State-Dependent Performance of Optic-Flow Processing Interneurons

Abstract

Active locomotive states are metabolically expensive and require efficient sensory processing both to avoid wasteful movements and to cope with an extended bandwidth of sensory stimuli. This is particularly true for flying animals because flight, as opposed to walking or resting, imposes a steplike increase in metabolism for the precise execution and control of movements. Sensory processing itself carries a significant metabolic cost, but the principles governing the adjustment of sensory processing to different locomotor states are not well understood. We use the blowfly as a model system to study the impact on visual processing of a neuromodulator, octopamine, which is known to be involved in the regulation of flight physiology. We applied an octopamine agonist and recorded the directional motion responses of identified visual interneurons known to process self-motion–induced optic flow to directional motion stimuli. The neural response range of these neurons is increased and the response latency is reduced. We also found that, due to an elevated spontaneous spike rate, the cells' negative signaling range is increased. Meanwhile, the preferred self-motion parameters the cells encode were state independent. Our results indicate that in the blowfly energetically expensive sensory coding strategies, such as rapid, large responses, and high spontaneous spike activity could be adjusted by the neuromodulator octopamine, likely to save energy during quiet locomotor states.