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 across conditions, we found that awake retinal output had in general (1) faster kinetics with less variability in the response latencies; (2) a larger dynamic range; and (3) higher firing activity, by ~20 Hz on average, for both baseline and visually evoked responses. Our modeling analyses further showed that such awake response patterns convey comparable total information but less efficiently, and allow for a linear population decoder to perform significantly better than the anesthetized or ex vivo responses. These results highlight distinct retinal behavior in awake states, in particular suggesting that the retina employs dense coding in vivo, rather than sparse efficient coding as has been often assumed from ex vivo studies.
Keywords: anesthesia; awake; efficient coding; in vivo recordings; mouse; neuroscience; retinal ganglion cells.
When light enters the eyes, it is focused onto the retina, a thin layer of brain tissue at the back of the eye. The retina converts light information into electrical signals that are transmitted to the rest of the brain to perceive vision. Unlike the rest of the brain, this light-processing tissue can continue working even when removed from an animal, making it easier for scientists to study how the retina works. This has helped it become one of the best-understood parts of the brain. Most knowledge of retinal signal processing comes from studies of isolated retinas. However, it was still unclear if these samples behave the same way as they do in live animals, and whether findings in isolated retinas apply to natural visual processing in an awake state. To determine this, Boissonnet et al. compared the visual responses of the retina in awake mice, anesthetised mice and when isolated from mice. Measurements of retinal electrical signals showed that awake mice responded to light substantially more quickly and strongly than the others. Computational analysis suggested that the amount of information carried to the brain was largely comparable across the different subjects, but the retina in awake mice used more energy. The findings indicate that further studies are needed to better understand how the retina processes visual information in awake animals, rather than just in isolated conditions. Progressing this understanding could ultimately help to develop prosthetic devices that can act as a retina in the future.
© 2023, Boissonnet et al.