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The Journal of Neuroscience, April 28, 2004, 24(17):4224-4232; doi:10.1523/JNEUROSCI.0381-04.2004

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Behavioral/Systems/Cognitive
A Novel Class of Neurons at the Trigeminal Subnucleus Interpolaris/Caudalis Transition Region Monitors Ocular Surface Fluid Status and Modulates Tear Production

Harumitsu Hirata,¹ Keiichiro Okamoto,¹ Akimasa Tashiro,¹ and David A. Bereiter^1,2

Departments of ¹Surgery and ²Neuroscience, Brown Medical School, Rhode Island Hospital, Providence, Rhode Island 02903

Reflex tears are produced by many conditions, one of which is drying of the ocular surface. Although peripheral neural control of the lacrimal gland is well established, the afferent pathways and properties of central premotor neurons necessary for this reflex are not known. Male rats under barbiturate anesthesia were used to determine whether neurons at the ventral trigeminal subnucleus interpolaris- caudalis (Vi/Vc) transition or the trigeminal subnucleus caudalis-cervical cord (Vc/C1) junction region in the lower brainstem were necessary for tears evoked by noxious chemical stimulation (CO₂ pulses) or drying of the ocular surface. Both the Vi/Vc transition and Vc/C1 junction regions receive a dense direct projection from corneal nociceptors. Synaptic blockade of the Vi/Vc transition, but not the Vc/C1 junction, by the GABA_A receptor agonist muscimol inhibited CO₂-evoked tears. Glutamate excitation of the Vi/Vc transition, but not the Vc/C1 junction, increased tear volume. Single units recorded at the Vi/Vc transition, but not at the Vc/C1 junction, were inhibited by wetting and excited by drying the ocular surface. Nearly all moisture-sensitive Vi/Vc units displayed an initial inhibitory phase to noxious concentrations of CO₂ followed by delayed excitation and displayed an inhibitory surround receptive field from periorbital facial skin. Drying of the ocular surface produced many Fos-positive neurons at the Vi/Vc transition, but not at the Vc/C1 junction. This is the first report of a unique class of moisture-sensitive neurons that exist only at the ventral Vi/Vc transition, and not at more caudal portions of Vc, that may underlie fluid homeostasis of the ocular surface.

Key words: cornea; dry eye; lacrimation; nociception; ocular irritation; spinal trigeminal nucleus

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Received Feb 3, 2004; revised March 18, 2004; accepted March 18, 2004.

This article has been cited by other articles:

				D. A. Bereiter, K. Okamoto, A. Tashiro, and H. Hirata Endotoxin-Induced Uveitis Causes Long-Term Changes in Trigeminal Subnucleus Caudalis Neurons J Neurophysiol, December 1, 2005; 94(6): 3815 - 3825. [Abstract] [Full Text] [PDF]

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