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Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster.

Alekseyenko OV, Lee C, Kravitz EA - PLoS ONE (2010)

Bottom Line: These flies did not escalate fights beyond brief low-intensity interactions and therefore did not yield dominance relationships.Selective disruption of 5HT neurotransmission yielded flies that fought, but with reduced ability to escalate fights, leading to fewer dominance relationships.Acute activation of 5HT neurons using temperature sensitive dTrpA1 channel expression, in contrast, resulted in flies that escalated fights faster and that fought at higher intensities.

View Article: PubMed Central - PubMed

Affiliation: Neurobiology Department, Harvard Medical School, Boston, Massachusetts, USA. olga_alekseenko@hms.harvard.edu

ABSTRACT
Dopamine (DA) and serotonin (5HT) are reported to serve important roles in aggression in a wide variety of animals. Previous investigations of 5HT function in adult Drosophila behavior have relied on pharmacological manipulations, or on combinations of genetic tools that simultaneously target both DA and 5HT neurons. Here, we generated a transgenic line that allows selective, direct manipulation of serotonergic neurons and asked whether DA and 5HT have separable effects on aggression. Quantitative morphological examination demonstrated that our newly generated tryptophan hydroxylase (TRH)-Gal4 driver line was highly selective for 5HT-containing neurons. This line was used in conjunction with already available Gal4 driver lines that target DA or both DA and 5HT neurons to acutely alter the function of aminergic systems. First, we showed that acute impairment of DA and 5HT neurotransmission using expression of a temperature sensitive form of dynamin completely abolished mid- and high-level aggression. These flies did not escalate fights beyond brief low-intensity interactions and therefore did not yield dominance relationships. We showed next that manipulation of either 5HT or DA neurotransmission failed to duplicate this phenotype. Selective disruption of 5HT neurotransmission yielded flies that fought, but with reduced ability to escalate fights, leading to fewer dominance relationships. Acute activation of 5HT neurons using temperature sensitive dTrpA1 channel expression, in contrast, resulted in flies that escalated fights faster and that fought at higher intensities. Finally, acute disruption of DA neurotransmission produced hyperactive flies that moved faster than controls, and rarely engaged in any social interactions. By separately manipulating 5HT- and DA- neuron systems, we collected evidence demonstrating a direct role for 5HT in the escalation of aggression in Drosophila.

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Selective disruption of serotonergic synaptic transmission results in less aggressive flies.No significant differences were seen in the numbers of encounters (A) or in the average duration of each encounter (B) throughout a fight (shown for the first 20 min only). (C) TRH-Gal4/UAS-shits1 flies at the restrictive temperature (gray striped bars), however, did show decreased numbers of lunges compared to the experimental males at the permissive temperature (gray bars). This effect was most pronounced at the 20–40 and 40–60 min time windows. Decreases also were seen in the numbers of lunges in genetic control flies, but these were not significant, and were related to switching flies to an elevated temperature. *p<0.05 vs. same genotype at the permissive temperature (19°C), analyzed by nonparametric two-independent-sample Mann-Whitney U-test.
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pone-0010806-g004: Selective disruption of serotonergic synaptic transmission results in less aggressive flies.No significant differences were seen in the numbers of encounters (A) or in the average duration of each encounter (B) throughout a fight (shown for the first 20 min only). (C) TRH-Gal4/UAS-shits1 flies at the restrictive temperature (gray striped bars), however, did show decreased numbers of lunges compared to the experimental males at the permissive temperature (gray bars). This effect was most pronounced at the 20–40 and 40–60 min time windows. Decreases also were seen in the numbers of lunges in genetic control flies, but these were not significant, and were related to switching flies to an elevated temperature. *p<0.05 vs. same genotype at the permissive temperature (19°C), analyzed by nonparametric two-independent-sample Mann-Whitney U-test.

Mentions: In order to reduce 5HT release from serotonergic neurons alone, we drove the expression of UAS-shibirets1 (UAS-shits1) using the TRH-Gal4 line. In contrast to the results obtained with the DDC-Gal4 driven progeny, the numbers of encounters and the average duration of each encounter did not differ significantly from either temperature or genetic controls during any of the three 20 min time periods (Fig. 4, A, B, data shown for the first 20 min period). Experimental flies did show an increase in the numbers of low-intensity fencing events during the first 20 min of a fight compared to the same genotype at the permissive temperature (7.3±2.0 at 19°C vs. 16.7±2.6 at 30°C; Mann-Whitney U = 50.5, p = 0.046). The most important difference in comparing DDC-Gal4 and TRH-Gal4 datasets was that we observed some escalation to higher intensity levels of aggression in fights between flies with disrupted 5HT neurotransmission.


Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster.

Alekseyenko OV, Lee C, Kravitz EA - PLoS ONE (2010)

Selective disruption of serotonergic synaptic transmission results in less aggressive flies.No significant differences were seen in the numbers of encounters (A) or in the average duration of each encounter (B) throughout a fight (shown for the first 20 min only). (C) TRH-Gal4/UAS-shits1 flies at the restrictive temperature (gray striped bars), however, did show decreased numbers of lunges compared to the experimental males at the permissive temperature (gray bars). This effect was most pronounced at the 20–40 and 40–60 min time windows. Decreases also were seen in the numbers of lunges in genetic control flies, but these were not significant, and were related to switching flies to an elevated temperature. *p<0.05 vs. same genotype at the permissive temperature (19°C), analyzed by nonparametric two-independent-sample Mann-Whitney U-test.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2875409&req=5

pone-0010806-g004: Selective disruption of serotonergic synaptic transmission results in less aggressive flies.No significant differences were seen in the numbers of encounters (A) or in the average duration of each encounter (B) throughout a fight (shown for the first 20 min only). (C) TRH-Gal4/UAS-shits1 flies at the restrictive temperature (gray striped bars), however, did show decreased numbers of lunges compared to the experimental males at the permissive temperature (gray bars). This effect was most pronounced at the 20–40 and 40–60 min time windows. Decreases also were seen in the numbers of lunges in genetic control flies, but these were not significant, and were related to switching flies to an elevated temperature. *p<0.05 vs. same genotype at the permissive temperature (19°C), analyzed by nonparametric two-independent-sample Mann-Whitney U-test.
Mentions: In order to reduce 5HT release from serotonergic neurons alone, we drove the expression of UAS-shibirets1 (UAS-shits1) using the TRH-Gal4 line. In contrast to the results obtained with the DDC-Gal4 driven progeny, the numbers of encounters and the average duration of each encounter did not differ significantly from either temperature or genetic controls during any of the three 20 min time periods (Fig. 4, A, B, data shown for the first 20 min period). Experimental flies did show an increase in the numbers of low-intensity fencing events during the first 20 min of a fight compared to the same genotype at the permissive temperature (7.3±2.0 at 19°C vs. 16.7±2.6 at 30°C; Mann-Whitney U = 50.5, p = 0.046). The most important difference in comparing DDC-Gal4 and TRH-Gal4 datasets was that we observed some escalation to higher intensity levels of aggression in fights between flies with disrupted 5HT neurotransmission.

Bottom Line: These flies did not escalate fights beyond brief low-intensity interactions and therefore did not yield dominance relationships.Selective disruption of 5HT neurotransmission yielded flies that fought, but with reduced ability to escalate fights, leading to fewer dominance relationships.Acute activation of 5HT neurons using temperature sensitive dTrpA1 channel expression, in contrast, resulted in flies that escalated fights faster and that fought at higher intensities.

View Article: PubMed Central - PubMed

Affiliation: Neurobiology Department, Harvard Medical School, Boston, Massachusetts, USA. olga_alekseenko@hms.harvard.edu

ABSTRACT
Dopamine (DA) and serotonin (5HT) are reported to serve important roles in aggression in a wide variety of animals. Previous investigations of 5HT function in adult Drosophila behavior have relied on pharmacological manipulations, or on combinations of genetic tools that simultaneously target both DA and 5HT neurons. Here, we generated a transgenic line that allows selective, direct manipulation of serotonergic neurons and asked whether DA and 5HT have separable effects on aggression. Quantitative morphological examination demonstrated that our newly generated tryptophan hydroxylase (TRH)-Gal4 driver line was highly selective for 5HT-containing neurons. This line was used in conjunction with already available Gal4 driver lines that target DA or both DA and 5HT neurons to acutely alter the function of aminergic systems. First, we showed that acute impairment of DA and 5HT neurotransmission using expression of a temperature sensitive form of dynamin completely abolished mid- and high-level aggression. These flies did not escalate fights beyond brief low-intensity interactions and therefore did not yield dominance relationships. We showed next that manipulation of either 5HT or DA neurotransmission failed to duplicate this phenotype. Selective disruption of 5HT neurotransmission yielded flies that fought, but with reduced ability to escalate fights, leading to fewer dominance relationships. Acute activation of 5HT neurons using temperature sensitive dTrpA1 channel expression, in contrast, resulted in flies that escalated fights faster and that fought at higher intensities. Finally, acute disruption of DA neurotransmission produced hyperactive flies that moved faster than controls, and rarely engaged in any social interactions. By separately manipulating 5HT- and DA- neuron systems, we collected evidence demonstrating a direct role for 5HT in the escalation of aggression in Drosophila.

Show MeSH
Related in: MedlinePlus