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Trigeminal Nerve Pathways to the Cerebral Arteries in Monkeys

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Trigeminal Nerve Pathways to the Cerebral Arteries in Monkeys J. Anat. (1987), 155, pp. 23-37 23 With 11 figures Printed in Great Britain Trigeminal nerve pathways to the cerebral arteries in monkeys G. L. RUSKELL AND TERESA SIMONS Department of Optometry and Visual Science, The City University, London EC1 V OHB (Accepted 27 January 1987) INTRODUCTION Nerve fibres are plentiful within the adventitia of the cerebral arteries of the circle of Willis. Most of them are autonomic motor but some are thought to be fibres of primary afferent neurons. Suggestive evidence for a sensory innervation in man was obtained from the responses of patients to stimulation of the cerebral vessels. For example, pain was elicited when the pial or dural arteries were stimulated electrically in patients under local anaesthesia (Fay, 1932; Penfield & McNaughton, 1940; Ray & Wolf, 1940). Sensitivity was greatest when the large pial arteries were stimulated proximally. Provision ofsensory nerve branches to the internal carotid artery probably occurs in the cavernous sinus where the ophthalmic and maxillary branches of the trigeminal nerve pass close to the artery but they have not been demonstrated satis- factorily. Several fine nerves located betweeen the trigeminal ganglion and internal carotid artery were noted by Hovelacque (1927) in dissected human material but he was uncertain whether they were branches of the trigeminal ganglion or sympathetic twigs passing through or to the ganglion. McNaughton (1938) and Fang (1961) assumed that trigeminal fibres joined the nerves of the sympathetic internal carotid plexus within the cavernous sinus and were distributed together to the intracranial branches of the internal carotid artery. They demonstrated the recurrent branches of the trigeminal ganglion to the tentorium in man but they were unsuccessful in their endeavours to identify and follow others passing forward from the ganglion or from the ophthalmic or maxillary nerves in the cavernous sinus. Numerous workers have observed substance P-like immunoreactivity in intracranial pial arteries including those of primates (Chan-Palay, 1977; Uddman, Edvinsson, Owman & Sundler, 1981; Edvinsson, Rosendal-Helgesen & Uddman, 1983) and there is evidence that such reactivity is associated especially with sensory nerves (Hokfelt, Kellerth, Nillson & Pernow, 1975; Jessel & Iversen, 1977; Duckles & Buck, 1982). Some reduction was found in the density and intensity of substance P (SP)-containing fibres in pial arteries of cats (Liu-Chen, Han & Moskowitz, 1983), and the quantity of SP measured by assay was approximately halved (Norregard & Moskowitz, 1985), after unilateral trigeminal ganglionectomy. The same manoeuvre in gerbils and guinea-pigs reduced SP fibres in the carotid system of arteries but had limited or no effect on their number in the walls of vertebral and basilar arteries (Yamamoto et al. 1983; Matsuyama et al. 1984) indicating that the trigeminal ganglion shares respon- sibility for provision of sensory fibres to the cerebral arteries; there is good evidence that the superior vagal ganglion is a source (Keller, Beduk & Saunders, 1985). These recent studies, employing mainly chemical markers, amply confirm earlier evidence for a sensory innervation of the cerebral vessels without providing details of nerve access to the vessels. We have traced three nerve pathways from the trigeminal 24 G. L. RUSKELL AND TERESA SIMONS ganglion to the cerebral arteries in cynomolgus monkeys and they are the subject of this report. MATERIALS AND METHODS Nine young adult cynomolgus (Macaca fascicularis) monkeys of both sexes were sedated parenterally with 2-3 mg/kg ketamine and anaesthetised with 15-25 mg/kg Sagatal (sodium pentobarbitone) given via the saphenous vein or intraperitoneally. The calvaria was removed and the left lateral lobe of the brain elevated to expose the trigeminal nerve. To minimise the risk ofdamage to adjacent nerves and the cavernous sinus, the ophthalmic nerve sheath was slit parallel to the nerve axis close to the trigeminal ganglion. The nerve was freed from sheath attachments, separated from adjacent structures with a hook, and divided and reflected in six animals. In addition, a short length of the maxillary nerve was removed close to its entry into the foramen rotundum in three of the animals. In three other monkeys only the maxillary nerve lesion was made. The operations were designed to induce Wallerian degeneration so that fibres from the divided nerves to the internal carotid artery could be traced. Maxillary neurectomy was included because earlier work on monkeys had shown that an extracranial branch of the maxillary nerve, the orbitociliary nerve, re-enters the cranium from the pterygo- palatine fossa and in part joins branches from the internal carotid plexus (Ruskell, 1974). Consequently, the orbitociliary nerve is a potential source of cerebral artery sensory nerve fibres. From three to seven days after operation animals were sedated, anaesthetised and given an injection of the anticoagulant heparin sodium (1500 units). The external jugular veins and the inferior vena cava were cut and a 2% glutaraldehyde, 3 % paraformaldehyde cacodylate-buffered solution was perfused through the heart. The heads were stored in the fixative at approximately 4 °C and dissected while immersed in a buffered sucrose solution using a dissection microscope. The cavernous sinus with its contents was removed in one piece from both sides. The internal carotid artery was cut posterior to the trigeminal ganglion and again a few millimetres beyond the position where it emerges dorsally from the cavqrnous sinus and all the soft tissue between these positions was freed from the cranial floor. The dissected tissues included the trochlear, ophthalmic and abducent nerves with a short length of the maxillary nerve, and the piece was divided vertically into anterior and posterior halves. Only the part ofthe trigeminal ganglion opposite the ophthalmic and maxillary nerves was retained; the hypophysis and the oculomotor nerve, where it lay external to the cavernous sinus, were discarded. The contents of the upper part of the pterygopalatine fossa, including the orbitociliary nerve and the rami orbitales, were left attached to the sinus tissues. Finally, in some preparations an additional length of the internal carotid artery was removed from the carotid canal together with the thick sleeve of connective tissue (including periosteum) enclosing the artery. Care had to be taken to ensure that the tissues were free of bone fragments. The pia-arachnoid canopy of the pons from the level of the superficial origins of the oculomotor nerves to the medulla was separated from the underlying nervous tissue. Incisions were made through the canopy just lateral to the line of cranial nerve origins on each side and the canopy was then grasped with forceps at its cut medullary end and slowly peeled free. The caudal cerebral vessels and the stumps of the abducent nerves were naturally retained within the thin sheet of tissue. Tissues of the cavernous sinus were postfixed in 1 % unbuffered osmium tetroxide, Trigeminal nerve pathways to cerebral arteries 25 dehydrated, embedded in Araldite and transversely sectioned using glass knives. Sections were cut 1 ,sm thick at intervals of 120-240 um in areas of least interest and at 60,um intervals or every fifth section elsewhere and stained with 1 % toluidine blue in an equal volume of 2-5 % sodium carbonate. Special attention was given to tissue areas that included the site of the lesion. The face of each large block of tissue was trimmed at appropriate points to present a small area for electron microscopical examination. Sample sections of the separate lengths of internal carotid artery were treated for light and electron microscopy. Sections for electron microscopy were mounted on unfilmed copper grids, immersed in a saturated solution of uranyl acetate in 30-70% ethanol for about 20 minutes, washed and immersed in 0-4 % lead citrate in 01 N sodium hydroxide for about 10 minutes. The pia-arachnoid canopy was similarly treated and embedded whole in an Araldite bath. Pieces pertinent to the present study were identified, cut out and prepared in the same manner as the sinus tissues. Histological evaluation of the ophthalmic lesions revealed some damage to the trochlear nerve in two monkeys but otherwise lesions were confined to the ophthalmic nerve. Retention of full integreity of autonomic filaments of the carotid plexus, which was crucial for the study, was verified in each animal. RESULTS Figure 1 includes most of the structures examined in the present study together with some neighbouring structures. The trigeminal ganglion was included in the first sections of each series and in all preparations ganglion cells infiltrated the ophthalmic nerve in large numbers. They made up the bulk of the nerve in the first millimetre reducing gradually to a few, 2 5 mm from the ganglion on average. Further forward, isolated or small groups of cell bodies were present. Animals displayed little variation in the length of nerve infiltrated. As a consequence large numbers of intact trigeminal cells lay distal to the damaged area following ophthalmic neurotomy. In contrast, the maxillary nerve was entirely free of cell bodies. Fine branches from the ophthalmic and maxillary nerves joined the plexus of autonomic nerves in the cavernous sinus before passing to the walls ofcerebral arteries or to other structures (Fig. 2). Autonomic nerves were derived from two sources, one from the sympathetic superior cervical ganglion
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