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.

Highlights

  • Of wide-field motion-sensitive neurons called lobula plate tangential cells (LPTCs)[10,11]

  • Our results obtained with signal classification theory, receiver operating characteristic (ROC) analysis, revealed that flies robustly process wide-field motion direction even if the stimulus contains a considerable amount of noise, and that the discriminative performance of horizontal system (HS) cell activity to motion directions revealed by ROC analysis accounts for this noise-robust sensation

  • A number of studies of the visual system have focused on robust information processing by investigating the effects of photon and motion noise[21,22,23]

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Summary

Introduction

Of wide-field motion-sensitive neurons called lobula plate tangential cells (LPTCs)[10,11]. LPTCs involve three horizontal system (HS) cells that respond to horizontal wide-field motion stimuli[9,12]. Response properties of either HS cells or the OMR in relation to several stimulus features such as speed, contrast, and pattern of motion stimulus have been thoroughly investigated. Few studies have simultaneously investigated both the OMR and HS cell activity in response to motion stimuli with added noise, and the relationship between the OMR and HS activity in this context remains poorly understood. We studied the properties of the OMR in response to wide-field motion stimuli with random dot noise and compared it with the neural activity of HS cells. This study provides a physiological basis for robust processing of wide-field motion stimuli with noise

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