Preganglionic and Postganglionic Neurons Responsible for Cerebral Vasodilation Mediated by Nitric Oxide in Anesthetized Dogs

Abstract

The authors performed investigations to functionally determine the route of efferent innervation in vivo responsible for cerebral vasodilation mediated by nitric oxide (NO). In anesthetized beagles, electrical stimulation of the pterygopalatine ganglion vasodilated ipsilateral cerebral arteries such as the middle cerebral and posterior communicating arteries. Intravenous injections of NG-nitro-L-arginine (L-NA) markedly inhibited the response to nerve stimulation, and the effect was reversed by L-arginine. Stimulation of the proximal portion of the greater superficial petrosal nerve, upstream of the pterygopalatine ganglion, also produced cerebral vasodilation, which was abolished by L-NA and restored by L-arginine. Treatment with hexamethonium abolished the response to stimulation of the petrosal nerve but did not affect the response to pterygopalatine ganglion stimulation. Destruction of the pterygopalatine ganglion by cauterization constricted the cerebral arteries. Postganglionic denervation abolished the vasodilation, lacrimation, and nasal secretion induced on the ipsilateral side by stimulation of the pterygopalatine ganglion and petrosal nerve. The vasodilator response was suppressed by L-NA but unaffected by atropine, whereas lacrimation and nasal secretion were abolished solely by atropine. It is concluded that postganglionic neurons from the pterygopalatine ganglion play crucial roles in cerebral vasodilation mediated by NO from the nerve, and preganglionic neurons, possibly from the superior salivatory nucleus through the greater superficial petrosal nerve, innervate the pterygopalatine ganglion. Tonic discharges from the vasomotor center participate significantly in the maintenance of cerebral vasodilation.

Nitrergic nerves derived from the pterygopalatine ganglion innervate arteries irrigating the cerebrum but not the cerebellum and brain stem in monkeys

“…[3][4][5][6] We have reported that electrical stimulation of the unilateral PPG or the greater petrosal nerve (GPN), a preganglionic parasympathetic nerve that synaptically connects to the PPG, dilates the ipsilateral anterior cerebral artery (ACA), and the middle cerebral artery (MCA) in anesthetized monkeys 7 and dogs. 8 We have also found that these dilatations are suppressed by a NOS inhibitor. Furthermore, electrical stimulation of unilateral nerve bundles containing parasympathetic nerves produced an increase of cerebral blood flow in the ipsilateral brain of rats treated with atropine and capsaicin; this increase of cerebral blood flow in the temporo-parietal area was abolished by a NOS inhibitor.…”

Neuronal nitric oxide mediates cerebral vasodilatation during acute hypertension

“…Essentially all of the nitroxidergic innervation of forebrain vessels derives from neurons of the pterygopalatine ganglia , bilateral ganglia that lie near the floor of the orbit and send ganglionic projections into the cranium through the mesial orbital wall (Hara, H. et al, 1993). Stimulation of those ganglia leads to cerebral arterial dilatation (Seylaz, J. et al, 1988;Toda, N. et al, 2000b;Toda, N. et al, 2000a) and some reports, which indicate that interruption of the ganglia or their innervation leads to cerebral vasoconstriction (Toda, N. et al, 2000b;Toda, N. et al, 2000a), suggest that they exert a tonic vasodilator influence. Stimulation of the superior salivatory nucleus (SSN), the site of preganglionic neurons that project to the pterygopalatine ganglia and thus influence CBF, also leads to vasodilatation of cerebral vessels (Agassandian, K. et al, 2002).…”

Localization of immunoreactivities for neuropeptides and neurotransmitter-synthesizing enzymes in the pterygopalatine ganglion of the pig

“…nerve fibers originating from the PPG (Yoshida et al, 1993;Goadsby et al, 1996;Toda et al, 2000) but involvement of other biologically active substances, like vasoactive intestinal polypeptide (VIP) is also possible (Hara et al, 1985). It is possible that pterygopalatine ganglion is somehow involved in the pathogenesis of headache and migraine (Ekbom, 1999;Goadsby, 2000).…”