Response propagation through photoreceptors that mediate high-acuity vision

Summary

Date: 
May 30, 2018 - 1:00pm - 2:00pm
Location: 
Northwest Building Room 243
About the Speaker
Name: 
Greg Bryman
Speaker Title: 
PhD Candidate
Speaker Affiliation: 
Do Lab

Humans and many other primates have the highest visual acuities observed in mammals (Veilleux and Kirk, 2014). This performance originates in the fovea, where the image is resolved at a fine grain by cone photoreceptors that are uniquely slender and tightly packed. Light has direct access to this photoreceptor array due to the lateral displacement of downstream cells. Foveal cones drive these cells by extending axons, called Henle fibers, that can reach half a millimeter in length (Drasdo et al., 2007; Perry and Cowey, 1988). High visual acuity depends on the effective propagation of graded electrical responses through the elongated foveal cones. However, computational modeling suggests that frequencies important to vision are attenuated several-fold by propagation (Hsu et al., 1998). We have now addressed this topic experimentally using macaque cones. Our principal approach was to make simultaneous patch-clamp recordings from the inner segment (IS) and presynaptic terminal of single cones that were dissociated from the retina, injecting currents of various waveforms into the IS and recording the membrane voltage at both sites. We found that peripheral cones had IS and terminal responses that were nearly indistinguishable, consistent with their stout shapes and short (~40 micron) axons. With regard to foveal cones, even the longest displayed effective propagation—for a stimulus at 60 Hz, IS and terminal responses differed by <20% in amplitude and phase lag. Although voltage-gated ion channels produced dynamic nonlinearities such as resonance and adaptation, blocking them did not diminish propagation. Indeed, passive compartmental models built according to the responses and morphologies of recorded cones showed propagation with little attenuation. These models indicated that one key property is a cytoplasmic resistivity that is >1 order of magnitude lower than values reported for cones of other species (Lasater et al., 1989). The characteristics of dissociated cones were similar to those of cones that we examined in the intact retina using single-site (IS) recordings. We conclude that electrotonic conduction is sufficient for high-fidelity, graded signaling that is robust to the extreme morphological variation of primate cones and is suitable for the sharp acuity of foveal vision.