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Sleep deprivation suppresses aggression in Drosophila.

Kayser MS, Mainwaring B, Yue Z, Sehgal A - Elife (2015)

Bottom Line: However, a clear effect of sleep deprivation on aggressive behaviors remains unclear.We find that acute sleep deprivation profoundly suppresses aggressive behaviors in the fruit fly, while other social behaviors are unaffected.This suppression is recovered following post-deprivation sleep rebound, and occurs regardless of the approach to achieve sleep loss.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, United States.

ABSTRACT
Sleep disturbances negatively impact numerous functions and have been linked to aggression and violence. However, a clear effect of sleep deprivation on aggressive behaviors remains unclear. We find that acute sleep deprivation profoundly suppresses aggressive behaviors in the fruit fly, while other social behaviors are unaffected. This suppression is recovered following post-deprivation sleep rebound, and occurs regardless of the approach to achieve sleep loss. Genetic and pharmacologic approaches suggest octopamine signaling transmits changes in aggression upon sleep deprivation, and reduced aggression places sleep-deprived flies at a competitive disadvantage for obtaining a reproductive partner. These findings demonstrate an interaction between two phylogenetically conserved behaviors, and suggest that previous sleep experiences strongly modulate aggression with consequences for reproductive fitness.

No MeSH data available.


Related in: MedlinePlus

Quantification of aggression in CS males fed either CDM or L-DOPA and mechanically sleep-deprived (n = 17, 20, 24 from left to right).*p < 0.05; 1 way ANOVA with Tukey's post-hoc test.DOI:http://dx.doi.org/10.7554/eLife.07643.015
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fig2s3: Quantification of aggression in CS males fed either CDM or L-DOPA and mechanically sleep-deprived (n = 17, 20, 24 from left to right).*p < 0.05; 1 way ANOVA with Tukey's post-hoc test.DOI:http://dx.doi.org/10.7554/eLife.07643.015

Mentions: Octopamine and dopamine have been implicated in controlling both sleep/arousal and aggressive behaviors. We examined whether either of these monoamines play a role in coupling sleep deprivation to changes in aggression. First, we asked how thermogenetic sleep deprivation via overnight activation of octopaminergic or dopaminergic neurons affects next day fighting. The Drosophila thermosensitive cation channel dTrpA1 (Hamada et al., 2008) was expressed using Tdc2-GAL4 (octopamine neurons) or TH-GAL4 (dopamine neurons), and flies were exposed to 29°C for 12 hr overnight. Activation of neurons using either GAL4 line resulted in near total sleep deprivation (Figure 2—figure supplement 1); importantly, overnight exposure to 29°C in flies lacking either the GAL4 or UAS did not impact sleep (Figure 2—figure supplement 2), in contrast to CS males exposed to 31°C. Aggression was assessed the following morning at 23°C, below the threshold for TrpA1 activation. Sleep deprivation by activation of Tdc2+ or TH+ neurons caused a significant suppression of aggression the following day (Figure 2A; Figure 2—source data 1), while genetic and temperature controls with normal prior sleep showed no such effect (Figure 2A; Figure 2—figure supplement 2). Our results suggest that perturbation of octopamine and/or dopamine signaling as a result of sleep deprivation could impair aggressive behaviors. Using a pharmacologic approach we tested whether octopamine or dopamine agonists rescue reduced aggression. Flies were fed the octopamine agonist chlordimeform (CDM) or the dopamine agonist L-DOPA leading up to aggression assays that were preceded by thermogenetic sleep deprivation. CDM, but not L-DOPA, rescued aggression following sleep deprivation via activation of Tdc2+ neurons (Figure 2B). Surprisingly, CDM also rescued aggression following sleep deprivation via activation of TH+ neurons, while L-DOPA did not (Figure 2C). This effect is not specific to thermogenetic sleep deprivation, as CDM alone rescued aggression after mechanical sleep deprivation as well (Figure 2—figure supplement 3). These results suggest that aggression-relevant octopamine function is compromised downstream of sleep deprivation signals, regardless of method of sleep loss.10.7554/eLife.07643.011Figure 2.Octopamine agonist CDM rescues reduced aggression following sleep deprivation.


Sleep deprivation suppresses aggression in Drosophila.

Kayser MS, Mainwaring B, Yue Z, Sehgal A - Elife (2015)

Quantification of aggression in CS males fed either CDM or L-DOPA and mechanically sleep-deprived (n = 17, 20, 24 from left to right).*p < 0.05; 1 way ANOVA with Tukey's post-hoc test.DOI:http://dx.doi.org/10.7554/eLife.07643.015
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4515473&req=5

fig2s3: Quantification of aggression in CS males fed either CDM or L-DOPA and mechanically sleep-deprived (n = 17, 20, 24 from left to right).*p < 0.05; 1 way ANOVA with Tukey's post-hoc test.DOI:http://dx.doi.org/10.7554/eLife.07643.015
Mentions: Octopamine and dopamine have been implicated in controlling both sleep/arousal and aggressive behaviors. We examined whether either of these monoamines play a role in coupling sleep deprivation to changes in aggression. First, we asked how thermogenetic sleep deprivation via overnight activation of octopaminergic or dopaminergic neurons affects next day fighting. The Drosophila thermosensitive cation channel dTrpA1 (Hamada et al., 2008) was expressed using Tdc2-GAL4 (octopamine neurons) or TH-GAL4 (dopamine neurons), and flies were exposed to 29°C for 12 hr overnight. Activation of neurons using either GAL4 line resulted in near total sleep deprivation (Figure 2—figure supplement 1); importantly, overnight exposure to 29°C in flies lacking either the GAL4 or UAS did not impact sleep (Figure 2—figure supplement 2), in contrast to CS males exposed to 31°C. Aggression was assessed the following morning at 23°C, below the threshold for TrpA1 activation. Sleep deprivation by activation of Tdc2+ or TH+ neurons caused a significant suppression of aggression the following day (Figure 2A; Figure 2—source data 1), while genetic and temperature controls with normal prior sleep showed no such effect (Figure 2A; Figure 2—figure supplement 2). Our results suggest that perturbation of octopamine and/or dopamine signaling as a result of sleep deprivation could impair aggressive behaviors. Using a pharmacologic approach we tested whether octopamine or dopamine agonists rescue reduced aggression. Flies were fed the octopamine agonist chlordimeform (CDM) or the dopamine agonist L-DOPA leading up to aggression assays that were preceded by thermogenetic sleep deprivation. CDM, but not L-DOPA, rescued aggression following sleep deprivation via activation of Tdc2+ neurons (Figure 2B). Surprisingly, CDM also rescued aggression following sleep deprivation via activation of TH+ neurons, while L-DOPA did not (Figure 2C). This effect is not specific to thermogenetic sleep deprivation, as CDM alone rescued aggression after mechanical sleep deprivation as well (Figure 2—figure supplement 3). These results suggest that aggression-relevant octopamine function is compromised downstream of sleep deprivation signals, regardless of method of sleep loss.10.7554/eLife.07643.011Figure 2.Octopamine agonist CDM rescues reduced aggression following sleep deprivation.

Bottom Line: However, a clear effect of sleep deprivation on aggressive behaviors remains unclear.We find that acute sleep deprivation profoundly suppresses aggressive behaviors in the fruit fly, while other social behaviors are unaffected.This suppression is recovered following post-deprivation sleep rebound, and occurs regardless of the approach to achieve sleep loss.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, United States.

ABSTRACT
Sleep disturbances negatively impact numerous functions and have been linked to aggression and violence. However, a clear effect of sleep deprivation on aggressive behaviors remains unclear. We find that acute sleep deprivation profoundly suppresses aggressive behaviors in the fruit fly, while other social behaviors are unaffected. This suppression is recovered following post-deprivation sleep rebound, and occurs regardless of the approach to achieve sleep loss. Genetic and pharmacologic approaches suggest octopamine signaling transmits changes in aggression upon sleep deprivation, and reduced aggression places sleep-deprived flies at a competitive disadvantage for obtaining a reproductive partner. These findings demonstrate an interaction between two phylogenetically conserved behaviors, and suggest that previous sleep experiences strongly modulate aggression with consequences for reproductive fitness.

No MeSH data available.


Related in: MedlinePlus