Ultraviolet irradiation of the eye and Fos-positive neurons induced in trigeminal brainstem after intravitreal or ocular surface transient receptor potential vanilloid 1 activation

Z. Chang; K. Okamoto; A. Tashiro; D. A. Bereiter

doi:10.1016/j.neuroscience.2010.07.019

Ultraviolet irradiation of the eye and Fos-positive neurons induced in trigeminal brainstem after intravitreal or ocular surface transient receptor potential vanilloid 1 activation

Z. Chang, K. Okamoto, A. Tashiro, D. A. Bereiter

Diagnostic and Biological Sciences

Research output: Contribution to journal › Article › peer-review

9 Scopus citations

Abstract

The interior structures of the eye are well supplied by the trigeminal nerve; however, the function of these afferent fibers is not well defined. The aim of this study was to use c-fos like immunohistochemistry (Fos-LI) to map the trigeminal brainstem complex after intravitreal microinjection or ocular surface application of capsaicin, a selective transient receptor potential vanilloid 1 (TRPV1) agonist in male rats under barbiturate anesthesia. The effect of ocular inflammation on Fos-LI was tested 2 or 7 days after UV irradiation of the eye. In non-inflamed controls, intravitreal capsaicin produced peaks of Fos-LI at the trigeminal subnucleus interpolaris/caudalis (Vi/Vcvl) transition and in superficial laminae at the caudalis/upper cervical cord (Vc/C1) junction regions. At the Vc/C1 junction intravitreal capsaicin induced Fos-LI in a dose-dependent manner, while at the Vi/Vcvl transition responses were similar after vehicle or capsaicin injections. Two days, but not 7 days, after UV irradiation intravitreal and ocular surface capsaicin-evoked Fos-LI at the Vc/C1 junction and nucleus tractus solitarius (NTS) were markedly enhanced, whereas the responses at the Vi/Vcvl transition were not different from non-inflamed controls. More than 80% of trigeminal ganglion neurons labeled after intravitreal microinjection of Fluorogold also expressed immunoreactivity for the TRPV1 receptor. These findings suggested that most intraocular trigeminal sensory nerves serve as nociceptors. The similar pattern and magnitude of Fos-LI after capsaicin suggested that TRPV1-responsive trigeminal nerves that supply intraocular and ocular surface tissues form a unified integrative circuit in the caudal brainstem. Intensity coding of capsaicin concentration and facilitation of Fos-LI expression after UV irradiation strongly supported the hypothesis that the Vc/C1 junction was critical for nociceptive processing related to ocular pain, whereas the Vi/Vcvl transition region likely served other functions in ocular homeostasis under naïve and inflamed conditions.

Original language	English (US)
Pages (from-to)	678-685
Number of pages	8
Journal	Neuroscience
Volume	170
Issue number	2
DOIs	https://doi.org/10.1016/j.neuroscience.2010.07.019
State	Published - Oct 13 2010

Bibliographical note

Funding Information:
The authors thank R. Thompson and P. Simone for excellent technical assistance. The authors have no financial or other relationships to report that might lead to a conflict of interest. This work was supported by a grant from the NIH ( NS26137 ).

Keywords

C-fos
Ocular inflammation
Trigeminal subnucleus caudalis
UV irradiation

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10.1016/j.neuroscience.2010.07.019

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title = "Ultraviolet irradiation of the eye and Fos-positive neurons induced in trigeminal brainstem after intravitreal or ocular surface transient receptor potential vanilloid 1 activation",

abstract = "The interior structures of the eye are well supplied by the trigeminal nerve; however, the function of these afferent fibers is not well defined. The aim of this study was to use c-fos like immunohistochemistry (Fos-LI) to map the trigeminal brainstem complex after intravitreal microinjection or ocular surface application of capsaicin, a selective transient receptor potential vanilloid 1 (TRPV1) agonist in male rats under barbiturate anesthesia. The effect of ocular inflammation on Fos-LI was tested 2 or 7 days after UV irradiation of the eye. In non-inflamed controls, intravitreal capsaicin produced peaks of Fos-LI at the trigeminal subnucleus interpolaris/caudalis (Vi/Vcvl) transition and in superficial laminae at the caudalis/upper cervical cord (Vc/C1) junction regions. At the Vc/C1 junction intravitreal capsaicin induced Fos-LI in a dose-dependent manner, while at the Vi/Vcvl transition responses were similar after vehicle or capsaicin injections. Two days, but not 7 days, after UV irradiation intravitreal and ocular surface capsaicin-evoked Fos-LI at the Vc/C1 junction and nucleus tractus solitarius (NTS) were markedly enhanced, whereas the responses at the Vi/Vcvl transition were not different from non-inflamed controls. More than 80% of trigeminal ganglion neurons labeled after intravitreal microinjection of Fluorogold also expressed immunoreactivity for the TRPV1 receptor. These findings suggested that most intraocular trigeminal sensory nerves serve as nociceptors. The similar pattern and magnitude of Fos-LI after capsaicin suggested that TRPV1-responsive trigeminal nerves that supply intraocular and ocular surface tissues form a unified integrative circuit in the caudal brainstem. Intensity coding of capsaicin concentration and facilitation of Fos-LI expression after UV irradiation strongly supported the hypothesis that the Vc/C1 junction was critical for nociceptive processing related to ocular pain, whereas the Vi/Vcvl transition region likely served other functions in ocular homeostasis under na{\"i}ve and inflamed conditions.",

keywords = "C-fos, Ocular inflammation, Trigeminal subnucleus caudalis, UV irradiation",

author = "Z. Chang and K. Okamoto and A. Tashiro and Bereiter, {D. A.}",

note = "Funding Information: The authors thank R. Thompson and P. Simone for excellent technical assistance. The authors have no financial or other relationships to report that might lead to a conflict of interest. This work was supported by a grant from the NIH ( NS26137 ).",

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AU - Chang, Z.

AU - Okamoto, K.

AU - Tashiro, A.

AU - Bereiter, D. A.

N1 - Funding Information: The authors thank R. Thompson and P. Simone for excellent technical assistance. The authors have no financial or other relationships to report that might lead to a conflict of interest. This work was supported by a grant from the NIH ( NS26137 ).

PY - 2010/10/13

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N2 - The interior structures of the eye are well supplied by the trigeminal nerve; however, the function of these afferent fibers is not well defined. The aim of this study was to use c-fos like immunohistochemistry (Fos-LI) to map the trigeminal brainstem complex after intravitreal microinjection or ocular surface application of capsaicin, a selective transient receptor potential vanilloid 1 (TRPV1) agonist in male rats under barbiturate anesthesia. The effect of ocular inflammation on Fos-LI was tested 2 or 7 days after UV irradiation of the eye. In non-inflamed controls, intravitreal capsaicin produced peaks of Fos-LI at the trigeminal subnucleus interpolaris/caudalis (Vi/Vcvl) transition and in superficial laminae at the caudalis/upper cervical cord (Vc/C1) junction regions. At the Vc/C1 junction intravitreal capsaicin induced Fos-LI in a dose-dependent manner, while at the Vi/Vcvl transition responses were similar after vehicle or capsaicin injections. Two days, but not 7 days, after UV irradiation intravitreal and ocular surface capsaicin-evoked Fos-LI at the Vc/C1 junction and nucleus tractus solitarius (NTS) were markedly enhanced, whereas the responses at the Vi/Vcvl transition were not different from non-inflamed controls. More than 80% of trigeminal ganglion neurons labeled after intravitreal microinjection of Fluorogold also expressed immunoreactivity for the TRPV1 receptor. These findings suggested that most intraocular trigeminal sensory nerves serve as nociceptors. The similar pattern and magnitude of Fos-LI after capsaicin suggested that TRPV1-responsive trigeminal nerves that supply intraocular and ocular surface tissues form a unified integrative circuit in the caudal brainstem. Intensity coding of capsaicin concentration and facilitation of Fos-LI expression after UV irradiation strongly supported the hypothesis that the Vc/C1 junction was critical for nociceptive processing related to ocular pain, whereas the Vi/Vcvl transition region likely served other functions in ocular homeostasis under naïve and inflamed conditions.

AB - The interior structures of the eye are well supplied by the trigeminal nerve; however, the function of these afferent fibers is not well defined. The aim of this study was to use c-fos like immunohistochemistry (Fos-LI) to map the trigeminal brainstem complex after intravitreal microinjection or ocular surface application of capsaicin, a selective transient receptor potential vanilloid 1 (TRPV1) agonist in male rats under barbiturate anesthesia. The effect of ocular inflammation on Fos-LI was tested 2 or 7 days after UV irradiation of the eye. In non-inflamed controls, intravitreal capsaicin produced peaks of Fos-LI at the trigeminal subnucleus interpolaris/caudalis (Vi/Vcvl) transition and in superficial laminae at the caudalis/upper cervical cord (Vc/C1) junction regions. At the Vc/C1 junction intravitreal capsaicin induced Fos-LI in a dose-dependent manner, while at the Vi/Vcvl transition responses were similar after vehicle or capsaicin injections. Two days, but not 7 days, after UV irradiation intravitreal and ocular surface capsaicin-evoked Fos-LI at the Vc/C1 junction and nucleus tractus solitarius (NTS) were markedly enhanced, whereas the responses at the Vi/Vcvl transition were not different from non-inflamed controls. More than 80% of trigeminal ganglion neurons labeled after intravitreal microinjection of Fluorogold also expressed immunoreactivity for the TRPV1 receptor. These findings suggested that most intraocular trigeminal sensory nerves serve as nociceptors. The similar pattern and magnitude of Fos-LI after capsaicin suggested that TRPV1-responsive trigeminal nerves that supply intraocular and ocular surface tissues form a unified integrative circuit in the caudal brainstem. Intensity coding of capsaicin concentration and facilitation of Fos-LI expression after UV irradiation strongly supported the hypothesis that the Vc/C1 junction was critical for nociceptive processing related to ocular pain, whereas the Vi/Vcvl transition region likely served other functions in ocular homeostasis under naïve and inflamed conditions.

KW - C-fos

KW - Ocular inflammation

KW - Trigeminal subnucleus caudalis

KW - UV irradiation

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Ultraviolet irradiation of the eye and Fos-positive neurons induced in trigeminal brainstem after intravitreal or ocular surface transient receptor potential vanilloid 1 activation

Abstract

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Keywords

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