Paradoxical Rules of Spike Train Decoding Revealed at the Sensitivity Limit of Vision

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. Wemeasured
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.