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Localization of Preganglionic Neurons That Innervate Choroidal Neurons of Pterygopalatine Ganglion

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Localization of Preganglionic Neurons That Innervate Choroidal Neurons of Pterygopalatine Ganglion Localization of Preganglionic Neurons That Innervate Choroidal Neurons of Pterygopalatine Ganglion Sherry Cuthbertson,1 Mark S. LeDoux,1,2 Seth Jones,1 Julia Jones,1 Qihong Zhou,2 Suzhen Gong,2 Patrick Ryan,3 and Anton Reiner1 PURPOSE. The pterygopalatine ganglion (PPG) receives pregan- mammals is innervated by parasympathetic, sympathetic, glionic input from the superior salivatory nucleus (SSN) of the and sensory nerve fibers that adaptively regulate ChBF accord- facial motor complex and is the main source of parasympa- ing to retinal needs.4–11 Such adaptive control may be impor- thetic input to the choroid in mammals. The present study was tant for maintaining the health of retinal photoreceptors and undertaken to determine in rats the location and neurotrans- maintaining normal visual functioning.1,12–15 Numerous stud- mitters of SSN neurons innervating those PPG neurons that ies have shown that the pterygopalatine ganglion (PPG) is the target the choroid and to determine the location and neuro- major source of parasympathetic input to the choroid in mam- transmitters of the PPG choroidal neurons themselves. mals.6–9,16–18 The PPG efferent fibers to the choroid contain METHODS. Retrograde labeling from rat choroid using a fluores- the vasodilators VIP and nitric oxide (NO).9,17,19,20 These fi- cent tracer, in combination with immunofluorescence labeling bers also appear to be, at least in part, cholinergic.21–24 for nitric oxide synthase (NOS), vasoactive intestinal polypep- The PPG receives its preganglionic input from the superior tide (VIP), and choline acetyltransferase (ChAT), was used to salivatory nucleus (SSN) of the hindbrain through the greater characterize the location and neurotransmitters of choroidal petrosal branch of the facial nerve.25–29 The SSN itself is lo- PPG neurons. To identify SSN neurons that innervate the cho- cated dorsolateral to the facial motor nucleus. The SSN neu- roidal PPG neurons, the Bartha strain of the retrograde trans- rons, which are somewhat intermingled among and sur- neuronal tracer pseudorabies virus (PRV-Ba) was injected into rounded by noradrenergic neurons of the A5 cell group, are rat choroid, and immunolabeling for NOS or ChAT was used to cholinergic, and, in rabbits and humans, some have been re- characterize their neurochemistry. ported to contain nitric oxide synthase (NOS) as well.30–32 The RESULTS. Fluorescent retrograde labeling showed that PPG neu- SSN also provides preganglionic input through the chorda rons projecting to the choroid contained NOS, VIP, and ChAT tympani nerve to the submandibular ganglion,25,26,28,33 which and were widely distributed in PPG and its preganglionic root, ϩ sends postganglionic fibers to the submandibular and sublin- the greater petrosal nerve. SSN neurons were ChAT , and a gual glands and thereby regulates blood flow and salivary subset of them was found to contain NOS. PRV-Ba transneuro- secretion within these glands. The PPG, in addition to its nal retrograde labeling revealed that choroidal preganglionic innervation of choroidal blood vessels, innervates orbital blood neurons were localized to the rostral medioventral part of the ϩ vessels, the meibomian glands, the lacrimal gland, the hard- ipsilateral SSN. The choroidal SSN neurons were ChAT and ϩ erian gland, blood vessels of the nasal mucosa and palate, and appeared largely to correspond to the NOS neurons of the 34–39 SSN. cerebral blood vessels. Thus, functionally diverse types of preganglionic neurons CONCLUSIONS. These results show that preganglionic neurons in may be present within the SSN. Although the location within rats that are presumed to regulate choroidal blood flow the SSN of the preganglionic neurons controlling the mei- through the PPG reside within the rostral medioventral SSN, bomian glands40 and the lacrimal gland29 has been de- and that NOS is a marker for these SSN neurons. (Invest scribed, the location within the SSN of the preganglionic Ophthalmol Vis Sci. 2003;44:3713–3724) DOI:10.1167/ neurons controlling choroid is unknown. In the present iovs.02-1207 study, we sought to determine the location within the SSN he choroid is the blood supply to the outer retina (includ- in rats of those neurons that innervate the PPG neurons Ting photoreceptors), and disturbances in choroidal blood innervating the choroid (prechoroidal neurons). This study flow (ChBF) can lead to impaired retinal function and dam- also sought to determine whether these SSN neurons con- age to photoreceptors.1–3 The choroid in both birds and tain NOS and can be distinguished by morphology or loca- tion from the nearby A5 adrenergic neurons. To this end, a transneuronal retrograde tracer, the Bartha strain of pseudo- From the Departments of 1Anatomy and Neurobiology, 2Neurol- rabies virus (PRV-Ba), was injected into the choroid of adult ogy, and 3Molecular Sciences, University of Tennessee, Memphis, Ten- rats to identify prechoroidal neurons of SSN, and immuno- nessee. labeling was used to further characterize these neurons. Our Supported by the Benign Essential Blepharospasm Research Foun- results show that the prechoroidal neurons of rat SSN reside dation Inc. (MSL) and National Eye Institute Grants EY12232 (MSL) and within a characteristic location within the SSN and largely EY05298 (AR). ϩ Submitted for publication November 25, 2002; revised April 29, coincide with NOS preganglionic neurons within the SSN. 2003; accepted May 19, 2003. In addition, retrograde labeling from the choroid using flu- Disclosure: S. Cuthbertson, None; M.S. LeDoux, None; S. orescent tracer (FG; Fluorogold; Flurochrome, Englewood, Jones, None; J. Jones, None; Q. Zhou, None; S. Gong, None; P. CO), in combination with immunofluorescence, was used to Ryan, None; A. Reiner, None show that PPG neurons projecting to choroid contain NOS, The publication costs of this article were defrayed in part by page VIP, and ChAT and are widely distributed in the PPG and its charge payment. This article must therefore be marked “advertise- preganglionic root, the greater petrosal nerve. The results of ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. Corresponding author: Anton Reiner, Department of Anatomy and the present studies will aid in elucidating the central sources Neurobiology, University of Tennessee Health Science Center, 855 of input to these SSN neurons and thereby help clarify the Monroe Avenue, Memphis, TN 38163; [email protected]. signals driving parasympathetic control of ChBF. Investigative Ophthalmology & Visual Science, September 2003, Vol. 44, No. 9 Copyright © Association for Research in Vision and Ophthalmology 3713 Downloaded from iovs.arvojournals.org on 10/02/2021 3714 Cuthbertson et al. IOVS, September 2003, Vol. 44, No. 9 MATERIALS AND METHODS The experimental design of the present studies using PRV-Ba, there- fore, incorporated these considerations. Twenty-three rats received Subjects and Approach PRV-Ba injections into the choroid. These rats were anesthetized with an intraperitoneal injection of a ketamine-xylazine mix of 87 and 13 The results reported are based on studies in 40 adult Sprague-Dawley mg/kg, and the right superior–temporal choroid was injected with 1.0 rats (220–550 g; Harlan Inc., Indianapolis, IN). All experiments per- to 2.0 ␮L of PRV-Ba (3 ϫ 108 plaque forming units/mL). The same formed were in compliance with the ARVO Statement for the Use of injection approach was used as for the above described intrachoroidal Animals in Ophthalmic and Vision Research and with National Insti- injections of FG. In 7 of the 23 cases, a strain of PRV-Ba bearing a LacZ tutes of Health and institutional guidelines. To identify SSN neurons construct (which codes for the enzyme ␤-galactosidase) was used. The involved in the control of ChBF, we injected a retrograde transneuro- animals were allowed to survive between 52 and 88 hours after virus nal tracer, the Bartha strain of pseudorabies virus (PRV-Ba), into the injection. All PRV-Ba injections were performed with a syringe (Ham- choroid of rats. Brains from these injected rats, or from normal animals, ilton) with a 30-gauge needle. The rats receiving an intrachoroidal were fixed by transcardial perfusion and processed by immunohisto- injection of PRV-Ba had already received bilateral resections of the chemistry to visualize PRV-Ba, NOS, ChAT, tyrosine hydroxylase (TH), superior cervical ganglia (SCG) to prevent retrograde transneuronal or pairs of the aforementioned (as well as by histochemistry to visual- labeling along sympathetic circuitry.40 Bilateral resections were per- ize reduced nicotinamide adenine dinucleotide phosphate diaphorase formed rather than unilateral because of evidence that the superior [NADPHd]), for the purpose of characterizing the location and neuro- cervical ganglion has a contralateral orbital projection.37,39 The SCG chemistry of neurons in the rat SSN that innervate PPG neurons that lies immediately dorsal to the bifurcation of the common carotid target choroid. To characterize the PPG neurons themselves involved artery. A single ventral midline neck incision allowed access to both in the control of ChBF, a retrograde tracer, FG (FluoroGold, Fluoro- the right and left SCG. Careful blunt and sharp dissection was used to chrome) was injected into the choroid of additional rats. These animals localize the common carotid artery and then the cervical portion of the were fixed by transcardial perfusion. The eyes, the greater petrosal sympathetic trunk. The cervical portion of the sympathetic trunk and nerves, and the PPG from the injected side were sectioned and FG in SCG were freed from the carotid artery and excised in toto. Because the PPG was visualized by fluorescence microscopy. PPG sections with ϩ PRV-Ba does not typically demonstrate transganglionic transport FG neurons were processed by immunofluorescence to visualize through sensory ganglia,33,40,42 there was no reason to transect the NOS, ChAT, or vasoactive intestinal polypeptide (VIP), to characterize ophthalmic nerve to prevent central transport of PRV through trigem- the neurochemistry of PPG neurons innervating the choroid.
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