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openaire: EC/H2020/713645/EU//BioMEP All sensory information is encoded in neural spike trains. It is unknown how the brain utilizes this neural code to drive behavior. Here, we unravel the decoding rules of the brain at the most elementary level by linking behavioral decisions to retinal output signals in a single-photon detection task. A transgenic mouse line allowed us to separate the two primary retinal outputs, ON and OFF pathways, carrying information about photon absorptions as increases and decreases in spiking, respectively. We measured the sensitivity limit of rods and the most sensitive ON and OFF ganglion cells and correlated these results with visually guided behavior using markerless head and eye tracking. We show that behavior relies only on the ON pathway even when the OFF pathway would allow higher sensitivity. Paradoxically, behavior does not rely on the spike code with maximal information but instead relies on a decoding strategy based on increases in spiking. Smeds et al. combine retinal ganglion cell recordings with markerless tracking of mouse behavior in photon detection. They show that behavior relies on information presented as increased spiking activity rather than the spike code carrying the maximal information.

Previous studies of the ferret visual cortex indicate that the development of direction selectivity requires visual experience. Here, we used two-photon calcium imaging to study the development of direction selectivity in layer 2/3 neurons of the mouse visual cortex in vivo. Surprisingly, just after eye opening nearly all orientation-selective neurons were also direction selective. During later development, the number of neurons responding to drifting gratings increased in parallel with the fraction of neurons that were orientation, but not direction, selective. Our experiments demonstrate that direction selectivity develops normally in dark-reared mice, indicating that the early development of direction selectivity is independent of visual experience. Furthermore, remarkable functional similarities exist between the development of direction selectivity in cortical neurons and the previously reported development of direction selectivity in the mouse retina. Together, these findings provide strong evidence that the development of orientation and direction selectivity in the mouse brain is distinctly different from that in ferrets.