Multifaceted luminance gain control beyond photoreceptors in Drosophila

Animals navigating in natural environments must handle vast changes in their sensory input. Visual systems, for example, handle changes in luminance at many timescales, from slow changes across the day to rapid changes during active behavior. To maintain luminance-invariant perception, visual systems must adapt their sensitivity to changing luminance at different timescales. We demonstrate that luminance gain control in photoreceptors alone is insufficient to explain luminance invariance at both fast and slow timescales and reveal the algorithms that adjust gain past photoreceptors in the fly eye. We combined imaging and behavioral experiments with computational modeling to show that downstream of photoreceptors, circuitry taking input from the single luminance-sensitive neuron type L3 implements gain control at fast and slow timescales. This computation is bidirectional in that it prevents the underestimation of contrasts in low luminance and overestimation in high luminance. An algorithmic model disentangles these multifaceted contributions and shows that the bidirectional gain control occurs at both timescales. The model implements a nonlinear interaction of luminance and contrast to achieve gain correction at fast timescales and a dark-sensitive channel to improve the detection of dim stimuli at slow timescales. Together, our work demonstrates how a single neuronal channel performs diverse computations to implement gain control at multiple timescales that are together important for navigation in natural environments. [Display omitted] •Luminance-invariant behavior uses fast and slow gain control beyond photoreceptors•Absolute luminance-sensitive L3 neurons mediate both gain increments and decrements•A computational model disentangles the L3-mediated gain correction by timescales•Gain control by the L3 pathway is bidirectional at both fast and slow timescales Combining fly behavior, in vivo imaging, and computational modeling, Ketkar and Shao et al. uncover distinct luminance gain control operations occurring downstream of the luminance-sensitive L3 neurons. This multifaceted gain control achieves luminance-invariant behavior at both fast and slow timescales and improves dim light vision.