NERVE F I B E R COMPONENTS O F CO&IMUNICATING RAM1 AND SYMPATHETIC ROOTS I N MAN' ALBERT KUNTZ, HENRY HARLAND HOFFMAN AND MERLE WILLIAM JACOBS a Department of Anatomy, St. Lozeis University School o f Medicine St. Louis. Missouri T W O *FIGURES The sympathetic preganglionic nerve fibers emerge from the spinal cord in the ventral roots of the thoracic and the rostra1 two or three lumbar spinal nerves. They join the sympathetic trunk through the communicating rami, which also convey afferent nerve fibers. The communicating (white) rami, consequently, are made up of preganglionic and visceral afferent fibers. The sympathetic postganglionic fibers join the spinal nerves through the sympathetic roots (gray communicating rami) which are made up chiefly of postganglionic fibers, but also convey some afferent ones. Most of the postganglionic fibers are unmyelinated. Most of the afferent fibers in the sympathetic roots are myelinated. Following degeneration of the afferent and any preganglionic fibers that may traverse a sympathetic root, in experimental animals (cats), some myelinated fibers in it remain intact (Ranson and Billingsley, '18 ; Kuntz and Farnsworth, '31). These appear to be myelinated postganglionic fibers. The abundance and the variability in the numbers of myelinated fibers in sympathetic roots in man (Pick and Sheehan, '46) favors the assumption that not all of them fall into the categories of afferent and preganglionic fibers. Supported by USPHS Grant B-666. 1955. * USPHS Fellow, Summer 29 30 KUNTZ, HOFFMAN A N D J A C O B S MATERIAL AND METHODS The relationships of communicating rami and sympathetic roots were studied in a series of dissections of the sympathetic trunks and their connections with the spinal nerves in man. Dorsal and ventral nerve roots, communicating rami and sympathetic roots were sectioned transversely and stained with Sudan black. Communicating rami and sympathetic roots obtained at autopsy were stained with osmic acid and sectioned transversely. Caliber measurements and counts of myelinated fibers were carried out in both Sudan black arid osmic acid preparations. The occurrence and the distribution of accessory ganglia located in relation to communicating rami and sympathetic roots was studied in serial longitudinal sections of these structures arid adjacent portions of the spinal nerves stained with hematoxylin and eosin. I n order to isolate in sympathetic roots myelinated fibers that are neither afferent nor preganglionic, cats and dogs were subjected to operative procedures in which afferent and preganglionic fibers were severed. After allowing ample time for degeneration of the interrupted fibers, communicating rami and sympathetic roots were stained with osmic acid and sectioned transversely. Caliber measurements and counts of the myelinated fibers in these sections were carried out. ANATOMICAL DATA Veatrnl roots. Throughout the sympathetic outflow every ventral spinal nerve root conveys preganglionic fibers that reach the sympathetic trunk through a communicating ramus. I n general, preganglionic fibers fall within the diameter range of less than 1 to 3.5 H. In the ventral nerve roots that convey preganglionic fibers most of the fibers within this diameter range are arranged in relatively dense aggregates that are surrounded by larger, less closely aggregated fibers (fig. 1A). These aggregates of small fibers occur throughout the entire transverse section of the ventral root (fig. IB). Coinparable fiber aggregates do not occur in the ventral roots of the spinal SYMPATHETIC RAM1 AND ROOTS 31 nerves rostral to the 8th cervical. Actual counts of the total number of aggregated fibers in a ventral nerve root and the fibers in the diameter range of preganglionic fibers in the communicating ramus arising from the same nerve indicate a relatively close correspondence. It appears highly probable, therefore, that the preganglionic fibers traverse the ventral nerve roots chiefly in these aggregates of small fibers. Communicating rami. The communicating rami (white) are made up predominantly of preganglionic fibers all of which appear to be myelinated (fig. 1C). They also include afferent fibers many of which are myelinated and larger than the preganglionic fibers. Most communicating rami are separate from the sympathetic roots (gray communicating rami), but in some instances preganglionic and postganglionic fibers are conveyed in the same ramus. Usually a communicating ramus joins a single sympathetic trunk ganglion, but in some instances it divides into two or more branches that join the same sympathetic trunk ganglion or adjacent ones. The numbers of preganglionic and afferent fibers in different communicating rami vary within a relatively wide range. I n the presence of accessory ganglia in the ventral primary ramus of a spinal nerve or adjacent to it, some preganglionic fibers make synaptic connections in these ganglia through either collateral or terminal branches. The total number of preganglionic fibers in a communicating ramus, therefore, need not equal the total number in the corresponding ventral nerve root. Our observations relative t o accessory ganglia located in relation to ventral primary and communicating rami support the assumption that they occur most frequently in the rostral two or three thoracic segments and from the 11th thoracic to the 3rd lumbar segment. Except in segments in which accessory ganglia occur in relation to the ventral primary or the communicating ramus, all the preganglionic fibers that emerge in a given ventral nerve root throughout the sympathetic outflow probably join the sympathetic trunk. Sympathetic roots. The sympathetic roots are made up predominantly of postganglionic fibers, most of which are Fig. 1 Photoniicrograplis from sections of ventral nerve root, a communicating ramus and sympathetic roots in man stained with Sudan black. A. Area of a section of the ventral root of the 4th thoracic nerve showing a n aggregate of small myelinated fibers surrounded b y larger myelinated fibers. B. Lower magnification of the same section showing the distribution of aggregates of small myelinated fibers. C. Section of the communicating ramus of the 9th thoracic nerve showing predominance of myelinated fibers. D. Section of the sympathetic root of a 5 t h thoracic nerve showing relatively few mgelinated fibers. E. Section of the sympathetic root of a n 8th thoracic nerve showing greater abundance of myelinated fibers. F. Section of the sympathetic root of a 9th thoracic nerve showing still greater abundance of myelinated fibers. 33 SYMPATHETIC RAM1 AND ROOTS 33 unmyelinated, but they include variable numbers of myelinated fibers interspersed among the unmyelinated ones (fig. lD, E, F). The sympathetic root in a given segment may consist of a single ramus or of two or more lesser rami. Sympathetic roots can be classified, as has been done by Pick and Sheehan ('46), according to the abundance of myelinated fibers in them. Most of the myelinated fibers fall within the diameter range of preganglionic fibers, but many are too large to be included in this category. Most of the larger fibers fall within the diameter range of 3.5 to 15 p. Myelinated fibers that exceed 3 . 5 ~in diameter are more abundant in the sympathetic roots of the nerves that contribute to the brachial and lumbosacral plexus than in those of the intervening thoracic nerves. Those of some of the thoracic nerves include relatively few larger fibers (fig. lE, F). Accessory ganglia are known to occur frequently in relation to sympathetic roots as well as in relation to ventral primary and communicating rami. Our data relative to accessory sympathetic ganglia in man, like those of other investigators (Rossi, '31 ; Gruss, '32 ; Skoog, '47 ; Wrete, '35, '51), support the assumption that they occur more frequently in the cervical and rostral two or three thoracic segments and in the caudal thoracic and lumbar segments than in the intervening ones. Accessory ganglia in the cervical region usually are located in relation to sympathetic roots. Many of those in the lumbar and sacral segments likewise are related to sympathetic roots. Others throughout the thoracic, lumbar and sacral segments are located in relation to ventral primary and communicating rami. Histological examination of serial longitudinal sections of sympathetic roots in 5 human cadavers has revealed accessory ganglion cells frequently in those of the nerves that make up the brachial and lumbosacral plexuses, less frequently in those of the more rostral cervical nerves and occasionally in those of thoracic nerves. Ganglion cells in sympathetic roots or adjacent to them occur in small and larger aggregates. Most of them are incorporated in compact ganglia. Actual counts 34 KUNTZ, KOFFMAN AND JACOBS of the ganglion cells in a limited number of accessory ganglia located in sympathetic roots or in relation t o them indicate a range of 10 to over 2000. Ganglia that comprise 100 to 250 ganglion cells were observed frequently. Many of the sympathetic roots examined revealed no ganglion cells. Most preganglionic fibers that make synaptic connections with accessory ganglion cells that are located in relation to sympathetic roots undoubtedly traverse these roots to the points at which the ganglion cells are located. I n some sympathetic roots such synaptic relationships are sufficiently numerous to account for large numbers of preganglionic fibers. I n sympathetic roots that include accessory ganglia, many of the myelinated fibers that do not exceed 3.5 p in diameter undoubtedly are preganglionic. Myelinated fibers within the preganglionic caliber range, however, occur in many sympathetic roots in the absence of accessory ganglion cells related to them. I n order to obtain data relative to the anatomical relationships of all the myelinated fibers, osmic acid preparations of sympathetic roots of cats and dogs were obtained following degeneration of the afferent and the preganglionic fibers in the nerves in question. The experimental animals were subjected to surgical procedures in which a series of spinal nerve roots was sectioned unilaterally distal to the spinal ganglia but proximal t o the sympathetic roots and communicating rami or the sympathetic trunk was divided caudal to the sympathetic preganglionic outflow. These procedures insure degeneration of both afferent and preganglionic fibers in t,he sympathetic roots affected. Osmic acid preparations of sympathetic roots in which the afferent and the preganglionic fibers had undergone degeneration, obtained from cats, exhibit many intact myelinated fibers. As compared with sections of the contralateral normal sympathetic roots, the myelinated fibers are reduced in numbers and most of those that remain intact do not exceed 2 p in diameter (fig. 2A, B). Counts of the intact myelinated fibers in sections of the sympathetic roots of the 6th and 7th lumbar and the 1st sacral nerves S Y M P A T H E T I C RAM1 A N D ROOTS 35 of a cat following degeneration of the fibers interrupted by section of the left sympathetic trunk just rostra1 to the 6th lumbar segment and between the 6th and 7th lumbar nerves a r e recorded in table 1. Fig. 2 A. Section of the sympathetic root of the right 7th lumbar nerve of a cat, stained with osmic acid, showing normal frequency of myelinated fibers. B. Section of the sympathetic root of the left 7th lumbar nerve of the same cat after degeneration of the preganglionic and the afferent fibers, stained with osmic acid, showing myelinated fibers t h a t remain intact. C . Section showing a slender ramus derived from the sympathetic trunk in man adjacent t o intercostal blood vessels. The ramus includes accessory ganglion cells. 36 IIUNTZ, HOFFMAN AND JACOBS Since the left sympathetic trunk was divided caudal to the sympathetic preganglionic outflow, both the afferent and the preganglionic fibers in the left sympathetic roots in question were interrupted and underwent degeneration. The myelinated fibers that remained intact in these roots, consequently, must be postganglionic. The demonstration by Ranson and Billingsley ( '18) of myelinated postganglionic fibers in the cat, therefore, is confirmed. Osmic acid preparations of normal sympathetic roots of dogs in general exhibit fewer myelinated fibers than those of cats. Following degeneration of both the afferent and the preganglionic fibers, most sympathetic roots of the dog exhibit no intact myelinated fibers. On the basis of these obswTABLE I SYMPATHETIC ROOT 6th lumbar 7th lumbar 1st sacral NUMBER O F MYELIBATED FIBERS Rieht Left 234 305 118 145 159 63 vations it may be assumed that myelinated postganglionic fibers occur only rarely, if at all, in the sympathetic roots in the dog. Sections of human sympathetic roots exhibit myelinated fibers in greater abundance than sections of those of the dog. With respect to the abundance of myelinated fibers the sympathetic roots of man resemble more closely those of the cat than those of the dog. A relatively high percentage of the myelinated fibers in human sympathetic roots falls within the diameter range of those that remain intact in the sympathetic roots of the cat after degeneration of the afferent and the preganglionic fibers. Counts of the myelinated fibers in three size categories are recorded in table 2. These counts cannot be regarded as highly accurate, but they reflect the variations in the total number of myelinated fibers and in the numbers of those in each of the several 37 SYMPATEETIC RAM1 A N D ROOTS size categories in different sympathetic roots. I n most of the sympathetic roots 50% or more of the myelinated fibers do not exceed 2 . 5 ~in diameter. They fall within the diameter range of most of the myelinated fibers in sympathetic roots of the cat that remain intact following degeneration of the preganglionic and the afferent fibers. Total numbers of myelinated fibers in the sympathetic roots vary w-ith the total numbers of both myelinated and unmyelinated ones. The total number of fibers in a given sympathetic root is correlated with the extent of the vascular bed and other autonomic effector organs that are innervated through that root. Segnzemtal sympathetic rami. I n addition to the sympathetic roots and the splanchnic nerves the sympathetic trunk gives off more slender rami that neither join the spinal nerves nor extend t o the thoracic or abdominal viscera. In the cervical and rostra1 thoracic segments some of these rami join the plexuses on the carotid and the vertebral arteries. In the thoracic and lumbar segments such rami in general extend along the segmental blood vessels and contribute to their innervation. Some segments include more than a single ramus of this kind. Frequently, two or more slender rami may be traced from a segment of the sympathetic trunk along the segmental vessels. DIAMETER OF FIBERS __-C6 C7 Less than 2.5 microns 45 1443 2.5 t o 3.5 iiiierons 93 Over 3.5 inicroiis 632 108 145T R W N E N T A L DESIGNATION C8 TI T3 T4 T5 T6 T7 TK TY L1 L2 L3 L4 L5 735 1747 62 135 185 113 424 435 403 1104 511 579 1932 630 265 697 68 71 57 33 128 130 83 293 244 235 574 220 679 1132 83 93 69 57 161 136 340 258 167 338 746 164 246 3532 1679 3576 213 299 311 203 713 701 626 1655 922 1152 3352 1014 38 KUNTZ, HOFFMAN A N D JACOBS The fiber composition of these slender rami is comparable to that of the sympathetic roots. Some of them also include ganglion cells in small numbers (fig. 2C). Most of the unmyelinated fibers undoubtedly are postganglionic and arise in sympathetic trunk ganglia. The larger myelinated fibers and some of the smaller ones probably are afferent. Rami in which ganglion cells are located must also include some preganglionic fibers. DISCUSSION The assumption that the white communicatiiig rami are made up predominantly of myelinated fibers is supported by the data obtained from both animal and human preparations, but they also include unmyelinated fibers. The sympathetic roots (gray communicating rami) are separate from communicating rami in most instances, but frequently at least a portion of the sympathetic root fibers and fibers of the communicating ramus traverse a common nerve bundle. I n man, as observed by Pick and Sheehan ( '46), the sympathetic roots vary widely with respect to the abundance of myelinated fibers that traverse them, but all include both small and larger ones. The finding of Ranson and Billingsley ( '18) that the sympathetic roots in the cat include myelinated postganglionic fibers is confirmed. I n view of the occurrence in the sympathetic roots in man of large numbers of myelinated fibers in the diameter range of those that remain intact in the sympathetic roots of the cat after degeneration of the preganglionic and the afferent fibers it appears probable that many postganglionic fibers in the sympathetic roots in man are myelinated. The assumption that the small myelinated fibers in human sympathetic roots are exclusively postganglionic is unwarranted, however, since some afferent fibers in these roots probably are smaller than some efferent ones. The larger myelinated fibers in the sympathetic roots in man undoubtedly are afferent. The afferent component probably also includes some small myelinated and some unmyelinated fibers. The occurrence of afferent fibers in sympathetic roots SYMPATHETIC RAM1 AND ROOTS 39 in animals has been amply demonstrated both anatomically (Kuntz and Farnsworth, '31) and physiologically (Threadgill and Solnitzky, '49). The assumption that some afferent conduction from the extremities is mediated through dorsal root fibers that traverse sympathetic roots and the sympathetic trunk is also supported by clinical experimental data (Walker and Nulsen, '48; Echlin, '49; Sweet and White, '53). Afferent conduction from trunk dermatomes through the sympathetic trunk has also been demonstrated (Van Harreveld and Smith, '53). On the basis of the available experimental data and the anatomical data obtained in the present study it appears highly probable that all sympathetic roots in man are traversed by afferent nerve fibers. On the basis of the fiber counts recorded in table 2 it is apparent that the sympathetic roots of the nerves that make up the brachial and the lumbosacral plexuses are traversed by myelinated fibers over 2.5 I-( in diameter in much larger numbers than those of the thoracic nerves caudal to the second. On the assumption that these fibers are predominantly afferent it is apparent that afferent fibers are distributed through sympathetic roots in greater abundance to the extremities than to trunk segments. The afferent fibers that traverse sympathetic roots probably are distributed chiefly to blood vessels. The total number of afferent fibers that traverse a given sympathetic root, like the total number of its efferent fibers, appears to be correlated with the extent of the vascular bed that is innervated through that root. It need not be assumed, however, that all the fibers concerned with the afferent innervation of the peripheral blood vessels and other peripheral autonomic effector organs traverse sympathetic roots. The frequent occurrence of accessory ganglion cells in sympathetic roots or in close proximity to them affords an explanation of the occurrence of preganglionic fibers in some sympathetic roots. The ganglion cells in question probably represent cells that have been displaced from the primordia of sympathetic trunk ganglia, and the preganglionic fibers to 40 KUNTZ, HOFFMAN AND JACOBS which they are synaptically related extend beyond the sympathetic trunk in the sympathetic roots. Only a small percentage of the myelinated fibers in synpathetic roots can be accounted for on this basis. Most of the preganglionic fibers that make synaptic connections with ganglion cells that are located in proximity to segmental blood vessels probably do not traverse sympathetic roots, but reach the cells in question through segmental rami from the sympathetic trunk. On the basis of all the available data, the sympathetic roots in man, like those in the cat, appear to be made up predominantly of postganglionic fibers most of which are unmyelinated. They are traversed by dorsal root fibers most of which probably are distributed to peripheral blood vessels. Some are also traversed by limited numbers of preganglionic fibers. SUMMARY The sympathetic preganglionic nerve fibers traverse the ventral nerve roots in dense aggregates of small myelinated fibers. The communicating rami are made up predominantly of myelinated fibers. Those that are larger than the preganglionic fibers are afferent. The afferent component also includes fibers that fall within the preganglionic caliber range. The sympathetic roots include myelinated fibers interspersed among the unmyelinated ones. The myelinated fibers that exceed 3.5 p in diameter and some smaller ones are afferent. All sympathetic roots in man probably are traversed by afferent fibers most of which are distributed to peripheral blood vessels. Sympathetic roots with which accessory ganglion cells are associated also include preganglionic fibers. The total number of afferent fibers in a given sympathetic root appears to be correlated with the extent of the vascular bed that is innervated through that root. In the cat many small myelinated fibers remain intact in sympathetic roots following degeneration of both the afferent and the preganglionic fibers. They are regarded as myelinated SYMPATHETIC RAM1 AND ROOTS 41 postganglionic fibers. A relatively high percentage of the myelinated fibers in human sympathetic roots falls within the caliber range of those that remain intact in sympathetic roots of the cat following degeneration of the afferent and the preganglionic fibers. It appears highly probable, therefore, that the sympathetic roots in man also include myelinated postganglionic fibers. LITERATURE CITED ECHLIN,F. 1949 Pain responses on stimulation of the lumbar sympathetic chain under local anesthesia-A case report. J. Teurosurg., 6: 530-533. GRUSS, W. 1932 Ueber Ganglien in Ramus Communicans. Z. Anat. u. Entwg., 9’7: 464-471. 1931 Distribution of afferent fibers via the KUNTZ,A., AND D. I. FARNSWORTH sympathetic trunks and gray communicating rami to the brachial and lumbosacral plexuses. J. Conip. Neur., 5 8 : 389-399. PICK, J., AND D. SHEEHAN1946 Sympathetic rami in man. J . Anat., 80: 12-20. ROW, F. 1931 Neue Befunde iiber die Entwicklung des Sympathicus. Verh. Anat. Ges. Jena., 40: 89-94. SKOOG,T. 1947 Ganglia in the communicating rami of the cervical sympathetic trunk. Lancet, 2: 457-460. SWEET, W. H., AND J. C. WHITE 1953 Disposition of pain fibers in some of the sympathetic nerves in man. Trans. Am. Neurol. Assoc., 78: 131-1 36. 1949 Anatomical studies of affereiicy THREADGILL, F. D., AND 0. SOLNITZKY within the lumbosacral sympathetic ganglia. Anat. Rec., lQ3 : 96. VAN HARREVELD, A., AND H. N. SMITH 1953 On a “sympathetic” component of the afferent innervation of trunk dermatomes. J. Neurophysiol., 15: 313-318. WALKER,E. A., AND F. NULSEN1948 Electrical stimulation of the upper thoracic portion of the sympathetic chain in man. Arch. Neurol. and Psychiat., 59: 559-560. WRETE,M. 1935 Die Entwickelung der intermediiiren Ganglien beim Menschen. Gegenbauer ’s Morph. Jahrb., 7’5 : 229-268. 1951 Ganglia of rami communicantes in man and mammals particularly monkey. Acta Anat., I S : 229-236.