Biogenic amines and activity levels alter the neural energetic response to aggressive social cues in the honey bee Apis mellifera

Abstract

Mitochondrial activity is highly dynamic in the healthy brain, and it can reflect both the signaling potential and the signaling history of neural circuits. Recent studies spanning invertebrates to mammals have highlighted a role for neural mitochondrial dynamics in learning and memory processes as well as behavior. In the current study, we investigate the interplay between biogenic amine signaling and neural energetics in the honey bee, Apis mellifera. In this species, aggressive behaviors are regulated by neural energetic state and biogenic amine titers, but it is unclear how these mechanisms are linked to impact behavioral expression. We show that brain mitochondrial number is highest in aggression-relevant brain regions and in individual bees that are most responsive to aggressive cues, emphasizing the importance of energetics in modulating this phenotype. We also show that the neural energetic response to alarm pheromone, an aggression inducing social cue, is activity dependent, modulated by the "fight or flight" insect neurotransmitter octopamine. Two other neuroactive compounds known to cause variation in aggression, dopamine, and serotonin, also modulate neural energetic state in aggression-relevant regions of the brain. However, the effects of these compounds on respiration at baseline and following alarm pheromone exposure are distinct, suggesting unique mechanisms underlying variation in mitochondrial respiration in these circuits. These results motivate new explanations for the ways in which biogenic amines alter sensory perception in the context of aggression. Considering neural energetics improves predictions about the regulation of complex and context-dependent behavioral phenotypes.

Keywords: aggression; honey bees; metabolic rate; mitochondrial bioenergetics; neural plasticity.