Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye

After the unilateral inflammation or nerve lesion of the ocular surface, the ipsilateral corneal sensory nerve activity is activated and sensitized, evoking ocular discomfort, irritation, and pain referred to the affected eye. Nonetheless, some patients with unilateral ocular inflammation, infection...

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Autores principales:	Carolina Luna, Susana Quirce, Adolfo Aracil-Marco, Carlos Belmonte, Juana Gallar, M. Carmen Acosta
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	dry eye sensory nerve activity contralateral effects corneal inflammation corneal lesion Medicine (General) R5-920
Acceso en línea:	https://doaj.org/article/1ec639e0e56a47e1a8082e01cc54a621
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spelling	oai:doaj.org-article:1ec639e0e56a47e1a8082e01cc54a6212021-11-15T04:51:57ZUnilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye2296-858X10.3389/fmed.2021.767967https://doaj.org/article/1ec639e0e56a47e1a8082e01cc54a6212021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmed.2021.767967/fullhttps://doaj.org/toc/2296-858XAfter the unilateral inflammation or nerve lesion of the ocular surface, the ipsilateral corneal sensory nerve activity is activated and sensitized, evoking ocular discomfort, irritation, and pain referred to the affected eye. Nonetheless, some patients with unilateral ocular inflammation, infection, or surgery also reported discomfort and pain in the contralateral eye. We explored the possibility that such altered sensations in the non-affected eye are due to the changes in their corneal sensory nerve activity in the contralateral, not directly affected eye. To test that hypothesis, we recorded the impulse activity of the corneal mechano- and polymodal nociceptor and cold thermoreceptor nerve terminals in both eyes of guinea pigs, subjected unilaterally to three different experimental conditions (UV-induced photokeratitis, microkeratome corneal surgery, and chronic tear deficiency caused by removal of the main lacrimal gland), and in eyes of naïve animals ex vivo. Overall, after unilateral eye damage, the corneal sensory nerve activity appeared to be also altered in the contralateral eye. Compared with the naïve guinea pigs, animals with unilateral UV-induced mild corneal inflammation, showed on both eyes an inhibition of the spontaneous and stimulus-evoked activity of cold thermoreceptors, and increased activity in nociceptors affecting both the ipsilateral and the contralateral eye. Unilateral microkeratome surgery affected the activity of nociceptors mostly, inducing sensitization in both eyes. The removal of the main lacrimal gland reduced tear volume and increased the cold thermoreceptor activity in both eyes. This is the first direct demonstration that unilateral corneal nerve lesion, especially ocular surface inflammation, functionally affects the activity of the different types of corneal sensory nerves in both the ipsilateral and contralateral eyes. The mechanisms underlying the contralateral affectation of sensory nerves remain to be determined, although available data support the involvement of neuroimmune interactions. The parallel alteration of nerve activity in contralateral eyes has two main implications: a) in the experimental design of both preclinical and clinical studies, where the contralateral eyes cannot be considered as a control; and, b) in the clinical practice, where clinicians must consider the convenience of treating both eyes of patients with unilateral ocular conditions to avoid pain and secondary undesirable effects in the fellow eye.Carolina LunaSusana QuirceAdolfo Aracil-MarcoCarlos BelmonteJuana GallarJuana GallarM. Carmen AcostaFrontiers Media S.A.articledry eyesensory nerve activitycontralateral effectscorneal inflammationcorneal lesionMedicine (General)R5-920ENFrontiers in Medicine, Vol 8 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	dry eye sensory nerve activity contralateral effects corneal inflammation corneal lesion Medicine (General) R5-920
spellingShingle	dry eye sensory nerve activity contralateral effects corneal inflammation corneal lesion Medicine (General) R5-920 Carolina Luna Susana Quirce Adolfo Aracil-Marco Carlos Belmonte Juana Gallar Juana Gallar M. Carmen Acosta Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
description	After the unilateral inflammation or nerve lesion of the ocular surface, the ipsilateral corneal sensory nerve activity is activated and sensitized, evoking ocular discomfort, irritation, and pain referred to the affected eye. Nonetheless, some patients with unilateral ocular inflammation, infection, or surgery also reported discomfort and pain in the contralateral eye. We explored the possibility that such altered sensations in the non-affected eye are due to the changes in their corneal sensory nerve activity in the contralateral, not directly affected eye. To test that hypothesis, we recorded the impulse activity of the corneal mechano- and polymodal nociceptor and cold thermoreceptor nerve terminals in both eyes of guinea pigs, subjected unilaterally to three different experimental conditions (UV-induced photokeratitis, microkeratome corneal surgery, and chronic tear deficiency caused by removal of the main lacrimal gland), and in eyes of naïve animals ex vivo. Overall, after unilateral eye damage, the corneal sensory nerve activity appeared to be also altered in the contralateral eye. Compared with the naïve guinea pigs, animals with unilateral UV-induced mild corneal inflammation, showed on both eyes an inhibition of the spontaneous and stimulus-evoked activity of cold thermoreceptors, and increased activity in nociceptors affecting both the ipsilateral and the contralateral eye. Unilateral microkeratome surgery affected the activity of nociceptors mostly, inducing sensitization in both eyes. The removal of the main lacrimal gland reduced tear volume and increased the cold thermoreceptor activity in both eyes. This is the first direct demonstration that unilateral corneal nerve lesion, especially ocular surface inflammation, functionally affects the activity of the different types of corneal sensory nerves in both the ipsilateral and contralateral eyes. The mechanisms underlying the contralateral affectation of sensory nerves remain to be determined, although available data support the involvement of neuroimmune interactions. The parallel alteration of nerve activity in contralateral eyes has two main implications: a) in the experimental design of both preclinical and clinical studies, where the contralateral eyes cannot be considered as a control; and, b) in the clinical practice, where clinicians must consider the convenience of treating both eyes of patients with unilateral ocular conditions to avoid pain and secondary undesirable effects in the fellow eye.
format	article
author	Carolina Luna Susana Quirce Adolfo Aracil-Marco Carlos Belmonte Juana Gallar Juana Gallar M. Carmen Acosta
author_facet	Carolina Luna Susana Quirce Adolfo Aracil-Marco Carlos Belmonte Juana Gallar Juana Gallar M. Carmen Acosta
author_sort	Carolina Luna
title	Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
title_short	Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
title_full	Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
title_fullStr	Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
title_full_unstemmed	Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye
title_sort	unilateral corneal insult also alters sensory nerve activity in the contralateral eye
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/1ec639e0e56a47e1a8082e01cc54a621
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Unilateral Corneal Insult Also Alters Sensory Nerve Activity in the Contralateral Eye

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