Abstract

The choroidal blood vessels of the eye provide the main vascular support to the outer retina. These blood vessels are under parasympathetic vasodilatory control via input from the pterygopalatine ganglion (PPG), which in turn receives its preganglionic input from the superior salivatory nucleus (SSN) of the hindbrain. The present study characterized the central neurons projecting to the SSN neurons innervating choroidal PPG neurons, using pathway tracing and immunolabeling. In the initial set of studies, minute injections of the Bartha strain of the retrograde transneuronal tracer pseudorabies virus (PRV) were made into choroid in rats in which the superior cervical ganglia had been excised (to prevent labeling of sympathetic circuitry). Diverse neuronal populations beyond the choroidal part of ipsilateral SSN showed transneuronal labeling, which notably included the parvocellular part of the paraventricular nucleus of the hypothalamus (PVN), the periaqueductal gray, the raphe magnus (RaM), the B3 region of the pons, A5, the nucleus of the solitary tract (NTS), the rostral ventrolateral medulla (RVLM), and the intermediate reticular nucleus of the medulla. The PRV+ neurons were located in the parts of these cell groups that are responsive to systemic blood pressure signals and involved in systemic blood pressure regulation by the sympathetic nervous system. In a second set of studies using PRV labeling, conventional pathway tracing, and immunolabeling, we found that PVN neurons projecting to SSN tended to be oxytocinergic and glutamatergic, RaM neurons projecting to SSN were serotonergic, and NTS neurons projecting to SSN were glutamatergic. Our results suggest that blood pressure and volume signals that drive sympathetic constriction of the systemic vasculature may also drive parasympathetic vasodilation of the choroidal vasculature, and may thereby contribute to choroidal baroregulation during low blood pressure.

Highlights

  • IntroductionThe choroidal blood vessels in the eye and orbital blood vessels supplying the choroid are innervated by parasympathetic, sympathetic and sensory nerve fibers that adaptively regulate choroidal blood flow (Kirby et al, 1978; Guglielmone and Cantino, 1982; Bill, 1984, 1985, 1991; Stone et al, 1987; Fitzgerald et al, 1990a,b, 1996; Cuthbertson et al, 1996, 1997)

  • We found that the pseudorabies virus (PRV)-labeled neurons of raphe magnus nucleus (RaM), raphe pallidus (RaPa), gigantocellular reticular nucleus (GiA) and parapyramidal nucleus (PPy) after intrachoroidal PRV injection tend to be serotonergic (Steinbusch, 1981)

  • Summary By means of transneuronal labeling with PRV from the choroid supplemented by conventional pathway tracing methods and immunolabeling, we implicated numerous central cell groups in the control of choroidal blood flow

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Summary

Introduction

The choroidal blood vessels in the eye and orbital blood vessels supplying the choroid are innervated by parasympathetic, sympathetic and sensory nerve fibers that adaptively regulate choroidal blood flow (Kirby et al, 1978; Guglielmone and Cantino, 1982; Bill, 1984, 1985, 1991; Stone et al, 1987; Fitzgerald et al, 1990a,b, 1996; Cuthbertson et al, 1996, 1997). Numerous studies have shown that the pterygopalatine ganglion (PPG) is the major source of parasympathetic input to the choroid and to periocular vessels in mammals (Ruskell, 1971b; Uddman et al, 1980a; Bill, 1984, 1985, 1991; Stone, 1986; Stone et al, 1987). Using transneuronal retrograde labeling from the choroid with the Bartha strain of pseudorabies virus (PRV), we have found that the neurons controlling choroidal blood flow via the PPG lie within rostromedial SSN and are largely co-incident with the nNOS+ population within SSN (Cuthbertson et al, 2003)

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