TY - JOUR
T1 - A Novel Class of Neurons at the Trigeminal Subnucleus Interpolaris/ Caudalis Transition Region Monitors Ocular Surface Fluid Status and Modulates Tear Production
AU - Hirata, Harumitsu
AU - Okamoto, Keiichiro
AU - Tashiro, Akimasa
AU - Bereiter, David A.
PY - 2004/4/28
Y1 - 2004/4/28
N2 - 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 GABAA 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 CO 2 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.
AB - 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 GABAA 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 CO 2 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.
KW - Cornea
KW - Dry eye
KW - Lacrimation
KW - Nociception
KW - Ocular irritation
KW - Spinal trigeminal nucleus
UR - http://www.scopus.com/inward/record.url?scp=2442629555&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=2442629555&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.0381-04.2004
DO - 10.1523/JNEUROSCI.0381-04.2004
M3 - Article
C2 - 15115818
AN - SCOPUS:2442629555
SN - 0270-6474
VL - 24
SP - 4224
EP - 4232
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 17
ER -