Microtubule Orientation to Light in Macular Cone Axons: Macular Pigment as a Polarization-Sensitive Filter That Influences Cone Alignment

Abstract

Purpose: : Because there is evidence in human retinas that macular pigment (MP) molecules are bound to microtubules, have their molecular axis perpendicular to the microtubule, and absorb light best if its electric vector is parallel to their molecular axis, microtubule orientation was examined in areas of human and monkey retinas containing MP.

Methods: : The orientation of macular cone axons and their microtubules was analysed in histological sections containing the fovea from macaque and human retinas by light microscopy (LM) and electron microscopy (EM).

Results: : By EM, the cone axons in macaque retinas had microtubules that were abundant and parallel to the axons, allowing LM to indicate microtubule orientation. By LM, at the foveal center the cone inner and outer axons were perpendicular to the outer retinal surface and parallel to incident light: the angle (β) between axons and light was 0⁰ [at retinal eccentricity (RE) of 0⁰, β = 0⁰]. At increasing RE, the cone axons were increasingly oblique so β increased [at RE of 0.06⁰, β~ 50⁰; at RE of 0.25⁰, β~ 70⁰]. At RE > 2⁰ the cone outer axons were quite parallel to the retina and perpendicular to light [β> 80⁰].

Conclusions: : Human and macaque maculas can be divided into three concentric zones (A-C) with different morphological, optical, and functional properties.(A) Foveal center has parallel microtubules: cone axon microtubules are parallel to light, so each individual microtubule has associated MP molecules whose molecular axes are parallel to, and absorb, incident light of all possible polarization planes.(B) Inner annulus has oblique microtubules: cone axon microtubules are radial on the retina and are increasingly oblique to light at increasing RE, so their MP molecules absorb tangentially polarized light plus intermediate levels of radially polarized light.(C) Outer annulus has perpendicular microtubules: cone axon microtubules are radial on the retina and perpendicular to light, so at each retinal location the axes of MP molecules are tangential and absorb only tangentially polarized light.Thus, MP associated with microtubules in human maculas acts as a polarization-sensitive filter for short wavelength light whose strength declines with eccentricity (all polarization planes are absorbed in A, some are absorbed in B, half are absorbed in C); this influences the amount of light absorbed by MP and its effective optical density.Since optical filtering by MP facilitates cone alignment in normal human eyes, a disturbance in MP orientation (or MP levels) that lowers optical filtering will disturb cone alignment and can lead to age-related macular degeneration.

Keywords: macular pigment • age-related macular degeneration • macula/fovea