun 2:1189–1196

    Article  CAS  Google Scholar 

  • Chatwin HM, Rudling JE, Patel D, Reale V, Evans PD (2003) Site-directed mutagenesis studies on the Drosophila octopamine/tyramine receptor. Insect Biochem Mol Biol 33(2):173–184

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Degen J, Gewecke M, Roeder T (2000) Octopamine receptors in the honey bee and locust nervous system: pharmacological similarities between homologous receptors of distantly related species. Br J Pharmacol 130:587–594

    Article  PubMed  CAS  Google Scholar 

  • Duch C, Pflueger HJ (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 

  • Eaton JL (1988) Lepidopteran anatomy, Wiley, New York

  • Edwards JS (2006) The central nervous control of insect flight. J Exp Biol 209:4411–4413

    Article  PubMed  Google Scholar 

  • Evans PD, Maqueira B (2005) Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5(3–4):111–118

    Article  PubMed  CAS  Google Scholar 

  • Evans PD, O’Shea M (1979) An octopaminergic neuron modulates neuromuscular transmission in the locust. Nature 270:257–259

    Article  Google Scholar 

  • Fox LE, Soll DR, Wu CF (2006) Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine β hydroxylase mutation. J Neurosci 26:1486–1498

    Article  PubMed  CAS  Google Scholar 

  • Grillner S, Markram H, De Schutter E, Silberberg G, LeBeau FE (2005) Microcircuits in action—from CPGs to neocortex. Trends Neurosci 28:525–533

    Article  PubMed  CAS  Google Scholar 

  • Harris JW, Woodring J (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L) brain. J Insect Physiol 38:29–35

    Article  CAS  Google Scholar 

  • Hoyle G (1985) Generation of motor activity and control of behavior: the role of the neuromodulator octopamine and the orchestration hypothesis. In: Kerkut GA, Gilbert L (eds) Comp insect physiol, biochem pharmacol 5. Pergamon, Toronto, pp 607–621

    Google Scholar 

  • Johnston RM, Levine RB (2002) Thoracic leg motoneurons in the isolated CNS of adult Manduca produce patterned activity in response to pilocarpine, which is distinct from that produced in larvae. Invert Neurosci 4(4):175–192

    Article  PubMed  CAS  Google Scholar 

  • Kammer AE (1967) Muscle activity during flight in some large lepidoptera. J Exp Biol 47:277–295

    PubMed  CAS  Google Scholar 

  • Kiehn O, Kullander K (2004) Central pattern generators deciphered by molecular genetics. Neuron 41:317–321

    Article  PubMed  CAS  Google Scholar 

  • Kinnamon SC, Klaassen LW, Kammer AE, Claassen D (1984) Octopamine and chlordimeform enhance sensory responsiveness and production of the flight motor pattern in developing and adult moths. J Neurobiol 15:283–293

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi EA (2001) Role of catecholamine signaling in brain and nervous system functions: new insights from mouse molecular genetic study. J Investig Dermatol Symp Proc 6:115–121

    Article  PubMed  CAS  Google Scholar 

  • Kononenko NL, Wolfenberg H, Pflüger H-J (2008) Tyramine as an independent transmitter and a precursor of octopamine in the locust central nervous system: an immunocytochemical study. J Comp Neurol 512(4):433–542

    Article  CAS  Google Scholar 

  • Kravitz EA, Huber R (2003) Aggression in invertebrates. Curr Opin Neurobiol 13:736–743

    Article  PubMed  CAS  Google Scholar 

  • Lange AB (2008) Tyramine: from octopamine precursor to neuroactive chemicals in insects. Gen Comp Endocrinol (Epub ahead of print)

  • Leitch B, Judge S, Pitman RM (2003) Octopaminergic modulation of synaptic transmission between an identified sensory afferent and flight motoneuron in the locust. J Comp Neurol 462:55–70

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986–R996

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687–717

    PubMed  CAS  Google Scholar 

  • Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 6:R685–R699

    Article  CAS  Google Scholar 

  • Matheson T (1997) Octopamine modulates the responses and presynaptic inhibition of proprioceptive sensory neurones in the locust Schistocerca gregaria. J Exp Biol 200:1317–1325

    PubMed  CAS  Google Scholar 

  • McClung C, Hirsh J (1999) The trace amine tyramine is essential for sensitization to cocaine in Drosophila. Curr Biol 9:853–860

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mustard JA, Kurshan PT, Hamilton IS, Blenau W, Mercer AR (2005) Developmental expression of a tyramine receptor gene in the brain of the honey bee, Apis mellifera. J Comp Neurol 483:66–75

    Article  PubMed  CAS  Google Scholar 

  • Nagaya Y, Kutsukake M, Chigusa SI, Komatsu A (2002) A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster. Neurosci Lett 329:324–328

    Article  PubMed  CAS  Google Scholar 

  • Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E (2001) The roles of co-transmission in neural network modulation. Trends Neurosci 24:146–154

    Article  PubMed  CAS  Google Scholar 

  • Ohta H, Utsumi T, Ozoe Y (2003) B96Bom encodes a Bombyx mori tyramine receptor negatively coupled to adenylate cyclase. Insect Mol Biol 12:217–223

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pearson KG (2004) Generating the walking gait: role of sensory feedback. Prog Brain Res 143:123–129

    Article  PubMed  Google Scholar 

  • Pflüger H-J (1999) Neuromodulation during motor development and behavior. Curr Opin Neurobiol 9:683–689

    Article  PubMed  Google Scholar 

  • Pflüger H-J, Watson AHD (1995) GABA- and glutamate-like immunoreactivity in central synapses of dorsal unpaired median neurones in the abdominal nerve cord of locusts. Cell Tissue Res 280:325–333

    Article  PubMed  Google Scholar 

  • Pflüger H-J, Witten JL, Levine RB (1993) Fate of abdominal ventral unpaired median cells during metamorphosis of the hawkmoth, Manduca sexta. J Comp Neurol 335:508–522

    Article  PubMed  Google Scholar 

  • Popova NK (2006) From genes to aggressive behavior: the role of the serotonergic system. BioEssays 28:495–503

    Article  PubMed  CAS  Google Scholar 

  • Ramirez JM, Pearson KG (1991a) Octopaminergic modulation of interneurons in the flight system of the locust. J Neurophysiol 66(5):1522–1537

    PubMed  CAS  Google Scholar 

  • Ramirez JM, Pearson KG (1991b) Octopaminergic modulation of plateau potentials in the flight system of the locust. Brain Res 549:332–337

    Article  PubMed  CAS  Google Scholar 

  • Riemensperger T, Voller T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 16:1741–1747

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roeder T, Degen J, Gewecke M (1998) Epinastine, a highly specific antagonist of insect neuronal octopamine receptors. Eur J Pharmacol 349:171–177

    Article  PubMed  CAS  Google Scholar 

  • Saraswati S, Fox LE, Soll DR, Wu CF (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58:425–441

    Article  PubMed  CAS  Google Scholar 

  • Saudou F, Amlaiky N, Plassat JL, Borrelli E, Hen R (1990) Cloning and characterization of a Drosophila tyramine receptor. EMBO J 9:3611–3617

    PubMed  CAS  Google Scholar 

  • Scholtissen B, Verhey FR, Steinbusch HW, Leentjens AF (2006) Serotonergic mechanisms in Parkinson’s disease: opposing results from preclinical and clinical data. J Neural Transm 113:59–73

    Article  PubMed  CAS  Google Scholar 

  • Schulz DJ, Robinson GE (2001) Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53–61

    Article  PubMed  CAS  Google Scholar 

  • Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502

    PubMed  CAS  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 (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol A 161:115–129

    Article  Google Scholar 

  • Stevenson PA, Dyakonova V, Rillich J, Schildberger K (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25:1431–1441

    Article  PubMed  CAS  Google Scholar 

  • Taylor C, Fricker AD, Devi LA, Gomes I (2005) Mechanisms of action of antidepressants: from neurotransmitter systems to signaling pathways. Cell Signal 17:549–557

    Article  PubMed  CAS  Google Scholar 

  • Trimmer BA, Weeks JC (1989) Effects of nicotinic and muscarinic agents on an identified motoneuron and its direct afferent inputs in larval Manduca sexta. J Exp Biol 144:303–337

    Google Scholar 

  • Tu MS, Daniel TL (2004) Submaximal power output from the dorsolongitudinal flight muscles of the hawkmoth, Manduca sexta. J Exp Biol 207:4651–4662

    Article  PubMed  Google Scholar 

  • Vanden Broeck J, Vulsteke V, Huybrechts R, De Loof A (1995) Characterization of a cloned locust tyramine receptor cDNA by functional expression in permanently transformed Drosophila S2 cells. J Neurochem 64:2387–2395

    Article  Google Scholar 

  • Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471–479

    Article  PubMed  CAS  Google Scholar 

  • Wilson DM (1961) The central nervous control of locust flight. J Exp Biol 38:471–490

    Google Scholar 

  • Wilson DM (1966) Central nervous mechanisms for the generation of rhythmic behavior in arthropods. Symp Soc Exp Biol 20:199–228

    PubMed  CAS  Google Scholar 

  • Wilson DM, Wyman RJ (1965) Motor output patterns during random and rhythmic stimulation of locust thoracic ganglia. Biophys J 5:121–143

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

R. Vierk was supported by DFG Graduate College, GRK 837 (Functional Insect Science). The experiments comply with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of Germany where the experiments were performed.

Author information

Authors and Affiliations

  1. Institute of Biology/Neurobiology, Free University of Berlin, 14195, Berlin, Germany

    R. Vierk & H. J. Pflueger

  2. School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA

    C. Duch

Authors
  1. R. Vierk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. J. Pflueger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Duch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Duch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vierk, R., Pflueger, H.J. & Duch, C. Differential effects of octopamine and tyramine on the central pattern generator for Manduca flight. J Comp Physiol A 195, 265–277 (2009). https://doi.org/10.1007/s00359-008-0404-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0404-5

Keywords

Search

Navigation