Retinal OFF ganglion cells allow detection of quantal shadows at starlight

Abstract

SUMMARYPerception of light in darkness requires no more than a handful of photons and this remarkable behavioral performance can be directly linked to a particular retinal circuit – the retinal ON pathway. However, the neural limits to shadow detection in very dim light have remained unresolved. Here, we unravel the neural mechanisms that determine the sensitivity of mice to the dimmest light decrements by measuring signals from the most sensitive ON and OFF retinal ganglion cell types and by correlating their signals with visually guided behavior. We show that mice can detect shadows when only a few photon absorptions are missing among thousands of rods. Behavioral detection of “quantal” shadows relies only on the retinal OFF pathway and is limited by noise and losses of single-photon signals in retinal processing. Thus, in the dim-light regime, light increments and decrements are encoded separately via the ON and OFF retinal pathways, respectively.

Reconfiguration of the visual code and retinal cell type complement in closely related diurnal and nocturnal mice

“…OFF BCs respond faster than ON BCs, allowing the possibility not only for faster visual reflexes but also higher acuity 43 . As a day active species, Rhabdomys may place a higher premium on detecting shadows (attributed to OFF pathways 44 ) and in a more general sense the negative spatial contrast to which natural scenes are biased 45 than high sensitivity vision (attributed to ON pathways 46 ). Finally, the enhanced capacity of OFF pathways could support better ability to detect overhead (dark) looming stimuli indicative of aerial predators 47 .…”

Human retina trades single-photon detection for high-fidelity contrast encoding

“…This result shows that retinal ON and OFF pathways carry out distinct functional roles for visually-guided behavior at visual threshold, such that behavior relies on the information encoded by increased firing rates of the ON cells for detection of light increments. It remains to be seen if behavioral detection of the weakest light decrements relies on the retinal OFF pathway, as our recent results on mice suggest 13 . Earlier results on primates at photopic light levels indeed suggest that light increments are encoded by ON RGCs and light decrements by OFF RGCs 14 .…”