Journal of Insect Physiology 63 (2014) 1–8

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Octopamine modulates a central pattern generator associated with egg-laying in the locust, Locusta migratoria Raymond Wong 1, Angela B. Lange ⇑ University of Toronto Mississauga, Department of Biology, 3359 Mississauga Rd., Mississauga, ON L5L 1C6, Canada

a r t i c l e

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Article history: Received 5 November 2013 Received in revised form 30 January 2014 Accepted 5 February 2014 Available online 13 February 2014 Keywords: Amine Egg-laying Digging Oviposition Protractor muscle Oviduct

a b s t r a c t Egg-laying in Locusta migratoria involves the control of a variety of complex behavioural patterns including those that regulate digging of the oviposition hole and retention of eggs during digging. These two behavioural patterns are under the control of central pattern generators (CPGs). The digging and egg-retention CPGs are coordinated and integrated with overlapping locations of neural substrate within the VIIth and VIIIth abdominal ganglia of the central nervous system (CNS). In fact, the egg-retention CPG of the VIIth abdominal ganglion is involved in both egg-retention and protraction of the abdomen during digging. The biogenic amine, octopamine, has peripheral effects on oviduct muscle, relaxing basal tension of the lateral and upper common oviduct and enabling egg passage. Here we show that octopamine also modulates the pattern of the egg-retention CPG by altering the motor pattern that controls the external ventral protractor of the VIIth abdominal segment. There is no change in the motor pattern that goes to the oviducts. Octopamine decreased the frequency of the largest amplitude action potential and decreased burst duration while leading to an increase in cycle duration and interburst interval. The effects of octopamine were greatly reduced in the presence of the a-adrenergic blocker, phentolamine, indicating that the action of octopamine was via a receptor. Thus, octopamine orchestrates events that can lead to oviposition, centrally inhibiting the digging behavior and peripherally relaxing the lateral and common oviducts to enable egg-laying. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Insects have proven valuable experimental models for studying the neural basis of behaviour (Grillner, 1975; Delcomyn, 1980); in particular, neurophysiological studies of rhythmic behaviour patterns such as walking, flight, and oviposition have been particularly rewarding (Ayali and Lange, 2010; Pearson, 2000). Many of these rhythmic patterns are generated and controlled by the central nervous system (CNS) using discrete neural circuits/networks. These central pattern generators (CPGs) have been extensively studied at the molecular, cellular and circuit levels and shown to generate rhythms in the absence of any patterned sensory or descending input (Ayali and Lange, 2010; Marder et al., 2005; Marder and Bucher, 2007; Pearson, 2000). Having said that, however, it is clear that sensory information/feedback is necessary for making the CPG network fully functional and context dependent and that these networks are targets for modulation by amines ⇑ Corresponding author. Tel.: +1 905 828 3972; fax: +1 905 828 3792. E-mail address: [email protected] (A.B. Lange). Present address: Toronto Western Research Institute, University Health Network, Department of Physiology, University of Toronto, Toronto, ON, Canada. 1

http://dx.doi.org/10.1016/j.jinsphys.2014.02.002 0022-1910/Ó 2014 Elsevier Ltd. All rights reserved.

and neuropeptides (Kravitz, 1988; Bicker and Menzel, 1989; Marder, 2012). Thus, the CPGs are not static but show plasticity and are able to generate varying outputs (Marder, 2012; Marder et al., 2005). In addition, CPGs may not be entirely independent of each other and may even be coupled to each other (see Rillich et al., 2013). The female locust, Locusta migratoria, lays fertilized eggs in an oviposition site (hole). Digging this hole involves rhythmic movements of the ovipositor valves that are under the control of a CPG whose circuit is located within the VIIth and VIIIth abdominal ganglia (Thompson, 1986a,b). During digging, the mature eggs are held in the lateral oviducts by rhythmic constriction of the lower lateral oviducts, whilst contractions of the upper lateral oviducts tend to propel them posteriorly towards the common oviduct (Lange et al., 1984; Facciponte and Lange, 1992, 1996). An egg-retention CPG, located in the VIIth abdominal ganglion, provides motor output that constricts the lower lateral oviducts and stimulates protraction of the abdomen during digging (Lange et al., 1984; Lange, 2009a,b; Ayali and Lange, 2010). This CPG is necessary and essential to ensure that the eggs are not deposited before the oviposition hole is fully excavated or in case the female is disturbed during egglaying and needs to find another suitable oviposition site. Both the

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digging CPG and the egg retention CPG are under descending neural inhibition and can be activated by transecting the nerve cord anteriorly to the neural substrate (Thompson, 1986a,b; Lange et al., 1984; Facciponte et al., 1995) and both of these CPGs are integrated and coordinated to allow for the retention of eggs during digging of the oviposition hole (Facciponte et al., 1995). Neuromodulators influence CPGs centrally, and/or influence peripheral sensory feedback onto the CPGs (see Marder, 2012). Recently the biogenic amine, octopamine, was found to evoke fictive flight in locusts and it was suggested that octopamine biases the motor network towards flight (Rillich et al., 2013). This is interesting since octopamine is also associated with egg-laying in L. migratoria and in Drosophila melanogaster (see Lange, 2009b; Rubinstein and Wolfner, 2013). Thus, octopamine, released from dorsal unpaired median (DUM) neurons inhibits contractions of the lateral oviducts in L. migratoria which relaxes the muscles enabling egg passage and oviposition (see Lange, 2009b; Cheung et al., 1994). A similar suggestion has been made in D. melanogaster where octopamine stimulates ovulation, and relaxes oviduct muscle tonus (Rubinstein and Wolfner, 2013). In light of octopamine’s action on peripheral tissues such as the oviducts during egg-laying, we questioned whether octopamine might centrally modulate the egg-retention CPG in the locust, L. migratoria. This would be appropriate at the time when octopamine is released peripherally to relax the oviducts during egg-laying allowing the passage of eggs

– a time when digging is completed and the egg-retention CPG is no longer required. Here we describe the effects of octopamine on the egg-retention CPG of the VIIth abdominal ganglion, and find that it does indeed modulate this CPG, by inhibiting several of its parameters. 2. Materials and methods 2.1. Animals Experiments were carried out on 7-week-old sexually mature female L. migratoria reared under crowded conditions at 30 °C and 50% humidity. Locusts were kept on a 12 h:12 h light:dark regime, and were given a diet of fresh wheat seedlings supplemented with bran. 2.2. Preparation Preparations were dissected and maintained in locust physiological saline (150 mM NaCl; 10 mM KCl; 4 mM CaCl2; 2 mM MgCl2; 3 mM NaHCO3; 5 mM HEPES, pH 7.2; 90 mM sucrose; 5 mM trehalose). The dissection consisted of the last three abdominal ganglia with the oviducts (both common oviduct and lateral oviducts) connected to the VIIth abdominal ganglion via the oviducal nerves (sternal nerve branches N2B of VIIth abdominal

Fig. 1. Extracellular recordings of neural activity in the oviducal nerve of L. migratoria from an isolated preparation of the VIIth and VIIIth abdominal ganglia in saline. (A) Characteristic rhythmic motor bursting pattern. Expanded portion of the upper trace is shown in (B) and (C) to show individual spikes and bursting pattern. Note three discernable sizes of action potentials; spike 1, 2, and 3 refer to the large, medium, and small amplitude action potentials respectively (n = 10).

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ganglion). All segmental nerves aside from the oviducal nerves were severed. The preparation was transferred to a Sylgard-coated dish and secured with insect minutien pins, taking care to avoid direct contact with the VIIth abdominal ganglion. The oviducal nerves were cut and the oviducts removed. This allowed for recordings to be made using suction electrodes from the oviducal nerves. The neural sheath of the VII abdominal ganglion was peeled off using fine forceps. To remove the descending inhibition and allow the CPG to be initiated the connectives between the VIth and VIIth abdominal ganglia were severed leaving the VIIth abdominal ganglion attached to the VIIIth abdominal ganglion (Facciponte et al., 1995). The CPG characteristic rhythmic motor bursting pattern with three distinguishable amplitudes of action potentials was observed in 10 out of 23 preparations. Only preparations that had the CPG initiated were used for the following experiments. The preparations displaying rhythmic neural activity in saline remained viable for up to 4 h. Octopamine and/or phentolamine was added (while simultaneously removing saline) to the preparation for a duration of 3 min. The preparations were washed thoroughly with saline after application of octopamine or phentolamine or both. 2.3. Neurophysiological recordings Extracellular recordings of electrical activity from the oviducal nerve (N2B) were carried out using glass suction electrodes. Recordings were obtained from either the cut end of an oviducal nerve and pre-amplified and filtered (band-pass filter 300–1000 Hz) via AM Systems (Everett, WA, USA) differential AC amplifier (model 1700). The recordings were displayed using a Powerlab computer-based acquisition system (ADInstruments, Colorado Springs, CO, USA) and the software LabChart 6 Pro was used for data storage and analysis. 2.4. Data analysis Phase analysis for each distinct amplitude of action potential (spikes 1–3) was performed by measuring the cycle duration, the burst duration, interburst interval and frequency of action potentials within a burst for three minutes prior to treatment and for three minutes after with octopamine or phentolamine or both. Cycle duration was measured from the beginning of the first action potential in a burst to the beginning of the next burst of the same size spike. The start of an interburst (or end of a burst) was determined when the time between the last action potential of a burst and the next action potential was significantly longer than the average interval between action potentials within the burst. The same parameter was used (in reverse) to determine the start of a burst (or end of an interbust). Statistical analyses via Graphpad Prism were performed using two-way ANOVAs with Tukey’s post hoc test. 3. Results Previous work has demonstrated that an egg-retention CPG is present in the VIIth abdominal ganglion and projects to the oviducts and the external ventral protractor muscles (M234) of the VIIth abdominal ganglion of the locust, L. migratoria (Facciponte and Lange, 1992, see Lange, 2009a,b). This rhythmic motor pattern is comprised of predominantly three discernible sizes of action potentials that can be recorded from disturbed egg-layers but not from non-egg-layers. This CPG has been shown to be under the control of descending inhibition (Facciponte and Lange, 1992, 1996; see Lange, 2009a,b). Electrophysiological recordings from the oviducal nerve in isolated VIIth abdominal

Fig. 2. Octopamine dose-dependently decreases spike frequency of the neural activity recorded from the oviducal nerve of L. migratoria in an isolated preparation consisting of the VIIth and VIIIth abdominal ganglia. (A) Bar indicates the addition of saline or varying concentrations of octopamine. Arrow indicates removal of octopamine by washing with saline. Note the decrease in frequency of the action potentials in the presence of octopamine. (n = 7). (B) Histogram of the frequency of spike 1 (largest amplitude spike) measured over the last 2 min of octopamine application. One-Way ANOVA with Tukey post hoc test. represents significant difference with control (⁄⁄⁄P < 0.001; ⁄⁄⁄⁄P < 0.0001).  represents significance between groups (  P < 0.01;     P < 0.0001). Sample size indicated in white numbers on histograms. Error bars represent mean ± SEM.

ganglia confirmed this pattern, with action potentials of three discernable sizes, labeled as spike 1 for the large amplitude action potentials, spike 2 for the medium amplitude action potentials, and spike 3 for the small amplitude action potentials (Fig. 1). Both spike 1 and 3 have been shown to stimulate contractions of the external ventral protractor muscle of the VIIth abdominal ganglion and spike 2 stimulates contraction of the oviducts allowing eggretention to be coordinated with ovipositional digging (Facciponte and Lange, 1992; Facciponte et al., 1995). Spikes 1 and 3 burst in a co-ordinated way which is mutually exclusive to spike 2 (Facciponte and Lange, 1992). Much smaller action potentials are occasionally seen in the background which are likely from the DUM neurons. These show no obvious rhythmic bursting pattern (see Facciponte and Lange, 1992). Addition of the biogenic amine, octopamine, to the VIIth abdominal ganglion led to a dose-dependent decrease in the frequency of action potentials recorded from the oviducal nerves

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Fig. 3. Octopamine decreases spike frequency whereas the a-adrenergic antagonist phentolamine has no effect on the spike frequency in recordings from the oviducal nerve of an isolated preparation of the VIIth and VIIIth abdominal ganglia. Bar indicates the addition of (A) octopamine (10 3 M) and (B) phentolamine (10 3 M). Arrow indicates removal of test chemical by washing with saline (n = 23).

(Fig. 2). This effect was observed in 7 out of the 9 preparations tested. In an attempt to determine if this inhibitory effect of octopamine on the frequency of action potentials was via a classical receptor we used the a-adrenergic blocker, phentolamine, which has been shown to be a very effective antagonist of octopamine at the locust oviducts (Orchard and Lange, 1986). Phentolamine on its own had no effect on action potential frequency (Fig. 3) but was capable of decreasing the inhibition produced by octopamine (Fig. 4). Quantitative analysis indicated that octopamine decreased the frequency of only the largest amplitude action potential, spike 1 (P < 0.05, ANOVA, Tukey’s post hoc test), while leaving spike 2 and spike 3 unchanged (ANOVA P > 0.05), when compared to the normal activity (i.e. when in saline, control) (Fig. 5). Phentolamine greatly reduced the effects of octopamine on spike 1 frequency (Fig. 5). To examine the effects of octopamine on other parameters of the egg retention pattern we also quantified cycle duration, burst duration, interburst interval and the frequency within the burst for all three spikes in the presence of octopamine and/or phentolamine (Figs. 6–8). In addition to the effects of octopamine on the frequency of spike 1, it also significantly increased cycle duration and interburst interval and significantly decreased burst duration (Fig. 6). Phentolamine was able to anatgonise all the effects of octopamine on the pattern (Fig. 6). None of the parameters examined for spike 2 or spike 3 were altered by octopamine (Figs. 7 and 8).

Fig. 5. Frequency of action potentials (APs) per minute as determined from the recordings of the neural activity from the oviducal nerve in the isolated preparation of the VIIth and VIIIth abdominal ganglia. Each wash or addition of drug was left for 3 min during recording and the last minute was used to analyze the frequency of each action potential. Spike 1 frequency was significantly reduced in the presence of octopamine (10 3 M) and addition of phentolamine (10 3 M) reduced the effects of octopamine. Octopamine had no effect of the frequency of either spike 2 of 3. (Data are mean ± S.E., n = 5; asterisks, P < 0.05 ANOVA and Tukey’s post hoc test; data for spikes 2 and 3 are non-significant, P > 0.05 ANOVA.)

Fig. 4. The a-adrenergic antagonist, phentolamine, blocks the effects of octopamine suggesting that the action of octopamine is via an a-adrenergic-type receptor. Bar denotes application of the test chemical and arrows indicate removal of the chemical by washing. (n = 5)

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Fig. 6. Time histogram analysis of the effects of octopamine and/or phentolamine on cycle duration, burst duration, interburst interval and frequency within a burst for spike 1 from neural activity recorded from the oviducal nerve in an isolated preparation of the VIIth and VIIIth abdominal ganglia. For this analysis, recordings were used from three individual locusts (represented by shading) that clearly displayed the rhythmic bursting motor pattern or the egg-retention CPG from the VIIth abdominal ganglion. Black bars denote the addition of 10 3 M octopamine, open bars denote the addition of 10 3 M phentolamine and no bars indicate preparation in saline, including washes. (Data are mean ± S.E., n = 3; P < 0.05 2-Way ANOVA with locusts as blocks to extract variance due to individual differences, P < 0.05 Tukey’s post hoc test; asterisks = ⁄⁄⁄⁄P < 0.0001, ⁄⁄⁄ P < 0.001, ⁄⁄P < 0.01, ⁄P < 0.05. Bars indicate significance level of a treatment, i.e. octopamine or octopamine + phentolamine and also indicate level of significance between octopamine alone and octopamine + phentolamine.)

4. Discussion Egg-laying in L. migratoria involves the control of a variety of complex behavioural patterns including those that regulate digging of the oviposition hole and retention of eggs during digging. Digging of the oviposition hole involves rhythmic movements of the ovipositor valves controlled via a digging CPG located in the VIIth and VIIIth abdominal ganglia (Thompson, 1986a,b). During digging the eggs are held in the lateral oviducts by rhythmic contractions of the lower lateral oviducts that propel the eggs

anteriorly towards the ovaries, thereby preventing their deposition (Lange et al., 1984). This rhythmic activity is under the control of the egg-retention CPG located in the VIIth abdominal ganglion (Facciponte and Lange, 1992). Interestingly, components of this egg-retention CPG also control the external ventral protractors of the VIIth abdominal ganglion thereby leading to reciprocal contractions of the oviducts and the protractor muscles of the VIIth abdominal ganglion (Facciponte and Lange, 1992). The digging and egg retention CPGs are both under descending neural inhibition and are coordinated and integrated with overlapping locations of

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Fig. 7. Time histogram analysis of the effects of octopamine and/or phentolamine on cycle duration, burst duration, interburst interval and frequency within a burst for spike 2 from neural activity recorded from the oviducal nerve in an isolated preparation of the VIIth and VIIIth abdominal ganglia. For this analysis, recordings were used from three individual locusts (represented by shading) that clearly displayed the rhythmic bursting motor pattern or the egg-retention CPG from the VIIth abdominal ganglion. Black bars denote the addition of 10 3 M octopamine, open bars denote the addition of 10 3 M phentolamine and no bars indicate preparation in saline or washes. Note that there was no significant changes in analysis of spike 2 for all of the parameters tested. (Data are mean ± S.E., n = 3, P > 0.05 2-Way ANOVA.)

neural substrate within the CNS (Thompson, 1986a,b; Facciponte and Lange, 1992, 1996; see Lange, 2009a,b). Therefore, during digging, CPG activity in the oviducal nerve drives contractions of the external ventral protractors of the VIIth abdominal ganglion which act in concert with the retractor and protractor muscles of the ovipositor valves in order to aid in digging (Facciponte and Lange, 1992), with one of the spikes also stimulating contractions of the oviducts. This coordination of the digging CPG and the egg-retention CPG demonstrates the importance of communication between pattern generators to orchestrate a behavior – in this case that of

digging, coordinated with egg-retention. Octopamine modifies the egg-retention CPG by altering the patterning of spike 1 which controls the external ventral protractor muscle of the VIIth abdominal ganglion with an increase in cycle duration and interburst interval and a decrease in burst duration and frequency of this large amplitude action potential. This change in pattern would lead to a decrease in contraction of the external ventral protractor muscle in the VIIth abdominal ganglion. The receptor antagonist phentolamine blocked the effects of octopamine suggesting that the mode of action was most likely via an a-adrenergic receptor.

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Fig. 8. Time histogram analysis of the effects of octopamine and/or phentolamine on cycle duration, burst duration, interburst interval and frequency within a burst for spike 3 from neural activity recorded from the oviducal nerve in an isolated preparation of the VIIth and VIIIth abdominal ganglia. For this analysis, recordings were used from three individual locusts (represented by shading) that clearly displayed the rhythmic bursting motor pattern or the egg-retention CPG from the VIIth abdominal ganglion. Black bars denote the addition of 10 3 M octopamine, open bars denote the addition of 10 3 M phentolamine and no bars indicate preparation in saline or washes. Note that there was no significant changes in analysis of spike 3 for all of the parameters tested. (Data are mean ± S.E., n = 3; P > 0.05 2-Way ANOVA.)

It is interesting to note that octopamine did not elicit any observable effect on these parameters for spikes 2 and 3. This means that spike 2 which controls contractions of the oviducts would not be altered by octopamine. Interestingly, spike 3 which stimulates weaker contraction of the external ventral protractor muscle (Facciponte et al., 1995) appears to not be affected by octopamine. Neuromodulators can influence CPGs both centrally and/or influence peripheral feedback onto the CPGs (see Ayali and Lange, 2010). In this study, octopamine was added to a fully isolated preparation that consisted only of the VIIth and VIIIth abdominal

ganglia and therefore its effects are central, most likely altering neural activity in neurons within the desheathed VIIth abdominal ganglion. Sombati and Hoyle (1984) were able to evoke flight behavior by locally releasing octopamine into specific regions of the neuropile of the locust metathoracic ganglion, i.e. via direct excitation of components of the motor neural circuit. They were also able to inhibit the rhythmic oviposition digging pattern by iontophoretic injection of octopamine into the neuropile of the VIth abdominal ganglion in the locust, Schistocerca gregaria, and conjectured that this simulated the natural descending inhibition

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controlling the digging CPG. Similarly, octopamine added to the VIIth abdominal ganglion of L. migratoria inhibits the rhythm of spike 1 by increasing cycle duration and interburst interval and deceasing burst duration and frequency; a consequence of which would be to reduce the frequency and amplitude of contractions of the external ventral protractor muscle in the VIIth abdominal segment. Therefore, octopamine, released centrally, may be involved in modulation or inhibition of neurons coordinating digging. Octopamine is not the only neuroactive chemical to influence the egg-retention CPG in the VIIth abdominal ganglion controlling the oviducts and the ventral protractor muscles. SchistoFLRFamide, perfused onto the VIIth abdominal ganglion, increases action potential frequency recorded from the oviducal nerves and resultant frequency of phasic oviduct contractions (Kwok and Orchard, 2002). Proctolin is also capable of altering the motor pattern produced by the egg-retention CPG when applied to the VIIth abdominal ganglion, resulting in changes in oviduct contraction (Kwok and Orchard, 2002). In addition, the pentapeptide proctolin has been shown to influence locust oviposition behavior both centrally and peripherally (Belanger and Orchard, 1993). Peripherally, proctolin is required for maintaining the tension of the ventral opener muscle during digging. Centrally the digging CPG declines in frequency in a totally isolated VIIIth abdominal ganglion and the original activity is restored by perfusion of the ganglion with proctolin. Belanger and Orchard (1993) suggested that proctolin is needed for the ‘‘functional integrity’’ of the digging CPG. Proctolin is also associated with the external ventral protractor muscle of the VIIth abdominal ganglion (Facciponte et al., 1995). The L. migratoria oviducts receive innervation from two octopaminergic DUM neurons lying in the posterior region of the VIIth abdominal ganglion of the locust (Orchard and Lange, 1985). These DUM neurons have bifurcating axons which project into the left and right oviducal nerves to innervate the lower lateral and upper common oviducts. The action potentials recorded extracellularly from their axons are quite small, relative to the 3 motor neurons. They also have extensive projections into the neuropile of the ganglion. The DUM neurons release octopamine onto the oviducts which acts via the second messenger cyclic AMP to inhibit neurally-evoked and spontaneous oviduct contractions, thereby peripherally relaxing muscle tonus (Orchard and Lange, 1986). Stimulation of these DUM neurons results in a reduction of the amplitude and frequency of oviducal contractions through peripheral release of octopamine onto the oviducts (Kalogianni and Theophilidis, 1993). DUM neurons have also been shown to project to the skeletal muscles involved in digging. It is tempting to speculate that octopamine might act counter to the egg-retention CPG; released peripherally to inhibit protractor muscles associated with digging and to relax oviduct muscle tonus to allow the passage of eggs; and released centrally to inhibit the CGP associated with digging. Thus octopamine orchestrates events that can lead to oviposition, stopping the digging behavior and relaxing the lateral and common oviducts thereby enabling egg-laying. It is interesting to observe that octopamine signaling is also an essential component of successful ovulation in Drosophila, with some parallels with L. migratoria, including central and peripheral octopamine receptors and octopamine-mediated relaxation of oviduct muscle tonus (Monastirioti, 2003; Lee et al., 2009; Rubinstein and Wolfner, 2013). Acknowledgements Special thanks to Dr. Ian Orchard for his help, expertise and for reading the manuscript. This work was supported by a Natural Sciences and Engineering Research Council of Canada award to ABL.

References Ayali, A., Lange, A.B., 2010. Rhythmic behaviour and pattern-generating circuits in the locust: key concepts and recent updates. J. Insect Physiol. 56, 834–843. Belanger, J.H., Orchard, I., 1993. The locust ovipositor muscle: proctolinergic central and peripheral neuromodulation in a centrally driven motor system. J. Exp. Biol. 174, 343–362. Bicker, G., Menzel, R., 1989. Chemical codes for the control of behaviour in arthropods. Nature 337, 33–39. Cheung, I.L., Facciponte, G., Lange, A.B., 1994. The effects of octopamine on neuromuscular transmission in the oviducts of Locusta. Biog. Amines 10, 519– 534. Delcomyn, F., 1980. Neural basis of rhythmic behaviour in animals. Science 210, 492–498. Facciponte, G., Lange, A.B., 1992. Characterization of a novel central pattern generator located in the VIIth abdominal ganglion of Locusta migratoria. J. Insect Physiol. 38, 1011–1022. Facciponte, G., Lange, A.B., 1996. Control of the motor pattern generator in the VIIth abdominal ganglion of Locusta: descending neural inhibition and coordination with the oviposition hole digging central pattern generator. J. Insect Physiol. 42, 791–798. Facciponte, G., Miksys, S., Lange, A.B., 1995. The innervation of a ventral abdominal protractor muscle in Locusta. J. Comp. Physiol. 177, 645–657. Grillner, S., 1975. Locomotion in vertebrates: central mechanisms and reflex interactions. Physiol. Rev. 55, 246–304. Kalogianni, E., Theophilidis, G., 1993. Centrally generated rhythmic activity and modulatory function of the oviductal dorsal unpaired median (DUM) neurones in two orthopeteran species (Calliptamus sp. and Decticus albifrons). J. Exp. Biol. 174, 123–138. Kwok, R., Orchard, I., 2002. Central effects of the peptides, SchistoFLRFamide and proctolin, on locust oviduct contraction. Peptides 23, 1925–1932. Kravitz, E.A., 1988. Hormonal control of behavior: amines and the biasing of behavioural output in lobsters. Science 241, 1775–1781. Lange, A.B., 2009a. Neural mechanisms coordinating the female reproductive system in the locust. Front. Biosci. 14, 4401–4415. Lange, A.B., 2009b. The female reproductive system and control of oviposition in the Locusta migratoria migratorioides. Can. J. Zool. 87, 649–661. Lange, A.B., Orchard, I., Loughton, B.G., 1984. Neural inhibition of egg-laying in the locust Locusta migratoria. J. Insect Physiol. 30, 271–278. Lee, H.-G., Rohila, S., Han, K.-A., 2009. The octopamine receptor OAMB mediates ovulation via Ca2+/calmodulin-dependent protein kinase II in the Drosophila oviduct epithelium. PLOS One 4 (3), e4716. Marder, E., 2012. Neuromodulation of neuronal circuits: back to the future. Neuron 76, 1–11. Marder, E., Bucher, D., 2007. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Ann. Rev. Physiol. 69, 291–316. Marder, E., Bucher, D., Schulz, D., Taylor, A., 2005. Invertebrate central pattern generation moves along. Curr. Biol. 15, R685–R699. Monastirioti, M., 2003. Distinct octopamine cell populations residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev. Biol. 264, 38–49. Orchard, I., Lange, A.B., 1985. Evidence for octopaminergic modulation of an insect visceral muscle. J. Neurobiol. 3, 171–181. Orchard, I., Lange, A.B., 1986. Pharmacological profile of octopamine receptors on the lateral oviducts of the locust Locusta migratoria. J. Insect Physiol. 32, 741– 745. Pearson, K., 2000. Neural adaptation in the generation of rhythmic behavior. Annu. Rev. Physiol. 62, 723–753. Rillich, J., Stevenson, P.A., Pflueger, H.-J., 2013. Flight and walking in locusts – cholinergic co-activation, temporal coupling and its modulation by biogenic amines. PLOS One 8 (5), e62899. Rubinstein, C.D., Wolfner, M.F., 2013. Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. PNAS. http:// dx.doi.org/10.1073/pnas.1220018110. 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. Thompson, K.J., 1986a. Oviposition digging in the grasshopper: I. Functional anatomy and the motor programme. J. Exp. Biol. 122, 387–411. Thompson, K.J., 1986b. Ovipositional digging in the grasshopper: II. Descending neural control. J. Exp. Biol. 122, 413–425.

Octopamine modulates a central pattern generator associated with egg-laying in the locust, Locusta migratoria.

Egg-laying in Locusta migratoria involves the control of a variety of complex behavioural patterns including those that regulate digging of the ovipos...
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