Bright light activates a trigeminal nociceptive pathway.
Bright light can cause ocular discomfort and/or pain; however, the mechanism linking luminance to trigeminal nerve activity is not known. In this study we identify a novel reflex circuit necessary for bright light to excite nociceptive neurons in superficial laminae of trigeminal subnucleus caudalis (Vc/C1). Vc/C1 neurons encoded light intensity and displayed a long delay (>10s) for activation. Microinjection of lidocaine into the eye or trigeminal root ganglion (TRG) inhibited light responses completely, whereas topical application onto the ocular surface had no effect. These findings indicated that light-evoked Vc/C1 activity was mediated by an intraocular mechanism and transmission through the TRG. Disrupting local vasomotor activity by intraocular microinjection of the vasoconstrictive agents, norepinephrine or phenylephrine, blocked light-evoked neural activity, whereas ocular surface or intra-TRG microinjection of norepinephrine had no effect. Pupillary muscle activity did not contribute since light-evoked responses were not altered by atropine. Microinjection of lidocaine into the superior salivatory nucleus diminished light-evoked Vc/C1 activity and lacrimation suggesting that increased parasympathetic outflow was critical for light-evoked responses. The reflex circuit also required input through accessory visual pathways since both Vc/C1 activity and lacrimation were prevented by local blockade of the olivary pretectal nucleus. These findings support the hypothesis that bright light activates trigeminal nerve activity through an intraocular mechanism driven by a luminance-responsive circuit and increased parasympathetic outflow to the eye.
Okamoto
Keiichiro
K
Department of Diagnostic and Biological Sciences, University of Minnesota School of Dentistry, 18-214 Moos Tower, 515 Delaware St. SE, Minneapolis, MN 55455, USA.
Tashiro
Akimasa
A
Chang
Zheng
Z
Bereiter
David A
DA
D000344:Afferent Pathways / Q000503:physiopathology / Q000528:radiation effects; D000779:Anesthetics, Local / Q000494:pharmacology; D000818:Animals; D006261:Headache / Q000209:etiology / Q000503:physiopathology*; D008027:Light / Q000009:adverse effects*; D008297:Male; D009619:Nociceptors / Q000528:radiation effects; D009880:Ophthalmic Artery / Q000294:innervation / Q000503:physiopathology; D009882:Ophthalmic Nerve / Q000503:physiopathology / Q000528:radiation effects; D010146:Pain / Q000209:etiology / Q000503:physiopathology*; D010275:Parasympathetic Nervous System / Q000187:drug effects / Q000502:physiology; D020795:Photophobia / Q000209:etiology / Q000503:physiopathology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D012039:Regional Blood Flow / Q000187:drug effects / Q000502:physiology; D012249:Rhombencephalon / Q000187:drug effects / Q000502:physiology; D014275:Trigeminal Caudal Nucleus / Q000503:physiopathology / Q000528:radiation effects; D012668:Trigeminal Ganglion / Q000503:physiopathology / Q000528:radiation effects; D014276:Trigeminal Nerve / Q000503:physiopathology* / Q000528:radiation effects*; D014662:Vasoconstrictor Agents / Q000494:pharmacology; D014664:Vasodilation / Q000187:drug effects / Q000502:physiology; D014795:Visual Pathways / Q000187:drug effects / Q000503:physiopathology
D000779:Anesthetics, Local; D014662:Vasoconstrictor Agents