Controlling the decision to fight or flee: the roles of biogenic amines and nitric oxide in the cricket†

Aggression is a common behavioral strategy employed by animals to secure limited resources, but must be applied with restraint to limit potential costs including injury. How animals make the adaptive decision to fight or flee is barely known. Here, we review our work on crickets that reveals the roles of biogenic amines, primarily octopamine (the insect analog of noradrenaline) and nitric oxide (NO). Using aminergic drugs, we found that amines are not essential for actually initiating aggression. However, octopamine is necessary for mediating the aggression-promoting effects of potentially rewarding experiences including stimulation with a male antenna, physical exertion, winning, and resource possession. Hence, octopamine can be considered as the motivational component of aggression. Imposed handicaps that impede aggressive signaling revealed that the agonistic actions of an opponent perceived during fighting act to reduce aggression, and that crickets make the decision to flee the moment the accumulated sum of such aversive experiences exceeds some critical level. Treatment with nitridergic drugs revealed that the impact of the opponent's aggressive actions is mediated by NO. NO acts to suppress aggression by promoting the tendency to flee and is primarily responsible for the depressed aggressiveness of subordinates after social defeat. Octopamine and dopamine can each restore aggression in subordinates, but only dopamine is necessary for normal recovery. The role of serotonin remains unclear, and is discussed. We conclude that octopamine and NO control the decision to fight or flee by mediating the effects of potentially rewarding and aversive experiences, respectively.