Distinct mechanisms mediate dopamine-octopamine opponency in an insect model of olfaction

Neuromodulators play a key role in determining how an organism processes and responds to sensory cues. Often, different neuromodulators act on the same set of neural circuits to produce diverging behavioral outcomes. In this study, we examined how dopamine and octopamine alter odor-driven neural activity in a peripheral olfactory circuit (the antennal lobe) of the locusts (Schistocerca americana, both sexes) and thereby alter behavioral responses in an opposing manner. Our results indicate that dopamine suppressed GABAergic local neuron activity during odor stimulation. Releasing the antennal lobe network from inhibition increased the principal neural activity for all odorants and led to nonspecific increases in a behavioral appetitive response. Octopamine, on the other hand, did not alter the GABAergic inhibition in the antennal lobe but still reduced the odor-evoked principal neural activity and the behavioral responses elicited by all odorants. Thus, both dopamine and octopamine used distinct mechanisms (altering recurrent inhibition vs intrinsic excitability) to mediate opponent changes in odor-evoked neural activity and behavioral outcomes.Significance Statement A basic question in neural computation concerns how various neuromodulators act on the same neural circuit to alter behavioral outcomes. In this study, we focused on three main neuromodulators: dopamine, octopamine, and serotonin and examined how they alter a relatively simpler insect olfactory circuit. Our results reveal that each neuromodulator alters a different neural circuit property, but this perturbs the excitation-inhibition balance in a biological neural network and thereby can fine-tune the behavioral output in opposing fashion. In sum, our results shed light on how neuromodulators impact the global computations of a biological neural network in an antagonistic fashion.