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

• Published in: Journal of neurochemistry 2021-01, Vol.156 (1), p.59-75
• Main Authors: Yuan, Deliang, Ji, Xiaoxiao, Hao, Shun, Gestrich, Julia Yvonne, Duan, Wenlan, Wang, Xinwei, Xiang, Yuanhang, Yang, Jihua, Hu, Pengbo, Xu, Mengbo, Liu, Li, Wei, Hongying
• Format: Article
• Language: English
• Subjects: Animals; Bandpass; bandpass response; Brain - physiology; Chloride ions; Drosophila; Drosophila melanogaster; Feedback; feedback neurons; Flicker; flicker‐induced orientation; frequency; Frequency spectrum; Fruit flies; Glutamatergic transmission; Insects; Ion channels; Neuromodulation; Neurons; Neurons - physiology; Orientation; Orientation behavior; Orientation, Spatial - physiology; Photic Stimulation; Picrotoxin; Visual perception; Visual Perception - physiology; Visual stimuli
• ISSN: 0022-3042; 1471-4159
• DOI: 10.1111/jnc.15036

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. Free walking fruit flies exhibited bandpass orientation responses to flicking stripes of different frequencies, which peaked at 2–4 Hz. This flicking stripe‐induced visual orientation is mediated by retinal R1‐R6 cells and the downstream lamina monopolar neurons, particularly L1 and L2 neurons, and could be modulated by lamina feedback neurons, such as Lawf1. In vivo inactivating Lawf1 neurons enhanced the orientation response to high frequency flicking stripes, while in vitro activating Lawf1 neurons inhibited calcium activities in both L1 and L2 neurons through glutamate‐gated chloride channels. This study provides a putative mechanism for generating proper frequency dependent responses.