Octopamine and Experience-Dependent Modulation of Aggression in Crickets

Abstract

Intraspecific aggression is influenced in numerous animal groups by the previous behavioral experiences of the competitors. The underlying mechanisms are, however, mostly obscure. We present evidence that a form of experience-dependent plasticity of aggression in crickets is mediated by octopamine, the invertebrate counterpart of noradrenaline. In a forced-fight paradigm, the experience of flying maximized the aggressiveness of crickets at their first encounter and accelerated the subsequent recovery of aggressiveness of the normally submissive losers, without enhancing general excitability as evaluated from the animals' startle responses to wind stimulation. This effect is transitory and concurrent with the activation of the octopaminergic system that accompanies flight. Hemocoel injections of the octopamine agonist chlordimeform (CDM) had similar effects on aggression but also enhanced startle responses. Serotonin depletion, achieved using ␣-methyl-tryptophan, enhanced startle responses without influencing aggression, indicating that the effect of CDM on aggression is not attributable to increased general excitation. Contrasting this, aggressiveness was depressed, and the effect of flying was essentially abolished, in crickets depleted of octopamine and dopamine using ␣-methyl-p-tyrosine (AMT). CDM restored aggressiveness in AMT-treated crickets, indicating that their depressed aggressiveness is attributable to octopamine depletion rather than to dopamine depletion or nonspecific defects. Finally, the flight effect was blocked in crickets treated with the octopamine receptor antagonist epinastine, or with the ␣-adrenoceptor and octopamine receptor antagonist phentolamine, but not with the ␤-adrenoceptor antagonist propranolol. The idea that activity-specific induction of the octopaminergic system underlies other forms of experiencedependent plasticity of aggressive motivation in insects is discussed.

Elementary Motion Detection

“…It has been known for decades that it changes the behavioral state of an animal. The level of octopamine is increased during stress and aggression (Davenport and Evans, 1984;Stevenson et al, 2005). The effects of octopamine on the flight system of the locust has been studied in detail ranging from work on adaptation to energy demanding processes to single-cell physiology (Morris et al, 1999;Orchard and Lange, 1984;Orchard et al, 1993;Ramirez and Pearson, 1991).…”

“…Given the different size of Calliphora and Lucilia the difference in total concentration per brain volume is assumed to be even higher and was approximated at 7.2 x 10 -10 mol/g. However, considering the broad range of concentrations in bath solutions used in other insects studies I consider the concentration well within the range of physiologically relevant concentrations for CDM (Duch and Pfluger, 1999;Kinnamon et al, 1984;Stevenson et al, 2005;Vierk et al, 2009). The spontaneous spike rate of H1 was reliable increased within 5 min after application and remained so throughout the duration of the stimulus presentation (20 min).…”

“…In addition, the application procedure does not disturb the animal at all. This is of critical importance since octopamine is known to be released during arousal (Davenport and Evans, 1984;Roeder, 1999;Stevenson et al, 2005). Therefore, bath application seems to be suitable as an initial experiment to address the question of whether octopamine contributes to some of the observed effects in flight.…”

“…Therefore, bath application seems to be suitable as an initial experiment to address the question of whether octopamine contributes to some of the observed effects in flight. The CDM concentration used in this work was more towards the lower end of the range used in previous studies (Duch and Pfluger, 1999;Kinnamon et al, 1984;Stevenson et al, 2005;Vierk et al, 2009). It was in the same order of magnitude as used previously in studies on flies (Longden and Krapp, 2009).…”

Exposure to static electric fields leads to changes in biogenic amine levels in the brains ofDrosophila

“…Amines play a major role in the behaviour of insects, from underpinning extreme changes in phenotypic plasticity in locusts where dopamine and serotonin have a major role in driving the swarming form of migratory and desert locusts [16][17][18], to social interactions between nest-mates influencing brain biogenic amine homeostasis in stressed ants [19,20]. They also play a crucial role in aggressive encounters between dominant and submissive animals [21].…”