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

Abstract

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.

Interneuron diversity and normalization specificity in a visual system

“…5b) contains a 3-cycle L3→Dm20→Lawf1→L3. Lawf1 is predicted cholinergic, consistent with transcriptomic evidence (Davis et al 2020), though immunolabeling suggests that Lawf1 is both cholinergic and glutamatergic (Yuan et al 2021). Assuming that Lawf1 excites L3, and Dm20 inhibits Lawf1, the 3-cycle is net inhibitory.…”

Organismal landscape of clock cells and circadian gene expression inDrosophila

“…The lamina wide-field feedback neurons subtype 2 (Lawf2) are relevant for orientation to visual cues and, thus far, have not been ascribed to any circadian function. Their cell bodies are located in the medulla cortex and project towards the medulla and lamina neuropils (77)(78)(79). To explore the possibility that Lawf2 cells support a functional circadian clock, we employed a characterized Lawf2 driver (80) to drive the expression of a green fluorescent reporter (GFP) to localize them within the medulla cortex of the optic lobe along with a tim fluorescent transcriptional reporter previously characterized (12).…”