March 8, 2021

Cone mitochondria act as microlenses to enhance light delivery and confer Stiles-Crawford-like direction sensitivity

Sensory systems that efficiently transduce physical energy into biochemical signaling are advantageous for survival. The vertebrate retina poses a challenge to such efficiency, featuring an inverted structure with multiple neural layers through which photons must pass-risking premature absorption or scattering-prior to detection. Multiple structural specializations may compensate for this challenge by removing scattering elements from the light path (fovea) or even serving as light gathering elements (rod nuclei, Muller cells, oil droplets). However, mammalian photoceptors hold numerous mitochondria in the ellipsoid region immediately before photoreceptor outer segments (OS), where light-sensitive opsin molecules are housed. These mitochondria are needed for the high metabolic demands of phototransduction, but it is yet unknown whether they increase light capture or instead diminish light delivery due to scattering by their complex membrane structure. Here, we demonstrate, via direct live imaging and computational modeling of ground squirrel cones, that such tightly packed mitochondria indeed concentrate light to enter the OS for detection. Intriguingly, this "microlens"-like feature of cone mitochondria also produces an angular dependence of light intensity, quantitively consistent with the Stiles-Crawford effect-a psychophysical phenomenon believed to improve visual resolution. We thus establish an unconventional optic function for cone mitochondria, which provides needed insights for the interpretation of their role in noninvasive optical tools for vision research and ophthalmology clinics.

 bioRxiv Subject Collection: Neuroscience

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