Octopamine Neuromodulatory Effects on a Social Behavior Decision-Making Network in Drosophila Males

Certel, Sarah J.; Leung, Adelaine Kwun-Wai; Lin, Cai; Perez, Philip; Chiang, Ann‐Shyn; Kravitz, Edward A.

doi:10.1371/journal.pone.0013248

Cited by 84 publications

(108 citation statements)

References 86 publications

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“…In Drosophila, a similar effect has been reported with octopaminergic neurons (octopamine is the invertebrate analog of the catecholamine norepinephrine) and courtship behavior. In that example, both lowering and enhancing the function of octopaminergic neurons resulted in increased male-male courtship (29).…”

Section: Discussionmentioning

confidence: 99%

Single dopaminergic neurons that modulate aggression in Drosophila

Alekseyenko

Chan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Monoamines, including dopamine (DA), have been linked to aggression in various species. However, the precise role or roles served by the amine in aggression have been difficult to define because dopaminergic systems influence many behaviors, and all can be altered by changing the function of dopaminergic neurons. In the fruit fly, with the powerful genetic tools available, small subsets of brain cells can be reliably manipulated, offering enormous advantages for exploration of how and where amine neurons fit into the circuits involved with aggression. By combining the GAL4/upstream activating sequence (UAS) binary system with the Flippase (FLP) recombination technique, we were able to restrict the numbers of targeted DA neurons down to a single-cell level. To explore the function of these individual dopaminergic neurons, we inactivated them with the tetanus toxin light chain, a genetically encoded inhibitor of neurotransmitter release, or activated them with dTrpA1, a temperature-sensitive cation channel. We found two sets of dopaminergic neurons that modulate aggression, one from the T1 cluster and another from the PPM3 cluster. Both activation and inactivation of these neurons resulted in an increase in aggression. We demonstrate that the presynaptic terminals of the identified T1 and PPM3 dopaminergic neurons project to different parts of the central complex, overlapping with the receptor fields of DD2R and DopR DA receptor subtypes, respectively. These data suggest that the two types of dopaminergic neurons may influence aggression through interactions in the central complex region of the brain involving two different DA receptor subtypes.A ggression is an innate behavior commonly used to obtain resources such as territories, mates, or food. Although some features of aggression are species-specific, broad similarities exist across species in the behavioral patterns and neurochemical systems involved (1, 2). Monoamines such as dopamine (DA) and serotonin have been linked to aggression in many species (3). Elaboration of the neural pathways that control aggression, however, has proven difficult because monoaminergic neurons also regulate other behaviors (1, 2). The pharmacological and genetic manipulations usually used for altering amine neuron function influence most of the neurons within a given monoaminergic population and thereby cause many behavioral changes. This makes it difficult to pinpoint the relationship between any particular amine-induced behavioral phenotype and an associated neuronal pathway.The fruit fly offers enormous advantages in these regards because existing powerful genetic methods permit manipulation of small subsets of brain cells for exploration of the neural mechanisms of behavior (4-6). In the Drosophila model of aggression (7,8), males fight and form stable hierarchical relationships. Using this model, we have shown that acute shutdown of serotonergic neurons yielded flies that could initiate fights but showed a reduced ability to escalate aggression. Activation of serotonergic ne...

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Section: Discussionmentioning

confidence: 99%

Single dopaminergic neurons that modulate aggression in Drosophila

Alekseyenko

Chan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

152

153

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“…In invertebrates, dopamine (DA) and octopamine (OA) are two important modulators of behaviour. OA, the invertebrate counterpart of the adrenergic vertebrate system, has been implicated in state-dependent changes in visual processing [1,2], experience-dependent modulation of aggression [3], social decision-making [4] and reward [5]. DA is also known for its countless roles in physiological and behavioural processes across animal phyla, such as reward [5][6][7], motivation [8 -10] and value-based or goal-directed decisionmaking [8,11 -15].…”

Section: Introductionmentioning

confidence: 99%

A decision underlies phototaxis in an insect

Gorostiza

Colomb

Brembs

2015

Preprint

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Like a moth into the flame-phototaxis is an iconic example for innate preferences. Such preferences probably reflect evolutionary adaptations to predictable situations and have traditionally been conceptualized as hardwired stimulus-response links. Perhaps for that reason, the century-old discovery of flexibility in Drosophila phototaxis has received little attention. Here, we report that across several different behavioural tests, light/dark preference tested in walking is dependent on various aspects of flight. If we temporarily compromise flying ability, walking photopreference reverses concomitantly. Neuronal activity in circuits expressing dopamine and octopamine, respectively, plays a differential role in photopreference, suggesting a potential involvement of these biogenic amines in this case of behavioural flexibility. We conclude that flies monitor their ability to fly, and that flying ability exerts a fundamental effect on action selection in Drosophila. This work suggests that even behaviours which appear simple and hard-wired comprise a value-driven decision-making stage, negotiating the external situation with the animal's internal state, before an action is selected.

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“…For example, octopamine modulates behaviors such as aggression (Hoyer et al, 2008;Zhou et al, 2008;Rillich et al, 2011), sleep (Crocker and Sehgal, 2008;Crocker et al, 2010), egg-laying (Monastirioti et al, 1996), food-seeking (Suo et al, 2006), as well as locomotion (Certel et al, 2010;Fussnecker et al, 2006;Saraswati et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Characterization of a β-adrenergic-like octopamine receptor from the rice stem borer (Chilo suppressalis)

Yao

Huang

et al. 2012

Journal of Experimental Biology

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SUMMARYOctopamine, the invertebrate counterpart of adrenaline and noradrenaline, plays a key role in regulation of many physiological and behavioral processes in insects. It modulates these functions through binding to specific octopamine receptors, which are typical rhodopsin-like G-protein coupled receptors. A cDNA encoding a seven-transmembrane receptor was cloned from the nerve cord of the rice stem borer, Chilo suppressalis, viz. CsOA2B2, which shares high sequence similarity to CG6989, a Drosophila -adrenergic-like octopamine receptor (DmOct2R). We generated an HEK-293 cell line that stably expresses CsOA2B2 in order to examine the functional and pharmacological properties of this receptor. Activation of CsOA2B2 by octopamine increased the production of cAMP in a dose-dependent manner (EC 50 2.33nmoll Supplementary material available online at

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Octopamine Neuromodulatory Effects on a Social Behavior Decision-Making Network in Drosophila Males

Cited by 84 publications

References 86 publications

Single dopaminergic neurons that modulate aggression in Drosophila

Single dopaminergic neurons that modulate aggression in Drosophila

A decision underlies phototaxis in an insect

Characterization of a β-adrenergic-like octopamine receptor from the rice stem borer (Chilo suppressalis)

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