High-Fidelity Backpropagation through Primate Foveal Cones

Primate vision has exceptionally high spatial acuity and contrast sensitivity. This performance originates in specialized photoreceptors of the fovea. These cones transduce light into electrical signals in the outer segment, and convey these signals to the presynaptic terminal for transmission. Backpropagating signals are also possible, as the terminal receives inputs. Such signals could influence phototransduction itself. To test this idea, we recorded electrophysiologically from both ends of single cones dissociated from the macaque fovea (either sex). We found that backpropagation was effective despite the extreme slenderness and length of these cells. Backpropagation was also effective in a passive compartmental model, indicating that amplification by voltage-gated channels is not required. We then modeled foveal cones receiving terminal inputs from retinal networks. Despite faithful backpropagation of these inputs, they appear unlikely to influence phototransduction. Thus, even though foveal cones exhibit effective backpropagation, their encoding of visual information may remain compartmentalized.