Flight Activity Alters Velocity Tuning of Fly Motion-Sensitive Neurons

Abstract

Sensory neurons are mostly studied in fixed animals, but their response properties might change when the animal is free to move. Indeed, recent studies found differences between responses of sensory neurons in resting versus moving insects. Since the dynamic range of visual motion stimuli strongly depends on the speed at which an animal is moving, we investigated whether the visual system adapts to such changes in stimulus dynamics as induced by self-motion. Lobula plate tangential cells of flies lend themselves well to study this question because they are known to code for ego-motion based on optic-flow. We recorded the responses of the lobula plate tangential cell H1 to a visual pattern moving at different velocities under three different conditions: fixed flies before and after application of the octopamine agonist chlordimeform (CDM) and tethered flying flies. CDM has been previously shown to induce arousal in flies. We found that flying as well as the application of CDM significantly broadens the velocity tuning of H1 toward higher velocities.

Dynamic use of optic flow during pheromone tracking by the male silkmoth, Bombyx mori

“…S2). Although we do not have any evidence that the onset of optic flow elicits particular neuronal responses in the visual system of silkmoths, studies on the motion-sensitive interneurons in blowflies show that activity responses rise sharply during the initial transient state after the onset of optic flow stimuli, and then decrease and stabilise to smaller steady-state values (Jung et al, 2011;Kalb et al, 2008;Suver et al, 2012). Therefore, we speculate that this kind of transient visual response occurred at the onset of each turn, and might be one of the potential factors that are responsible for the modulation of zigzagging observed only in our biased closed-loop experiment (Fig.…”

“…In D. melanogaster, optomotor response is enhanced during walking and flying when compared with the response during resting (Chiappe et al, 2010;Maimon et al, 2010). In addition, in the blowfly Lucilia spp., velocity tuning of motionsensitive neurons is broadened towards higher velocities by flight activity (Jung et al, 2011). These observations suggest that the behavioural response and the visual response of neck motor neurons to optic flow stimuli are altered with locomotion states.…”

Head and body stabilization in blowflies walking on differently structured substrates

“…One possible approach to investigate this issue may be to record the activity of optic-flow-processing neurons during stimulation with reconstructed optic flow as perceived by freely walking blowflies, as has already been done for flying flies Karmeier et al, 2006). Because behavioral activity and, in particular, locomotion can affect the response properties of these neurons to some extent (Jung et al, 2011;Chiappe et al, 2010;Maimon et al, 2010;Rosner et al, 2010), it would be desirable to make neuronal recordings in the behaving fly as has recently been successfully accomplished in the much larger locust (Fotowat et al, 2011). With this new technique, it might be possible to estimate what spatial information can be extracted from optic-flow-processing neurons during free walking.…”

Octopaminergic modulation of the visual flight speed regulator ofDrosophila

“…Studies in mice (Andermann et al, 2011;Niell and Stryker, 2010), monkeys (Moran and Desimone, 1985;Treue and Maunsell, 1996) and flies (Jung et al, 2011;Maimon et al, 2010) show that modulation of the visual processing system in particular is a common feature across taxa; however, the behavioral implications of these modulations are unknown. Increasing the sensitivity of the visual system during certain behaviors might allow these animals to react more quickly to visual disturbances through a sensory-motor feedback control loop.…”