This mesh of cells may explain how some blind mice can still tell day from night.
Abstract
We have discovered an expansive photoreceptive 'net' in the mouse inner retina, visualized by using an antiserum against melanopsin, a likely photopigment1,2. This immunoreactivity is evident in a subset of retinal ganglion cells that morphologically resemble those that project to the suprachiasmatic nucleus (SCN), the site of the primary circadian pacemaker3,4. Our results indicate that this bilayered photoreceptive net is anatomically distinct from the rod and cone photoreceptors of the outer retina, and suggest that it may mediate non-visual photoreceptive tasks such as the regulation of circadian rhythms.
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Main
Most SCN-projecting retinal ganglion cells express melanopsin messenger RNA5. SCN-projecting retinal gangion cells are also photosensitive6 and have spectral absorbance profiles that are characteristic of opsin-based photopigments6. The dimensions of the receptive fields of these cells are identical to those of their dendritic fields, indicating that photopigments that are capable of activating the depolarizing responses may reside in the dendrites (D. M. Berson et al., personal communication).
We have found that melanopsin, the only opsin known to exist in retinal ganglion cells, is indeed expressed in the dendrites of this small subset of retinal ganglion cells (Fig. 1). Most striking are the plexuses formed by immunopositive dendrites in the outermost and innermost laminae of the inner plexiform layer (Fig. 2). These cells form an extensive network of opsin- containing dendrites, a photoreceptive apparatus previously overlooked in the mammalian retina.
The mammalian eye must complete two distinct photoreceptive tasks: vision and irradiance detection. Vision requires a fine array of 'narrow-capture' photoreceptive elements that allows fine spatial resolution; the photoreceptors (rods and cones) and downstream inner-retinal neurons involved in vision have been well characterized. By contrast, tasks such as photic regulation of circadian rhythms require the detection of changes in ambient irradiance, for which fine spatial resolution is not only unnecessary but may even confound the system. The retinal structures required for this 'broad-capture' photoreception have so far not been identified.
One strategy to determine irradiance levels from large sectors of visual space is to sum or average the outputs of many narrow-capture photoreceptors. Alternatively, a distinct anatomical apparatus may fulfil the requirement for a broad-capture, integrating photoreceptive system. The expansive photoreceptive net described here within the inner retina could serve such a function. Moreover, this photoreceptive system could explain why photo-entrainment of circadian rhythms is abolished by bilateral eye removal, yet persists in mice that lack rods and cones7.
References
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Provencio, I., Rollag, M. & Castrucci, A. Photoreceptive net in the mammalian retina. Nature 415, 493 (2002). https://doi.org/10.1038/415493a
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DOI: https://doi.org/10.1038/415493a
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