Yasuaki Kuwayama

A quantitative correlation of substance P-, calcitonin gene-related peptide- and cholecystokinin-like immunoreactivity with retrogradely labeled trigeminal ganglion cells innervating the eye

To evaluate the intraganglionic organization of ocular sensory neurons in the guinea pig, we studied the retrograde axonal transport from the eye to the trigeminal ganglion of cholera toxin B subunit and then applied immunohistochemistry for substance P, calcitonin gene-related peptide and cholecystokinin. Retrogradely labeled cells were observed only in the anteromedial portion of the ipsilateral ganglion. We observed no somatotopical organization to trigeminal neurons containing any of these three peptides, either for cells projecting to the eye or for the ganglion as a whole. The relative proportion of neurons immunoreactive for each of these three peptides was similar among the population of neurons retrogradely labeled with cholera toxin B and among the population of neurons without direct projections to the eye.

Autonomic neurons supplying the rat eye and the intraorbital distribution of vasoactive intestinal polypeptide (VIP)-like immunoreactivity

We traced the origin and path of autonomic nerves to the rat eye using, as an aid to dissection, a modified thiocholine method for the histochemical demonstration of cholinesterase. When applied to whole nerves and ganglia supplying the rat eye, this procedure is not specific for cholinergic neurons; instead it stains both sympathetic and parasympathetic nerves, many of which are otherwise too fine to identify in dissection. We found that nerves from the superior cervical and pterygopalatine ganglia form a plexus at the orbital apex corresponding to the retro-orbital plexus found in rabbit, monkey and man. In the rat, nerves from the retro-orbital plexus travel peripherally to the superior surface of the optic-nerve sheath. Here, they fuse with long ciliary nerves and the post-ganglionic nerves from the ciliary ganglion to form another dense nerve-fiber plexus that ultimately supplies the eye. Importantly, the plexus on the optic nerve contains many isolated or aggregated ganglion cells. These are comparable in number to those in the ciliary ganglion itself and are assumed to be accessory ciliary neurons. Using immunohistochemistry, we also sought evidence for vasoactive intestinal polypeptide in these ganglia and nerves. As previously known, many pterygopalatine ganglion cells are immunoreactive for this peptide. Vasoactive intestinal polypeptide (VIP)-like immunoreactive nerve fibers are present in nerves from the retro-orbital plexus to the optic-nerve sheath plexus, in most nerves of the latter plexus, and in most nerves entering the eye. Furthermore, a small proportion of nerve cells in the main and accessory ciliary ganglia also are immunoreactive for VIP. We conclude that in addition to the pterygopalatine ganglion, the ciliary ganglion and its accessory ganglia are sources of VIP-like immunoreactive nerves in the rat eye.

Pterygopalatine ganglion cells contain neuropeptide Y

By immunohistochemistry, neuropeptide Y (NPY) localizes to neurons in the rat pterygopalatine ganglion. These cells also are intensely or moderately reactive with acetylcholinesterase histochemistry. In contrast, both tyrosine hydroxylase immunohistochemistry and glyoxylic acid-induced fluorescence for catecholamines stain smaller clustered cells, similar in appearance to small intensely fluorescent (SIF) cells and clearly distinct from the NPY-immunoreactive cells. By reverse phase high-performance liquid chromatography, the NPY-immunoreactive material in the rat pterygopalatine ganglion migrates as a single peak characteristic of the peptide. We conclude that NPY-containing cholinergic cells are present in this classical parasympathetic ganglion. NPY-like immunoreactive neurons similarly occur in the pterygopalatine ganglion of the guinea pig.

Neuropeptide immunoreactivity of pericellular baskets in the guinea pig trigeminal ganglion

Using immunohistochemical techniques, calcitonin gene-related peptide, substance P and cholecystokinin localize to baskets of fine nerve fibers that completely surround occasional neurons in the guinea pig trigeminal ganglion. These observations, viewed with prior neuroanatomical studies indicating an intrinsic origin for these structures, raise again the possibility of intraganglionic communication within the trigeminal ganglion.

Peptide immunoreactivity of the ciliary ganglion and its accessory cells in the rat

By means of immunohistochemistry, calcitonin gene-related peptide, Leu-enkephalin and neuropeptide Y localize to rat ciliary and accessory ganglion cells. The proportion of ciliary and accessory neurons immunoreactive to each peptide is provided and compared to previous data for vasoactive intestinal peptide. These findings indicate considerable neurochemical complexity for a parasympathetic ganglion with a small cell population.

Cholecystokinin-like immunoreactivity occurs in ocular sensory neurons and partially co-localized with substance P

Based on immunohistochemical analysis of the trigeminal, superior cervical, ciliary and sphenopalatine ganglia and of the eye after sensory denervation and sympathectomy, cholecystokinin (CCK)-like immunoreactive nerves in the guinea pig eye derive from the trigeminal ganglion. Substance P (SP) also occurs in some ocular sensory neurons, suggesting the possible co-localization in this system of CCK- and SP-immunoreactivities. A double-labeling immunofluorescence technique stained 3 types of trigeminal cells and ocular nerve fibers: some immunoreactive for both peptides, some immunoreactive only for CCK and some immunoreactive only for SP.

Neuropeptides and the ocular innervation

The eye is designed to provide the retina with protection and nutrition as well as a focussed image. The present review concentrates on regulatory peptides in nerves to the supportive structures of the eye. The retina itself will be discussed but briefly. To understand the innervation of the eye requires an overview of ocular physiology and anatomy.