Abstract
We have tested the effect of a known insect neuromodulator, octopamine, on flight initiation in the cockroach. Using minimally dissected animals, we found that octopamine lowered the threshold for windevoked initiation of flight when applied to either of two major synaptic sites in the flight circuitry: 1) the last abdominal ganglion, where wind-sensitive neurons from the cerci excite dorsal giant interneurons, or 2) the metathoracic ganglion, where the dorsal giant interneurons activate interneurons and motoneurons which are involved in producing the rhythmic flight motor pattern in the flight muscles (Fig. 2).
Correlated with this change in flight initiation threshold, we found that octopamine applied to the last abdominal ganglion increased the number of action potentials produced by individual dorsal giant interneurons when recruiting the cereal wind-sensitive neurons with wind puffs (Figs. 3, 4, 5) or with extracellular stimulation of their axons (Fig. 6). Octopamine increases the excitability of the giant interneurons (Figs. 7, 8). Also, when we stimulated individual dorsal giant interneurons intracellularly, the number of action potentials needed to initiate flight was reduced when octopamine was applied to the metathoracic ganglion (Fig. 9).
Similar content being viewed by others
Abbreviations
- EMG :
-
electromyogram
- dGIs :
-
dorsal giant interneurons
- GI :
-
giant interneuron
- A6 :
-
sixth abdominal ganglion
- T3 :
-
third thoracic ganglion
- EPSP :
-
excitatory postsynaptic potential
References
Bellah KL, Fitch GK, Kammer AE (1984) A central action of octopamine on ventilation frequency in Corydalus cornutus. J Exp Zool 231: 289–292
Bicker G, Menzel R (1989) Chemical codes for the control of behavior in arthropods. Nature 337: 33–39
Blagburn JM, Sattelle DB (1987) Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach, Periplaneta americana. J Exp Biol 127: 135–157
Camhi JM (1984) A case study in neuroethology: The escape system of the cockroach. In: Camhi JM (ed) Neuroethology. Sinauer Associates Inc., Sunderland Massachusetts, pp 79–105
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
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
Collins C, Miller T (1977) Studies on the action of biogenic amines on cockroach heart. J Exp Biol 67: 1–15
Daley DL, Vardi N, Appignani B, Camhi J (1981) Morphology of the giant interneurons and cereal nerve projections of the American cockroach. J Comp Neurol 196: 41–52
Davenport AP, Evans PD (1984) Stress-induced changes in the octopamine levels of insect haemolymph. Insect Biochem 14: 135–143
David JC, Coulon JF, Lafon-Cazal M (1985) Octopamine changes in nervous and non-nervous tissues of the locust, Locusta migratoria L., after different flight conditions. Comp Biochem Physiol C 82: 427–432
Eckert M, Rapus J, Nurnberger A, Penzlin H (1992) A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322: 1–15
Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15: 317–473
Evans PD, Siegler MVS (1982) Octopamine mediated relaxation of maintained and catch tension in locust skeletal muscle. J Physiol (Lond) 324: 93–112
Glanzman DL, Krasne FB (1983) Serotonin and octopamine have opposite modulatory effects on the crayfish's lateral giant escape reaction. J Neurosci 3: 2263–2269
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
Goosey MW, Candy DJ (1980) The D-octopamine content of the haemolymph of the locust, Schistocerca americana gregaria and its elevation during flight. Insect Biochem 10: 393–397
Hirashima A, Eto M (1993) Effect of stress on levels of octopamine, dopamine and serotonin in the American cockroach (Periplaneta americana L.). Comp Biochem Physiol C 105: 279–284
Hoyle G, Dagan D (1978) Physiological characteristics and reflex activation of DUM (octopaminergic) neurons of locust metathoracic ganglion. J Neurobiol 9: 59–79
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
Kloppenburg P, Hildebrand JG (1995) Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta. J Exp Biol 198: 603–611
Libersat F (1992) Modulation of flight by the giant interneurons of the cockroach. J Comp Physiol A 170: 379–392
Libersat F (1994) The dorsal giant interneurons mediate evasive behavior in flying cockroaches. J Exp Biol 197: 405–411
Libersat F, Levy A, Camhi JM (1989) Multiple feedback loops in the flying cockroach: Excitation of the dorsal and inhibition of the ventral giant interneurons. J Comp Physiol A 165: 651–668
Long TF, Murdock LL (1983) Stimulation of blowfly feeding behavior by octopaminergic drugs. Proc Natl Acad Sci USA 80: 4159–4163
Malamud JG, Mizisin AP, Josephson RK (1988) The effects of octopamine on contraction kinetics and power output of a locust flight muscle. J Comp Physiol A 162: 827–835
Mercer AR, Hayashi JH, Hildebrand JG (1995) Modulatory effects of 5-hydroxytryptamine on voltage-activated currents in cultured antennal lobe neurons of the sphinx moth Manduca sexta. J Exp Biol 198: 613–627
Orchard I (1982) Octopamine in insects: neurotransmitter, neurohormone, and neuromodulator. Can J Zool 60: 659–669
Orchard I, Lange AB (1985) Dual role for octopamine in the control of haemolymph lipid during flight in Locusta. In: Gewecke M, Wendler G (eds) Insect locomotion. Parey, Berlin, pp 131–138
Orchard I, Ramirez JM, Lange AB (1993) A multifunctional role for octopamine in locust flight. Annu Rev Entomol 38: 227–249
Pollack AJ, Ritzmann RE, Westin J (1988) Activation of DUM cell interneurons by ventral giant interneurons in the cockroach Periplaneta americana. J Neurobiol 19: 489–497
Ramirez JM, Orchard I (1990) Octopaminergic modulation of the forewing stretch receptor in the locust Locusta migratoria. J Exp Biol 149: 255–279
Ramirez JM, Pearson K (1991) Octopamine induces bursting and plateau potentials in insect neurones. Brain Res 549: 332–337
Ritzmann RE (1984) The cockroach escape response. In: Eaton R (ed) Neural mechanisms of startle behavior. Plenum Press, New York, pp 93–131
Ritzmann RE, Pollack AJ (1986) Identification of thoracic interneurons that mediate giant interneurons-to-motor pathways in the cockroach. J Comp Physiol A 159: 639–654
Ritzmann RE, Pollack AJ, Tobias ML (1982) Flight activity mediated by intracellular stimulation of dorsal giant interneurons of the cockroach Periplaneta americana. J Comp Physiol 147: 313–322
Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53: 110–128
Selverston AI (1993) Neuromodulatory control of rhythmic behaviors in invertebrates. Internat Rev Cytology 147: 1–24
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
Stevenson PA, Kutsch W (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol A 161: 115–130
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
Washio H, Tanaka Y (1992) Some effects of octopamine, proctolin and serotonin on dorsal unpaired median neurons of cockroach (Periplaneta americana) thoracic ganglia. J Insect Physiol 38: 511–517
Weisel Eichler A, Libersat F (1994) Neuromodulation of flight initiation by octopamine. Proc Israel Society for Neuroscience, Third Annual Meeting, pp 27
Westin J, Langberg JJ, Camhi JM (1977) Responses of giant interneurons of the cockroach Periplaneta americana to wind puffs of different directions and velocities. J Comp Physiol 121: 307–324
Whim MD, Evans PD (1988) Octopaminergic modulation of flight muscle in the locust. J Exp Biol 134: 247–266
Yawo H, Kojima H, Kuno M (1985) Low threshold, slow inactivating Na+ potentials in the cockroach giant axon. J Neurophysiol 54: 1087–4100
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Weisel-Eichler, A., Libersat, F. Neuromodulation of flight initiation by octopamine in the cockroach Periplaneta americana . J Comp Physiol A 179, 103–112 (1996). https://doi.org/10.1007/BF00193438
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00193438