PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT
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 lig...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2016-08-01
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| Series: | Frontiers in Neural Circuits |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00060/full |
| _version_ | 1818253314534408192 |
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| author | Anna Matynia Anna Matynia Eileen Nguyen Xiao-Ping Sun Frank Blixt Sachin Parikh Sachin Parikh Jason Kessler Luis Perez de Sevilla Muller Samer Habib Paul Kim Zoey Zhe Wang Allen Rodriguez Andrew Charles Andrew Charles Steven Nusinowitz Lars Edvinsson Steven Barnes Steven Barnes Nicholas Brecha Nicholas Brecha Nicholas Brecha Michael B Gorin Michael B Gorin |
| author_facet | Anna Matynia Anna Matynia Eileen Nguyen Xiao-Ping Sun Frank Blixt Sachin Parikh Sachin Parikh Jason Kessler Luis Perez de Sevilla Muller Samer Habib Paul Kim Zoey Zhe Wang Allen Rodriguez Andrew Charles Andrew Charles Steven Nusinowitz Lars Edvinsson Steven Barnes Steven Barnes Nicholas Brecha Nicholas Brecha Nicholas Brecha Michael B Gorin Michael B Gorin |
| author_sort | Anna Matynia |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-12T16:38:06Z |
| format | Article |
| id | doaj.art-db6756685cc14d90b89bb7977c0c2623 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-12-12T16:38:06Z |
| publishDate | 2016-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-db6756685cc14d90b89bb7977c0c26232022-12-22T00:18:38ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102016-08-011010.3389/fncir.2016.00060198813PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHTAnna Matynia0Anna Matynia1Eileen Nguyen2Xiao-Ping Sun3Frank Blixt4Sachin Parikh5Sachin Parikh6Jason Kessler7Luis Perez de Sevilla Muller8Samer Habib9Paul Kim10Zoey Zhe Wang11Allen Rodriguez12Andrew Charles13Andrew Charles14Steven Nusinowitz15Lars Edvinsson16Steven Barnes17Steven Barnes18Nicholas Brecha19Nicholas Brecha20Nicholas Brecha21Michael B Gorin22Michael B Gorin23UCLAUCLAUCLAUCLALund UniversityUCLAUCLAUCLAUCLAUCLAUCLAUCLAUCLAUCLAUCLAUCLALund UniversityUCLADalhousie UniversityUCLAUCLAVeterans Administration Greater Los Angeles Health SystemUCLAUCLAThe 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.http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00060/fullChoroidCorneaTrigeminal GanglionMigraineMelanopsinoptic nerve injury |
| spellingShingle | Anna Matynia Anna Matynia Eileen Nguyen Xiao-Ping Sun Frank Blixt Sachin Parikh Sachin Parikh Jason Kessler Luis Perez de Sevilla Muller Samer Habib Paul Kim Zoey Zhe Wang Allen Rodriguez Andrew Charles Andrew Charles Steven Nusinowitz Lars Edvinsson Steven Barnes Steven Barnes Nicholas Brecha Nicholas Brecha Nicholas Brecha Michael B Gorin Michael B Gorin PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT Frontiers in Neural Circuits Choroid Cornea Trigeminal Ganglion Migraine Melanopsin optic nerve injury |
| title | PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT |
| title_full | PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT |
| title_fullStr | PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT |
| title_full_unstemmed | PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT |
| title_short | PERIPHERAL SENSORY NEURONS EXPRESSING MELANOPSIN RESPOND TO LIGHT |
| title_sort | peripheral sensory neurons expressing melanopsin respond to light |
| topic | Choroid Cornea Trigeminal Ganglion Migraine Melanopsin optic nerve injury |
| url | http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00060/full |
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