A reconsideration of the central pattern generator concept for locust flight

Stevenson, Paul A.; Kutsch, W.

doi:10.1007/bf00609460

Cited by 116 publications

(50 citation statements)

References 31 publications

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“…This effect depends on flight duration and gradually wanes, following a time course similar to the transient elevation in octopamine hemolymph levels that occurs after flight in crickets and other orthopterans (Goosey and Candy, 1980;Bailey et al, 1983). The maximum octopamine hemolymph level (57 pg/l or 3 ϫ 10 Ϫ7 M) is, however, unlikely to affect aggression, because only higher concentrations influence the CNS (locusts, 10 Ϫ1 M) (Stevenson and Kutsch, 1987;Roeder et al, 1998) because of the bloodbrain barrier (Schofield et al, 1984). Although honeybees are influenced by fed (Schulz and Robinson, 2001) or injected octopamine (1 l; 10 mM) (Scheiner et al, 2002), cricket aggression was unaffected by octopamine injected at concentrations equal or exceeding that in the hemolymph after flying (Fig.…”

Section: Flight Fight and Octopaminementioning

confidence: 99%

Octopamine and Experience-Dependent Modulation of Aggression in Crickets

Stevenson¹,

Dyakonova²,

Rillich³

et al. 2005

J. Neurosci.

217

216

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Intraspecific aggression is influenced in numerous animal groups by the previous behavioral experiences of the competitors. The underlying mechanisms are, however, mostly obscure. We present evidence that a form of experience-dependent plasticity of aggression in crickets is mediated by octopamine, the invertebrate counterpart of noradrenaline. In a forced-fight paradigm, the experience of flying maximized the aggressiveness of crickets at their first encounter and accelerated the subsequent recovery of aggressiveness of the normally submissive losers, without enhancing general excitability as evaluated from the animals' startle responses to wind stimulation. This effect is transitory and concurrent with the activation of the octopaminergic system that accompanies flight. Hemocoel injections of the octopamine agonist chlordimeform (CDM) had similar effects on aggression but also enhanced startle responses. Serotonin depletion, achieved using ␣-methyl-tryptophan, enhanced startle responses without influencing aggression, indicating that the effect of CDM on aggression is not attributable to increased general excitation. Contrasting this, aggressiveness was depressed, and the effect of flying was essentially abolished, in crickets depleted of octopamine and dopamine using ␣-methyl-p-tyrosine (AMT). CDM restored aggressiveness in AMT-treated crickets, indicating that their depressed aggressiveness is attributable to octopamine depletion rather than to dopamine depletion or nonspecific defects. Finally, the flight effect was blocked in crickets treated with the octopamine receptor antagonist epinastine, or with the ␣-adrenoceptor and octopamine receptor antagonist phentolamine, but not with the ␤-adrenoceptor antagonist propranolol. The idea that activity-specific induction of the octopaminergic system underlies other forms of experiencedependent plasticity of aggressive motivation in insects is discussed.

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Section: Flight Fight and Octopaminementioning

confidence: 99%

Octopamine and Experience-Dependent Modulation of Aggression in Crickets

Stevenson¹,

Dyakonova²,

Rillich³

et al. 2005

J. Neurosci.

217

216

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“…Although acute application of OA is sufficient to elicit flight in a number of different insect preparations (Sombati and Hoyle, 1984;Claassen and Kammer, 1986;Stevenson and Kutsch, 1987;Duch and Pflueger, 1999), OA is not necessary for the initiation of flight in Drosophila but modulates flight initiation and maintenance. Even flies without any OA/TA-containing neurons can fly.…”

Section: Oa Is Not Required For Flight Initiationmentioning

confidence: 99%

“…In principle, both could be controlled by aminergic action on the CPG and/or on the fly's sensory system. It is well established that OA acts on the CPG in a number of insect species (Sombati and Hoyle, 1984;Claassen and Kammer, 1986;Stevenson and Kutsch, 1987), but central actions of TA are not known. OA has also been reported to increase the responsiveness of flight-associated sensory cells in insects (Ramirez and Orchard, 1990), and TA could conceivably reduce excitability of sensory neurons as Drosophila TARs activate chloride currents (Cazzamali et al, 2005).…”

Section: Sites Of Oa and Ta Actionmentioning

confidence: 99%

Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels

Brembs

Christiansen²,

Pflüger³

et al. 2007

J. Neurosci.

148

147

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Insect flight is one of the fastest, most intense and most energy-demanding motor behaviors. It is modulated on multiple levels by the biogenic amine octopamine. Within the CNS, octopamine acts directly on the flight central pattern generator, and it affects motivational states. In the periphery, octopamine sensitizes sensory receptors, alters muscle contraction kinetics, and enhances flight muscle glycolysis. This study addresses the roles for octopamine and its precursor tyramine in flight behavior by genetic and pharmacological manipulation in Drosophila. Octopamine is not the natural signal for flight initiation because flies lacking octopamine [tyramine-␤-hydroxylase (T␤H) null mutants] can fly. However, they show profound differences with respect to flight initiation and flight maintenance compared with wild-type controls. The morphology, kinematics, and development of the flight machinery are not impaired in T␤H mutants because wing-beat frequencies and amplitudes, flight muscle structure, and overall dendritic structure of flight motoneurons are unaffected in T␤H mutants. Accordingly, the flight behavior phenotypes can be rescued acutely in adult flies. Flight deficits are rescued by substituting octopamine but also by blocking the receptors for tyramine, which is enriched in T␤H mutants. Conversely, ablating all neurons containing octopamine or tyramine phenocopies T␤H mutants. Therefore, both octopamine and tyramine systems are simultaneously involved in regulating flight initiation and maintenance. Different sets of rescue experiments indicate different sites of action for both amines. These findings are consistent with a complex system of multiple amines orchestrating the control of motor behaviors on multiple levels rather than single amines eliciting single behaviors.

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“…One of the first identified CPGs underlies flight in locusts (Wilson, 1961;Edwards, 2006). This CPG can be experimentally activated in the isolated nervous system of adult and larval locusts by octopamine (Stevenson and Kutsch, 1987;Stevenson and Kutsch, 1988), which induces plateau potentials in flight interneurones (Ramirez and Pearson, 1991). Octopamine, the invertebrate analogue of noradrenaline (Evans, 1985;Roeder, 1999), is now generally accredited with playing a primary role in flight initiation (for reviews, see Orchard et al, 1993;Libersat and Pflüger, 2004).…”

Section: Introductionmentioning

confidence: 99%

A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight

Buhl

Schildberger

Stevenson

2008

Journal of Experimental Biology

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SUMMARYA central question in behavioural control is how central pattern generators (CPGs) for locomotion are activated. This paper disputes the key role generally accredited to octopamine in activating the CPG for insect flight. In deafferented locusts, fictive flight was initiated by bath application of the muscarinic agonist pilocarpine, the acetylcholine analogue carbachol, and the acetylcholinesterase blocker eserine, but not by nicotine. Furthermore, in addition to octopamine, various other amines including dopamine, tyramine and histamine all induced fictive flight, but not serotonin or the amine-precursor amino acid tyrosine. However, flight initiation was not reversibly blocked by aminergic antagonists, and was still readily elicited by both natural stimulation (wind) and pilocarpine in reserpinized, amine-depleted locusts. By contrast, the muscarinic antagonists atropine and scopolamine reversibly blocked flight initiated by wind, cholinergic agonists, octopamine, and by selective stimulation of a flightinitiating interneurone (TCG). The short delay from TCG stimulation to flight onset suggests that TCG acts directly on the flight CPG, and accordingly that TCG, or its follower cell within the flight generating circuit, is cholinergic. We conclude that acetylcholine acting via muscarinic receptors is the key neurotransmitter in the mechanism underlying the natural activation of the locust flight CPG. Amines are not essential for this, but must be considered as potential neuromodulators for facilitating flight release and tuning the motor pattern. We speculate that muscarinic activation coupled to aminergic facilitation may be a general feature of behavioural control in insects for ensuring conditional recruitment of individual motor programs in accordance with momentary adaptive requirements.

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A reconsideration of the central pattern generator concept for locust flight

Cited by 116 publications

References 31 publications

Octopamine and Experience-Dependent Modulation of Aggression in Crickets

Octopamine and Experience-Dependent Modulation of Aggression in Crickets

Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels

A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight

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