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Adding up the odds-Nitric oxide signaling underlies the decision to flee and post-conflict depression of aggression.

Stevenson PA, Rillich J - Sci Adv (2015)

Bottom Line: We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount.This effect of aversive experience is mediated by the NO signaling pathway.NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species.

View Article: PubMed Central - PubMed

Affiliation: Institute for Biology, Leipzig University, Talstraße 33, 04103 Leipzig, Germany.

ABSTRACT
Fighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.

No MeSH data available.


Related in: MedlinePlus

NO translates the effect of the opponent’s agonistic signals to promote the decision to flee.(A) Effect of the NO/cGMP pathway activator SNAP (red and gray bars: Ringer) on a contestant’s aggressiveness when matched against opponents that received no drug (top, level; middle, duration; bottom, win chances; circles, median; bars, IQR; n is given on top x axis). As depicted from left to right, one or both contestants received either no further treatment or a handicap to impede transmission/perception of agonistic signals: None# versus none, Blind# versus none, Blind# versus disarmed (none, no handicap; blind, blackened eyes; disarmed, immobilized mandibles; # denotes drug/vehicle-treated contestant). (B) As for (A), but showing the effect of the NO/cGMP pathway inhibitor LNAME (blue bars) compared to its inactive enantiomer (DNAME, gray bars). Handicaps, from left to right: None# versus none, Disarmed# versus none, Disarmed # versus blind. Significant differences between drug-treated and control groups are indicated by asterisks (U test for level and duration, χ2 test for win chances compared to controls: *P < 0.05, **P < 0.01, ***P < 0.001). Note that SNAP reduces the win chances of blind and LNAME increases win chances of disarmed, without any significant effect on escalation level and fight duration.
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Figure 3: NO translates the effect of the opponent’s agonistic signals to promote the decision to flee.(A) Effect of the NO/cGMP pathway activator SNAP (red and gray bars: Ringer) on a contestant’s aggressiveness when matched against opponents that received no drug (top, level; middle, duration; bottom, win chances; circles, median; bars, IQR; n is given on top x axis). As depicted from left to right, one or both contestants received either no further treatment or a handicap to impede transmission/perception of agonistic signals: None# versus none, Blind# versus none, Blind# versus disarmed (none, no handicap; blind, blackened eyes; disarmed, immobilized mandibles; # denotes drug/vehicle-treated contestant). (B) As for (A), but showing the effect of the NO/cGMP pathway inhibitor LNAME (blue bars) compared to its inactive enantiomer (DNAME, gray bars). Handicaps, from left to right: None# versus none, Disarmed# versus none, Disarmed # versus blind. Significant differences between drug-treated and control groups are indicated by asterisks (U test for level and duration, χ2 test for win chances compared to controls: *P < 0.05, **P < 0.01, ***P < 0.001). Note that SNAP reduces the win chances of blind and LNAME increases win chances of disarmed, without any significant effect on escalation level and fight duration.

Mentions: This led us to ask whether the NO-signaling pathway directly suppresses the tendency to fight (that is, aggressive motivation) or alternatively promotes the decision to flee by mediating the effect of the opponent’s agonistic signals [cf. (12)]. To tease these two possibilities apart, only one contestant of each competing pair was drug-treated, and one or both were handicapped to impede the transmission and/or perception of agonistic signals. We first verified that crickets with either blackened eyes (“blind”) or immobilized mandibles (“disarmed”) engaged nonhandicapped crickets with unabated fight intensity, duration, and win chances, irrespective of whether treated with no drug [cf. (12)] or drug-control solutions (Ringer, Fig. 3A; DNAME, Fig. 3B, gray bars). In these control experiments, the blind contestants also engaged disarmed opponents without any decrement in escalation level or fight duration; remarkably, however, the blind crickets practically always won (87%; n = 23; χ2 compared to 50%, 7.3; P = 0.007; Fig. 3). This illustrates that crickets conform to the cumulative assessment model (8) because only the opponent’s actions influence the decision to flee [see (12) for supporting experiments and arguments]. Accordingly, blind always beat disarmed, because they receive no visual and reduced physical signals from opponents lacking functional mandibles, whereas disarmed accumulate the full brunt of blind’s visual and physical actions and hence become the first to flee. This now puts us in a position to evaluate the influence of nitrergic drugs on the process of opponent assessment.


Adding up the odds-Nitric oxide signaling underlies the decision to flee and post-conflict depression of aggression.

Stevenson PA, Rillich J - Sci Adv (2015)

NO translates the effect of the opponent’s agonistic signals to promote the decision to flee.(A) Effect of the NO/cGMP pathway activator SNAP (red and gray bars: Ringer) on a contestant’s aggressiveness when matched against opponents that received no drug (top, level; middle, duration; bottom, win chances; circles, median; bars, IQR; n is given on top x axis). As depicted from left to right, one or both contestants received either no further treatment or a handicap to impede transmission/perception of agonistic signals: None# versus none, Blind# versus none, Blind# versus disarmed (none, no handicap; blind, blackened eyes; disarmed, immobilized mandibles; # denotes drug/vehicle-treated contestant). (B) As for (A), but showing the effect of the NO/cGMP pathway inhibitor LNAME (blue bars) compared to its inactive enantiomer (DNAME, gray bars). Handicaps, from left to right: None# versus none, Disarmed# versus none, Disarmed # versus blind. Significant differences between drug-treated and control groups are indicated by asterisks (U test for level and duration, χ2 test for win chances compared to controls: *P < 0.05, **P < 0.01, ***P < 0.001). Note that SNAP reduces the win chances of blind and LNAME increases win chances of disarmed, without any significant effect on escalation level and fight duration.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643817&req=5

Figure 3: NO translates the effect of the opponent’s agonistic signals to promote the decision to flee.(A) Effect of the NO/cGMP pathway activator SNAP (red and gray bars: Ringer) on a contestant’s aggressiveness when matched against opponents that received no drug (top, level; middle, duration; bottom, win chances; circles, median; bars, IQR; n is given on top x axis). As depicted from left to right, one or both contestants received either no further treatment or a handicap to impede transmission/perception of agonistic signals: None# versus none, Blind# versus none, Blind# versus disarmed (none, no handicap; blind, blackened eyes; disarmed, immobilized mandibles; # denotes drug/vehicle-treated contestant). (B) As for (A), but showing the effect of the NO/cGMP pathway inhibitor LNAME (blue bars) compared to its inactive enantiomer (DNAME, gray bars). Handicaps, from left to right: None# versus none, Disarmed# versus none, Disarmed # versus blind. Significant differences between drug-treated and control groups are indicated by asterisks (U test for level and duration, χ2 test for win chances compared to controls: *P < 0.05, **P < 0.01, ***P < 0.001). Note that SNAP reduces the win chances of blind and LNAME increases win chances of disarmed, without any significant effect on escalation level and fight duration.
Mentions: This led us to ask whether the NO-signaling pathway directly suppresses the tendency to fight (that is, aggressive motivation) or alternatively promotes the decision to flee by mediating the effect of the opponent’s agonistic signals [cf. (12)]. To tease these two possibilities apart, only one contestant of each competing pair was drug-treated, and one or both were handicapped to impede the transmission and/or perception of agonistic signals. We first verified that crickets with either blackened eyes (“blind”) or immobilized mandibles (“disarmed”) engaged nonhandicapped crickets with unabated fight intensity, duration, and win chances, irrespective of whether treated with no drug [cf. (12)] or drug-control solutions (Ringer, Fig. 3A; DNAME, Fig. 3B, gray bars). In these control experiments, the blind contestants also engaged disarmed opponents without any decrement in escalation level or fight duration; remarkably, however, the blind crickets practically always won (87%; n = 23; χ2 compared to 50%, 7.3; P = 0.007; Fig. 3). This illustrates that crickets conform to the cumulative assessment model (8) because only the opponent’s actions influence the decision to flee [see (12) for supporting experiments and arguments]. Accordingly, blind always beat disarmed, because they receive no visual and reduced physical signals from opponents lacking functional mandibles, whereas disarmed accumulate the full brunt of blind’s visual and physical actions and hence become the first to flee. This now puts us in a position to evaluate the influence of nitrergic drugs on the process of opponent assessment.

Bottom Line: We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount.This effect of aversive experience is mediated by the NO signaling pathway.NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species.

View Article: PubMed Central - PubMed

Affiliation: Institute for Biology, Leipzig University, Talstraße 33, 04103 Leipzig, Germany.

ABSTRACT
Fighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent's aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO's effect is manifested in losers by prolonged avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.

No MeSH data available.


Related in: MedlinePlus