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Awake responses suggest inefficient dense coding in the mouse retina

The structure and function of the vertebrate retina have been extensively studied across species with an isolated, ex vivo preparation. Retinal function in vivo, however, remains elusive, especially in awake animals. Here we performed single-unit extracellular recordings in the optic tract of head-fixed mice to compare the output of awake, anesthetized, and ex vivo retinas. While the visual response properties were overall similar, we found that awake retinal output had 1) faster kinetics with less variability in the response latencies across different cell types; and 2) higher firing activity, by ∼20 Hz on average, for both baseline and visually evoked responses. Notably, unlike the other conditions, many awake ON cells did not increase firing in response to light increments due to high baseline activity near saturation. Instead, they encoded light intensity fluctuations primarily by decreasing firing upon light decrements. In either condition, the visual message remains the same: the more spikes, the higher light intensity. The awake response patterns, however, violate efficient coding principles, predicting that sensory systems should favor firing patterns minimizing energy consumption. Our findings suggest that the retina employs dense coding in vivo, rather than sparse efficient coding as suggested from previous ex vivo studies.