Editors' ChoicePhysiology

Photoreception is not just for neurons

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Sci. Signal.  27 Jun 2017:
Vol. 10, Issue 485, eaao1796
DOI: 10.1126/scisignal.aao1796

Muscles in the mouse iris are intrinsically sensitive to light.

Smooth muscles in the iris contract to control the diameter of the pupil in response to changes in light, a phenomenon called the pupillary light reflex (PLR). The dilator muscles around the periphery of the iris contract to enlarge the pupil in response to input from the sympathetic nervous system, and the sphincter muscle that lines the hole in the center of the iris contracts to constrict the pupil when stimulated by cholinergic parasympathetic neurons from the optic nerve. In amphibians, fish, birds, and some nocturnal mammals, there is an additional local component of the PLR that depends on the sphincter muscle but is independent of innervation. Wang et al. found that the mouse iris sphincter muscle, in addition to being responsive to acetylcholine, was also intrinsically responsive to light. Sphincter muscles excised from mice contracted in response to a flash of light or the application of acetylcholine, and light enhanced the response to acetylcholine. Blocking acetylcholine receptors did not prevent the muscles from contracting in response to light. Opn4, the gene that encodes melanopsin, was expressed in small clusters of muscle cells around the pupil, and sphincter muscles from mice in which Opn4 was specifically knocked out in smooth muscle were not responsive to light. Although Opn4 was expressed only in a small subset of sphincter muscle cells, the contractile Ca2+ signal was likely propagated throughout the muscle through gap junctions, because gap junction blockers reduced contraction of the muscle in response to light. Additional experiments with tissue from various mutant mouse lines indicated that melanopsin and acetylcholine activated similar G proteins and second messenger systems to elicit contraction of the muscle. These findings identify a population of muscle cells as photosensitive, a trait usually associated only with neurons.

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