Corneal sensory pathway in the rat: A horseradish peroxidase tracing study

Abstract

The methods of transganglionic transport of horseradish peroxidase (HRP) and horseradish peroxidase--wheat germ agglutinin (HRP-WGA) were used to determine the location within the trigeminal ganglion of the primary afferent neurons that innervate the rat central cornea, and the brainstem and spinal cord termination sites of these cells. In each of 18 animals, solutions of HRP or HRP-WGA were applied to the scarified corneal surface and allowed to infiltrate into the corneal epithelium and stroma for 15 minutes. Postmortem examination of the corneal whole mounts from the experimental animals, and of corneas and neural tissues from several control animals, showed that the HRP/HRP-WGA remained confined to the central cornea with no spread into adjacent intra- or extraorbital tissues. HRP-labeled corneal afferent somata were located in the dorsal part of the ophthalmic region of the ipsilateral trigeminal ganglion. The central fibers of the corneal afferent neurons projected very heavily to interstitial nuclei of Cajal in the spinal tract of V at the level of caudal pars interpolaris and rostral pars caudalis, lightly to the pars caudalis/C1 transition zone, and sparsely to the dorsal horn of spinal cord segments C1-C3. The trigeminal main sensory nucleus, pars oralis, the rostral three-fourths of pars interpolaris, and an extensive midregion of pars caudalis were totally devoid of reaction product. Terminal fields in caudal pars caudalis and in the spinal cord dorsal horn were concentrated largely in the outer half of lamina II, with lesser accumulations in lamina I, the deeper half of lamina II, and in lamina III. The present study demonstrates for the first time by means of an anatomical tracing procedure the brainstem termination sites of corneal afferent neurons in the rat. The patchy, discontinuous nature of the corneal afferent projection to the caudal trigeminal brainstem nuclear complex (TBNC), and the total lack of corneal projections to rostral subdivisions of the TBNC, provide an exception to the general rule of trigeminal organization in which most areas of the head and face are represented as continuous columns throughout the rostrocaudal extent of the ipsilateral TBNC.

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

“…and Burton, 1981;Marfurt and del Toro, 1987;Anton and Peppel, 1991;Takemura et al, 1991;Lu et al, 1993;Strassman and Vos, 1993;Strassman et al, 1994;Meng and Bereiter, 1996;Gong et al, 2003). Noxious sensory input from other trigeminal structures such as the temporomandibular joint (Hathaway et al, 1995) and masseter muscle (Ikeda et al, 2003), however, also activates neurons at the ventral Vi/Vc transition, suggesting a broader role in trigeminal nociception.…”

“…This has led to the proposal that different subnuclei of the Vsp serve different aspects of trigeminal function (Renehan and Jacquin, 1993;Bereiter et al, 2000;Sessle, 2000). In rodents the ocular surface is represented mainly at two spatially distinct regions: the trigeminal subnucleus interpolaris-caudalis (Vi/Vc) transition and subnucleus caudalis-upper cervical spinal cord (Vc/C1) junction regions (Marfurt and del Toro, 1987;Lu et al, 1993;Strassman and Vos, 1993;Meng and Bereiter, 1996;Gong et al, 2003). The present study measured tear volume and recorded single unit activity to test the hypothesis that the rostral Vi/Vc transition and caudal Vc/C1 junction regions contribute differentially to the control of fluid homeostasis of the ocular surface.…”

“…Despite considerable progress in defining the peripheral neural mechanisms that directly influence lacrimal gland secretion (Walcott, 1998), no studies have determined the location or properties of central neurons that respond to acute changes in moisture status of the ocular surface and project to the SSN, i.e., the afferent limb of this reflex arc, the so-called premotor neurons. The ocular surface is supplied mainly by trigeminal ganglion neurons (Marfurt et al, 1989) that, in turn, send fibers centrally to terminate in the trigeminal brainstem complex (Marfurt, 1981;Panneton and Burton, 1981;Marfurt and del Toro, 1987;Gong et al, 2003). The lower portion of the trigeminal brainstem complex, the spinal trigeminal nucleus (Vsp), consists of three subnuclei-oralis (Vo), interpolaris (Vi), and caudalis (Vc), from rostral to caudal, respectively-and receives somatic sensory information from all structures of the head and oral cavity.…”

Neurobiology in primary headaches

“…Nociceptin immunoreactivity in the superficial dorsal horn is not affected by dorsal root rhizotomy, suggesting that at the spinal cord level nociceptin is produced by central rather by primary afferent neurons [162]. In tracing experiments, it has been demonstrated that the primary trigeminal fibers descend to the superficial layer of the dorsal horn of the cervical spinal cord [130]. About 70% of neuronal cells in trigeminal ganglia are nociceptin immunopositive [103].…”

FK962 Promotes Neurite Elongation and Regeneration of Cultured Rat Trigeminal Ganglion Cells: Possible Involvement of GDNF

“…The sensory neurons innervating the cornea are located in the medial or ophthalmic region of the trigeminal nerve. 24 In cornea, fibers forming the basal epithelial plexus and branch into the epithelium originate from myelinated Ad-and unmyelinated C-fibers. 25 Ad fibers participate in mechanical sensitivity in cornea, which is very important for the blinking reflux leading to tear secretion.…”