Noise-robust recognition of wide-field motion direction and the underlying neural mechanisms in Drosophila melanogaster

Abstract

Appropriate and robust behavioral control in a noisy environment is important for the survival of most organisms. Understanding such robust behavioral control has been an attractive subject in neuroscience research. Here, we investigated the processing of wide-field motion with random dot noise at both the behavioral and neuronal level in Drosophila melanogaster. We measured the head yaw optomotor response (OMR) and the activity of motion-sensitive neurons, horizontal system (HS) cells, with in vivo whole-cell patch clamp recordings at various levels of noise intensity. We found that flies had a robust sensation of motion direction under noisy conditions, while membrane potential changes of HS cells were not correlated with behavioral responses. By applying signal classification theory to the distributions of HS cell responses, however, we found that motion direction under noise can be clearly discriminated by HS cells, and that this discrimination performance was quantitatively similar to that of OMR. Furthermore, we successfully reproduced HS cell activity in response to noisy motion stimuli with a local motion detector model including a spatial filter and threshold function. This study provides evidence for the physiological basis of noise-robust behavior in a tiny insect brain.

Dopamine modulates the optomotor response to unreliable visual stimuli in Drosophila melanogaster

“…We evaluated the head yaw response over a range of SNRs (Figure ). Wild‐type flies reacted obviously to motion stimuli that included a substantial amount of noise, as described previously (Figure c, CS, Suzuki et al, ). The head‐turning angle of each fly was normalized by the average head‐turning angle during stimulation without noise in the same fly, and thus, the normalized response indicated how well the response was maintained during the stimulus that included noise, despite the maximum OMR.…”

“…We used an LED insect arena system (Metrix Technology Corp., New York, NY, USA) for visual stimuli, as described previously (Suzuki et al, ). Briefly, we presented the flies with horizontally moving stripe patterns with and without a random dot pattern, which was independent from frame to frame.…”

“…We measured the head yaw angle as an indicator of the OMR as described previously (Kikuchi et al, 2012;Suzuki et al, 2015). Briefly, cold-anaesthetized flies were tethered at the thorax to a steel pin with glue.…”

“…[Colour figure can be viewed at wileyonlinelibrary.com] shown in Figure 1a, the flies turned their heads towards the direction of motion during the stimulus presentation. To quantify the response, we measured the head yaw angle as an index of the OMR, as described in previous studies (Kikuchi et al, 2012;Suzuki et al, 2015). We controlled the SNR of the motion in the stimulus to test the effects of less reliable stimuli on the perception of wide-field motion.…”

“…A number of researchers have studied on the neural mechanisms underlying the OMR (Egelhaaf & Borst, ; Joesch, Plett, Borst, & Reiff, ). We previously reported that flies have a robust perception of wide‐field motion stimuli that contain noise (Suzuki et al, ). Here, we investigated whether and how the OMR to stimuli with and without noise can be modulated by DA.…”