Innervation of the Spinal Dura Mater
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J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.6.530 on 1 December 1966. Downloaded from J. Neurol. Neurosurg. Psychiat., 1966, 29, 530 Innervation of the spinal dura mater M. A. EDGAR AND S. NUNDY From the Anatomy School, Cambridge The nerve supply to the spinal dura mater has long eal rami. However, Hilbert (1878) described nerve been a subject of controversy. fibres passing along the ligamenta denticulata from Von Luschka (1850), in his classic monograph, the spinal cord to the internal surface of the dura. described a series of nerves which passed through In addition, Stilwell (1956) and Kimmel (1961) the intervertebral foramina. Each nerve corre- observed dorsal recurrent nerves supplying the sponded with one foramen and traversed it ventral dorsal aspect of the dura mater. to the spinal nerve. He traced this recurrent nerve by Clarification of the nerve supply to the spinal gross dissection and noted that, within the spinal dura mater is important, especially with regard to canal, it supplied the bone and blood vessels. the mechanism of dural sensitivity and pain in Hence it was named the sinu-vertebral nerve (now its clinical application. termed ramus meningeus P.N.A.). Luschka ob- served that branches of each ramus meningeus guest. Protected by copyright. remained entirely outside the spinal dura mater METHODS although some were seen close to its surface. Other The difficulty of distinguishing small nerve filaments contemporary workers, notably Piirkinje (1845), from connective tissue strands is well documented, saw no epidural nerves piercing the dura. and it is hard to follow finer ramifications of nerves Rudinger (1857), however, dissected nerves which even in stained serial sections. Roofe (1940) was not ran along the ventral surface of the dura mater and convinced that any of the fibrous strands within the then entered it. Some fibres were found to be peri- intervertebral foramina were in fact nerves. In this vascular, others to pursue an independent course. study, a combination of methods, involving gross Further studies by other workers, reviewed by dissection and histological examination, has been em- ployed in an attempt to circumvent these difficulties and Testut (1930), confirmed these findings. By 1904 to define the origin, course, and distribution of nerves the presence of intrinsic nerves of the spinal dura to the spinal dura mater. mater was well enough established for Poirier and Charpy to describe them in their textbook. Hove- GROSS DISSECTION Two formalin-fixed cadavers (one lacque (1925), Pederson, Blunck, and Gardner adult and an 8-month foetus) were dissected to demon- (1956), and Stilwell (1956), by various methods, strate the origin and distribution of nervous filaments including gross dissection and examination of running through the inter-vertebral foramina. Strands stained serial sections, identified the presence of of ambiguous nature were examined histologically after nerves which penetrated the spinal dura mater. silver impregnation. a In addition four paravertebral blocks of fresh adult http://jnnp.bmj.com/ However, contrary to century of agreed findings, post-mortem material and three whole specimens of Bridge (1959) stated definitely that the spinal dura spinal dura with epidural tissue were similarly dissected mater, unlike its cranial counterpart (Penfield and after staining in Schiff's reagent (McManus, Saunders, McNaughton, 1940), had no intrinsic nerve supply; Penton, and Cason, 1950; Bridge, 1959). By this technique epidural nerves were seen to end on the dural finer ramifications of nerves, stained blue, were more surface only. readily identified. Kimmel's recent study (1961) of Bodian-stained foetal sections, however, demonstrated intrinsic HISTOLOGY The dura from seven spinal cords was divided nerve fibres. He concluded that these were only to into segments. These were impregnated with silver to on September 29, 2021 by and that con- stain intrinsic nerve fibres using a modified Bielschowsky- be seen with difficulty the different Gross method (Penfield and McNaughton, 1940). Some clusions reached by previous workers were due to dural segments were stained by osmic acid to detect the varying quality of their preparations. myelinated nerve fibres. The origin of nerve fibres supplying the dura Finally an attempt was made to stain nerve endings in (whether they are confined to its surface or are truly spinal dura using intravital methylene blue in two intrinsic) is generally agreed to be from the mening- rabbits (Feindel, Sinclair, and Weddell, 1947). 53C J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.6.530 on 1 December 1966. Downloaded from Innervation ofthe spinal dura mater 531 RESULTS COURSE Each 'ramus meningeus' is composed of up to six separate nerve filaments running through an The origin, course, and relevant distribution of the intervertebral foramen. Usually one filament is meningeal rami were determined. There was con- larger than the others and may be considered as the siderable variation in the findings at different levels main ramus. and at certain levels the nerves were asymmetrical Within the spinal canal the branches of the ramus on the two sides. There were no significant differ- meningeus destined for the dura mater follow three ences between adult and foetal dissections. main courses: 1 The most prominent ramus passes cranially base of the ascending, ORIGIN OF RAMUS MENINGEUS Typically a ramus around the pedicle giving descending, and transverse branches to a plexus of meningeus has a dual origin receiving sympathetic within fibres from the related ramus communicans and nerves situated around and the posterior Here are anastomoses other fibres from the anterior primary ramus (Fig. longitudinal ligament. there 1). The sympathetic contribution is usually multiple with similar nerves of adjacent segments and also across midline. Anterior to the with two or three main filaments coming from the the posterior longi- this is continuous with that ramus communicans. Occasional branches pass tudinal ligament plexus veins. a few from the adjacent sympathetic ganglion or sym- around the basi-vertebral Posteriorly pathetic trunk. branches from this plexus pass directly backwards midline to of the dura The spinal component usually consists of one near the the ventral aspect main filament and comes off the anterior primary mater. to dura ramus. At several different levels in the foetal 2 A small filament passes directly the within it ventral dissection additional nerve roots could be traced mater the spinal canal, reaching just from the dorsal root ganglion. In the adult thoracic to the point at which the spinal nerve root pierces the guest. Protected by copyright. region the posterior primary ramus was observed to dura. give contributions at several levels. 3 A third group of fibres passes longitudinally within the epidural tissue. Mostly these are directed caudally although a small number pass cranially. Branches of these epidural nerves reach the dura. DISTRIBUTION OF NERVES ON THE DURAL SURFACE The ventral surface of the spinal dura mater shows numerous fine nerve trunks running longitudinally on it in parallel. Nerves from adjacent levels overlap. No nerves were observed on the dorsal surface of the dura mater. Nerves as described under (1) above are few and lie along or adjacent to the midline anteriorly. Nerves as described under (2) above are placed postero-laterally near the line of emerging nerve roots. Nerves as described under (3) above, passing from the epidural tissues, lie in an intermediate position. Each nerve, on reaching the surface of the dura divides into an and descend- mater, ascending http://jnnp.bmj.com/ ing branch (Fig. 2). The descending division passes caudally one half to two segments of the spinal cord, the other ascends up to one segment. DISTRIBUTION OF NERVES WITHIN THE DURA MATER ... .. ... .are.~~~~~~~~~~~~-:00 During their course the longitudinally running FIG. 1. Paravertebral gross dissection of an 8-month nerve filaments pierce the dural surface and give foetus at the level of TJO demonstrating a prominent transverse branches, many of which subdivide on September 29, 2021 by filament of the ramus meningeus (R.M.). Two finer All filaments have broken. The dorsal root ganglion (D.R.G.) within the dural substance. finer ramifications and sympathetic trunk (S.T.) are drawn aside by fine are intrinsic. This fact was established by assessing thread to gain a better exposure. The two roots of the focus levels in microscopic examination of stained ramus meningeus are from the ramus communicans (R.C.) dural segments, by microdissection, and by examin- and the anterior primary ramus (A.P.R.). x 12. ation of selected transverse sections of stained dura. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.6.530 on 1 December 1966. Downloaded from 532 M. A. Edgar and S. Nundy FIG. 2. Filament ofa ramus meningeus (R.M.) stained with Schiff's reagentpassing to the ventralsurface ofthe durajust medial to the spinalnerve root in the upper lumbar region. (1) Branch to dura dividing into a short ascending and much longer descendingfilament. (2) Branch to dura (heldaside bypin) reaching it more medially after a short epidural course. Here its ascending branch on the duralsurface is longer. x 8. guest. Protected by copyright. ..s NY..m ..f r a'% http://jnnp.bmj.com/ -..} :: :i: ~~~~~~ ~ ~ ~ ~~~~~~.-?.. ... ..~ .... FIG. 3. Perivascular nervefibres within the dura stainedby the Bielschowsky-Gross method. x 360. on September 29, 2021 by .......~~~~ ~ ..... J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.29.6.530 on 1 December 1966. Downloaded from Innervation ofthe spinal dura mater 533 Most fibres accompany blood vessels (Fig. 3), a uncertain as to the extent of distribution. From few run independently. No intrinsic nerve fibres their point of origin Kimmel describes longer were found in the dorsal part of the dura mater descending nerves in the lumbar region and longer although blood vessels were numerous. ascending nerves in the cervical region. In the Osmic acid staining revealed some myelinated present study a considerable degree of overlap of fibres within the dural substance.