High-fidelity backpropagation through primate foveal cones

Abstract

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. 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. SIGNIFICANCE STATEMENTHumans, like other primates, see a fineness of detail that eludes other mammals. This capability is used for tasks like reading and recognizing faces. It is lost in leading forms of vision impairment, such as age-related macular degeneration. Investigating it therefore provides insight into the origin of exceptional sensory performance while strengthening the foundation for preserving and restoring sight. This study examines cells that initiate high-acuity vision, the foveal cones, which produce electrical signals from light and send them forward. It reveals that electrical signals also travel effectively in reverse, from the site of transmission to that of production, and how the production of light responses may be independent nonetheless.