Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in pigeons

Abstract

Orbital and choroidal blood vessels in mammals are known to receive a parasympathetic innervation from the pterygopalatine ganglion, which appears to utilize vasoactive intestinal polypeptide (VIP) and nitric oxide (NO) to increase choroidal blood flow. The present studies were undertaken to elucidate the anatomical and neurotransmitter organization of the pterygopalatine ganglion input to orbital and choroidal blood vessels in pigeons. Single- or double-label immunohistochemistry were employed on paraformaldehyde-fixed cryostat sections of the pigeon eye and surrounding orbital tissue to localize 1) VIP+ neurons and fibers; 2) choline acetyltransferase (CHAT)-containing cholinergic neurons and fibers; 3) axons containing the 3A10 neurofilament-associated antigen; and 4) neuronal NO synthase (nNOS)-containing neurons and fibers. NOS+ neurons and fibers were also identified by NADPH-diaphorase histochemistry in sections and whole-mount specimens. The pterygopalatine ganglion was found to consist of an interconnected series of three to four main microganglia of about 50-200 neurons each and numerous lesser microganglia. The major microganglia of the pterygopalatine network in pigeon lie along the superior aspect of the Harderian gland, with many additional fibers and microganglia of the network encircling the gland. Neurons of all microganglia were extremely rich in VIP, nNOS, and NADPH-diaphorase and moderate in CHAT. The majority of the pterygopalatine ganglion neurons were observed to co-contain VIP and nNOS. Axons labeled for VIP, nNOS, NADPH-diaphorase, or the 3A10 antigen could be traced from the pterygopalatine ganglion network to perivascular fiber plexi on orbital blood vessels. These orbital vessels, many of which enter the choroid posteriorly and nasally, appear to be a conduit by which pterygopalatine postganglionic fibers reach the choroid. The pterygopalatine postganglionic fibers were also seen to innervate the Harderian gland and contribute branches to the nearby ophthalmic nerve. Within the choroid, VIP+ fibers were widely scattered and sparse but were most abundant in nasal choroid. A few VIP+ and NADPH- diaphorase+ neurons were also observed in the choroid. These results suggest that pterygopalatine ganglion neurons of birds use VIP and NO to exert vasodilatory control over blood flow to and within the avian choroid.

Intrinsic choroidal neurons in the duck eye receive sympathetic input: anatomical evidence for adrenergic modulation of nitrergic functions in the choroid

“…Choroidal blood vessels and NVSMC also receive a prominent innervation by cholinergic neurons in the ciliary ganglion (Meriney and Pilar 1987;De Stefano et al 1993;De Stefano and Mugnaini 1997a) and by nitrergic/VIP-ergic neurons in the pterygopalatine ganglion (Cuthbertson et al 1997). It remains to be established whether ICN are also intercalated in a parasympathetic pathway to the choroid, similar to their relationship to the sympathetic pathway.…”

“…However, they have only recently become amenable to closer scrutiny by virtue of their nitric oxide synthase (nNOS)/ NADPH-diaphorase (NADPH-d) reactivity (Bergua et al 1993;Flügel et al 1994;Cuthbertson et al 1997). Immunocytochemical and histochemical techniques have made apparent their abundance in humans and higher primates and their scarcity or even absence in lower mammals (Flügel et al 1994).…”

“…ICN share an nNOS/VIP phenotype with neurons in the pterygopalatine ganglion (Walcott et al 1989;Yamamoto et al 1993;Alm et al 1995;Cuthbertson et al 1997). Thus, it seems reasonable to assume that ICN represent peripherally displaced parasympathetic postganglionic neurons.…”

Distribution and organization of the nerve fiber and ganglion cells of the human choroid

“…Previous reports have shown that they protect the fovea against extreme temperature changes and suggest that they influence the position of the fovea by altering the thickness of the choroid. (Parver et al 1980(Parver et al , 1983Bill 1985;Bill and Nilsson 1985;Parver 1991;Zagvazdin et al 1996;Cuthbertson et al 1997;Poukens et al 1998;Shih et al 1999).…”

The Autonomic Facial Nerve Pathway in Birds: A Tracing Study in Chickens

“…7,12 Because of the concealed position of the pterygopalatine ganglion, however, far less is known both functionally and structurally of the facial nerve pathway than of the oculomotor pathway. This applies especially to birds, a major animal model in experimental ophthalmology, in which the pterygopalatine ganglion consists of a chain of interconnected microganglia [13][14][15][16] that reside deep in the nasal side of the orbit, between the sclera and the Harderian gland, an accessory lacrimal gland found in many species. 17,18 Hence, experimental manipulation of this pathway appears to require a quite invasive technique.…”