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Front Neural Circuits. 2016 Aug 10;10:60. doi: 10.3389/fncir.2016.00060. eCollection 2016.

Peripheral Sensory Neurons Expressing Melanopsin Respond to Light.

Author information

1
Department of Ophthalmology, Jules Stein Eye Institute, David Geffen School of Medicine, UCLALos Angeles, CA, USA; Brain Research Institute, UCLALos Angeles, CA, USA.
2
Department of Ophthalmology, Jules Stein Eye Institute, David Geffen School of Medicine, UCLA Los Angeles, CA, USA.
3
Department of Neurobiology and Medicine, David Geffen School of Medicine, UCLA Los Angeles, CA, USA.
4
Division of Experimental Vascular Research, Department of Clinical Sciences, Lund University Lund, Sweden.
5
Brain Research Institute, UCLALos Angeles, CA, USA; Department of Neurology, David Geffen School of Medicine, UCLALos Angeles, CA, USA.
6
Department of Neurobiology and Medicine, David Geffen School of Medicine, UCLALos Angeles, CA, USA; Departments of Physiology & Biophysics and Ophthalmology and Visual Sciences, Dalhousie UniversityHalifax, NS, Canada.
7
Brain Research Institute, UCLALos Angeles, CA, USA; Department of Neurobiology and Medicine, David Geffen School of Medicine, UCLALos Angeles, CA, USA; Veterans Administration Greater Los Angeles Health SystemLos Angeles, CA, USA.

Abstract

The ability of light to cause pain is paradoxical. The retina detects light but is devoid of nociceptors while the trigeminal sensory ganglia (TG) contain nociceptors but not photoreceptors. Melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) are thought to mediate light-induced pain but recent evidence raises the possibility of an alternative light responsive pathway independent of the retina and optic nerve. Here, we show that melanopsin is expressed in both human and mouse TG neurons. In mice, they represent 3% of small TG neurons that are preferentially localized in the ophthalmic branch of the trigeminal nerve and are likely nociceptive C fibers and high-threshold mechanoreceptor Aδ fibers based on a strong size-function association. These isolated neurons respond to blue light stimuli with a delayed onset and sustained firing, similar to the melanopsin-dependent intrinsic photosensitivity observed in ipRGCs. Mice with severe bilateral optic nerve crush exhibit no light-induced responses including behavioral light aversion until treated with nitroglycerin, an inducer of migraine in people and migraine-like symptoms in mice. With nitroglycerin, these same mice with optic nerve crush exhibit significant light aversion. Furthermore, this retained light aversion remains dependent on melanopsin-expressing neurons. Our results demonstrate a novel light-responsive neural function independent of the optic nerve that may originate in the peripheral nervous system to provide the first direct mechanism for an alternative light detection pathway that influences motivated behavior.

KEYWORDS:

choroid; cornea; ipRGC; migraine; optic nerve injury; sensory ganglion

PMID:
27559310
PMCID:
PMC4978714
DOI:
10.3389/fncir.2016.00060
[Indexed for MEDLINE]
Free PMC Article

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