Cellular Biophysics Underlying the Initiation of High-Acuity Vision

Abstract

Vision in humans and other primates is exceptional—its spatial acuity is the highest among mammals (~100-fold greater than mice) and its contrast sensitivity exceeds that of all animals tested (~10-fold greater than birds of prey). This performance originates in the fovea, a specialization of the retina that other mammals lack. The visual image over the fovea is resolved by cone photoreceptors that are extremely slender and tightly packed for high spatial resolution. Light has direct access to this cone array due to the lateral displacement of downstream cells. Foveal cones drive these cells by extending axons that reach up to ~400 microns in length. Visual acuity and sensitivity depend on the effective propagation of graded electrical responses through the elongated foveal cones. In this dissertation, I experimentally examine propagation through foveal cones and through the short, stout cones outside the fovea, in the peripheral retina. Simultaneous patch-clamp recordings from each end of single foveal cones revealed that these cells propagate responses with unexpectedly little distortion. Propagation was unhindered by block of voltage-gated ion channels; thus, active amplification is unnecessary. Indeed, effective propagation was exhibited by passive compartmental models built in silico, according to the responses and morphologies of recorded cones. These models indicate that two biophysical parameters optimize propagation in foveal cones: a lower membrane conductivity than that of peripheral cones, and an internal (axial) conductivity that is >1 order of magnitude higher than that reported for cones of other species. Propagation was compromised in modeled cones lacking these specializations, as well as in cones of unnaturally smaller diameter or greater length. I conclude that the slenderness and elongation of foveal cones, which are integral to the spatial resolving power of the primate fovea, are permitted by an optimization of biophysical parameters and limited by the need for effective signal propagation.