First-order visual interneurons distribute distinct contrast and luminance information across ON and OFF pathways to achieve stable behavior.

Burak Gür,Sebastian Molina-Obando,Madhura D Ketkar,Maria Ioannidou,Carlotta Martelli,Marion Silies

doi:10.7554/elife.74937

Burak Gür, Sebastian Molina-Obando + Show 4 more

Open Access

https://doi.org/10.7554/elife.74937

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Abstract

The accurate processing of contrast is the basis for all visually guided behaviors. Visual scenes with rapidly changing illumination challenge contrast computation because photoreceptor adaptation is not fast enough to compensate for such changes. Yet, human perception of contrast is stable even when the visual environment is quickly changing, suggesting rapid post receptor luminance gain control. Similarly, in the fruit fly Drosophila, such gain control leads to luminance invariant behavior for moving OFF stimuli. Here, we show that behavioral responses to moving ON stimuli also utilize a luminance gain, and that ON-motion guided behavior depends on inputs from three first-order interneurons L1, L2, and L3. Each of these neurons encodes contrast and luminance differently and distributes information asymmetrically across both ON and OFF contrast-selective pathways. Behavioral responses to both ON and OFF stimuli rely on a luminance-based correction provided by L1 and L3, wherein L1 supports contrast computation linearly, and L3 non-linearly amplifies dim stimuli. Therefore, L1, L2, and L3 are not specific inputs to ON and OFF pathways but the lamina serves as a separate processing layer that distributes distinct luminance and contrast information across ON and OFF pathways to support behavior in varying conditions.

Highlights

IntroductionContrast information forms the basis of visual computations. Contrast is the relative change in luminance, which can be computed across space or across time
The stable computation of contrast at changing background luminance in OFF-motion guided behavior (OFF behavior) is ensured by a corrective signal from luminance-sensitive L3 neurons (Ketkar et al, 2020). It is not known whether ON-motion-driven behavior (ON behavior) requires a post-receptor luminance gain and whether L1 can provide it along with its contrast signal (Figure 1B)
Behavioral responses were measured in a fly-on-a-ball assay

Summary

Introduction

Contrast information forms the basis of visual computations. Contrast is the relative change in luminance, which can be computed across space or across time. The stable computation of contrast at changing background luminance in OFF-motion guided behavior (OFF behavior) is ensured by a corrective signal from luminance-sensitive L3 neurons (Ketkar et al, 2020) It is not known whether ON-motion-driven behavior (ON behavior) requires a post-receptor luminance gain and whether L1 can provide it along with its contrast signal (Figure 1B). Many different types of first order interneurons, bipolar cells, exist They are generally thought to capture the contrast component of the photoreceptor response, luminance information has been shown to be preserved in visual circuitry postsynaptic to photoreceptors (Awatramani and Slaughter, 2000; Ichinose and Hellmer, 2016; Ichinose and Lukasiewicz, 2007; Odermatt et al., 2012; Oesch and Diamond, 2011). Our data reveal how luminance and contrast information are distributed to both ON and OFF pathways to achieve stable visual behavior

Results

Discussion

Methods

Single-luminance edges

Mixed-contrast edges