Lamina feedback neurons regulate the bandpass property of the flicker-induced orientation response in Drosophila

Natural scenes contain complex visual cues with specific features, including color, motion, flicker, and position. It is critical to understand how different visual features are processed at the early stages of visual perception to elicit appropriate cellular responses, and even behavioral output. Here, we studied the visual orientation response induced by flickering stripes in a novel behavioral paradigm in Drosophila melanogaster. We found that free walking flies exhibited bandpass orientation response to flickering stripes of different frequencies. The most sensitive frequency spectrum was confined to low frequencies of 2–4 Hz. Through genetic silencing, we showed that lamina L1 and L2 neurons, which receive visual inputs from R1 to R6 neurons, were the main components in mediating flicker-induced orientation behavior. Moreover, specific blocking of different types of lamina feedback neurons Lawf1, Lawf2, C2, C3, and T1 modulated orientation responses to flickering stripes of particular frequencies, suggesting that bandpass orientation response was generated through cooperative modulation of lamina feedback neurons. Furthermore, we found that lamina feedback neurons Lawf1 were glutamatergic. Thermal activation.of Lawf1 neurons could suppress neural activities in L1 and L2 neurons, which could be blocked by the glutamate-gated chloride channel inhibitor picrotoxin (PTX). In summary, lamina monopolar neurons L1 and L2 are the primary components in mediating flicker-induced orientation response. Meanwhile, lamina feedback neurons cooperatively modulate the orientation response in a frequency-dependent way, which might be achieved through modulating neural activities of L1 and L2 neurons.

自然场景包含具有特定特征的复杂视觉线索，包括颜色、运动、闪烁和位置。了解不同视觉特征在视觉感知的早期阶段是如何被处理以引发适当的细胞反应，甚至行为输出是至关重要的。在此，我们在黑腹果蝇的一种新型行为范式中研究了由闪烁条纹诱导的视觉定向反应。我们发现自由行走的果蝇对不同频率的闪烁条纹表现出带通定向反应。最敏感的频谱局限于2 - 4Hz的低频。通过基因沉默，我们表明从R1到R6神经元接收视觉输入的薄板L1和L2神经元是介导闪烁诱导的定向行为的主要成分。此外，对不同类型的薄板反馈神经元Lawf1、Lawf2、C2、C3和T1的特异性阻断调节了对特定频率闪烁条纹的定向反应，这表明带通定向反应是通过薄板反馈神经元的协同调节产生的。此外，我们发现薄板反馈神经元Lawf1是谷氨酸能的。Lawf1神经元的热激活能够抑制L1和L2神经元的神经活动，这可以被谷氨酸门控氯离子通道抑制剂印防己毒素（PTX）阻断。总之，薄板单极神经元L1和L2是介导闪烁诱导的定向反应的主要成分。同时，薄板反馈神经元以频率依赖的方式协同调节定向反应，这可能是通过调节L1和L2神经元的神经活动来实现的。