The History Of Me Arch Of Neurol

HISTORY OF NEUROLOGY SECTION EDITOR: CHRISTOPHER G. GOETZ, MD

The History of Dermatome Mapping Steven A. Greenberg, MD

D

ermatome maps are commonly used in clinical neurology. These maps are valuable for the localization of varied sensory phenomena in patients with neurological disorders. The methods used in the construction of the classic maps by Sir Henry Head, Sir Charles Sherrington, Otfrid Foerster, and Jay Keegan and Frederic Garrett are of historical interest and are relevant to the current understanding of dermatome anatomy and physiology. In particular, the work of Derek Denny-Brown and his colleagues demonstrates that patterns of dermatomal sensory loss depend on the anatomical and physiological characteristics of large regions of nervous tissue, multiple adjacent dorsal ganglia, and the nearby caudal and rostral spinal cord. Arch Neurol. 2003;60:126-131 The word dermatome refers to a correspondence between the skin and the nervous system. Ambiguity exists with regard to the aspect of skin function involved (distinct cutaneous sensations), precise neural structure mapped (spinal nerve, dorsal root, dorsal horn, or spinal segment), and nature of the correspondence (anatomical, physiological, overlapping, or degree of individual variation). Some of the difficulties in the construction of dermatome maps have resulted from nontrivial differences in these 3 aspects of the definition. Dermatomes defined by cutaneous areas of hypersensitivity to light touch may not be the same as those defined by areas of hyposensitivity. Dorsal horn and spinal nerve lesions may not produce the same areas of sensory disturbance. Whether the nature of the correspondence is anatomical rather than physiological with specific conditions is crucial. Despite a generally assumed anatomical definition of the dermatome, the maps in current use have been constructed mostly by physiological methods. The ability of the central nervous system to modulate the activity of primary sensory neurons through suppression, facilitation, and reorganization suggests that dermatomes may not represent static anatomical relationships.

From the Department of Neurology, Division of Neuromuscular Disease, Brigham and Women’s Hospital, Harvard Medical School, Boston, Mass.

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The ambiguity concerning which neural structures correspond to the skin in various maps is not trivial. Intersegmental anastomoses exist among posterior spinal rootlets, allowing for sensory neurons with a ganglion cell at one level to enter the spinal cord at a different level.1-4 In addition, ventral roots contain afferents, the function of which remains uncertain.5,6 Thus, dorsal roots, dorsal root ganglia, and spinal nerves may differ in their supply of skin. The concept of spinal cord segments is also problematic.7-10 The spinal cord is not segmented in the embryo; according to Warwick and Williams,7(p117) “it is only the paraxial mesoderm alongside the notochord which is physically segmented.” Cutaneous afferents can descend as much as 10 segments after entering the spinal cord.11 The existence of uniformly spaced posterior spinal rootlets exiting along the entire length of the spinal cord is often ignored in favor of an organizational scheme at the level of the dorsal root. PATTERNS OF SENSORY DISTURBANCES: THE WORK OF CHARCOT AND MITCHELL Jean Martin Charcot (1825-1893), the first European to occupy a chair of clinical neurology, and his contemporary Silas Weir Mitchell (1829-1914), an American medical and literary scholar who has been compared with Benjamin Franklin, were both

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concerned with sensory localization in clinical neurology, although not primarily at the level of the spinal nerve roots. Charcot, who described and named amyotrophic lateral sclerosis and contributed to our understanding of the group of inherited neuropathies termed Charcot-MarieTooth disease, commented on patterns of sensory disturbance in patients with spinal cord injuries and patients with hysteria. He noted (as Charles Brown-Sequard had) the crossed hemianesthesia present with unilateralspinalcordlesions“bounded above on a level with the spinal lesion by a well defined horizontal line, and bounded very exactly in front by the median line.”12(p104) Charcot did seem to err, however, in his belief that such crossed phenomena existed with lesions at the level of the cauda equina. In an example of the consequences of a lesion on the right side at the level of the third sacral nerve, he listed right motor paralysis affecting little more than the leg and foot; preservation of the sense of feeling on this side . . . ; complete or nearly complete anesthesia of the corresponding parts of the left side with retention of voluntary movement.12(pp121-122)

In patients with hysteria, he commented on nonphysiological sensory disturbances such as unilateral hemianesthesia in all sensory modalities, including vision, hearing, and taste. Mitchell, who treated many patients with injuries during the American Civil War, provided exhaustive studies on patients with peripheral nerve injuries and made many keen observations. Contrary to popular medical belief at the time, he noted that sensory and motor nerve filaments, after leaving the spinal nerve, likely remain in discrete physiological bundles rather than becoming randomly interspersed. The fascicular nature of peripheral nerve anatomy is now an essential element of clinical and electrodiagnostic methods, explaining why proximal nerve lesions occasionally exhibit the same initial manifestations as more distal ones. Mitchell also noted the overlap of cutaneous nerve territories and the value of anatomical patterns of nerve distribution. He emphasized the need for “cutaneous

nerve anatomy . . . to be made anew” and predicted, “[W]e shall soon come to understand correctly how much of the skin each great nerve supplies . . .”13(p403) Despite his meticulous and lasting descriptions of the clinical consequences of nerve injuries, he also erred when extrapolating to physiological theory: I am unwilling to look upon pain as a distinct sense with afferent tracks peculiar to itself. . . . It becomes more and more probable that pain is the central expression of a certain grade of irritation in any centripetal nerve.14(p40)

CLINICAL OBSERVATION IN SPINAL CORD DISEASE AND EARLY DERMATOME MAPS: THE WORK OF THORBURN AND STARR In a series of case studies, William Thorburn, a surgical registrar to the Manchester Royal Infirmary (Manchester, England), reported patterns of sensory disturbances in patients with spinal cord lesions that allowed him to publish some of the earliest dermatome maps.15-18 In his 1886 and 1887 articles, he reported his findings in patients with cervical cord lesions, and in 1888, in patients with cauda equina lesions. These reports focused as much on the motor deficits as the sensory deficits. By the time he wrote his 1893 article, his work on dermatomes had matured, and he published detailed maps of the lumbar and sacral dermatomes (Figure 1). Thorburn was quite aware that “certain serial sections of the nervous system” were responsible for the dermatomes and noted, “[I]t remains to be proved whether these ‘sections’ are spinal segments, nerve roots, or other serial arrangements.”18(p356) M. Allen Starr, a professor at the College of Physicians and Surgeons (New York, NY), also studied patients with cauda equina lesions and constructed maps of the lumbar and sacral dermatomes that were similar to those of Thorburn (Figure 2).19 CLINICAL OBSERVATION IN VISCERAL DISEASE AND HERPES ZOSTER: THE WORK OF SIR HENRY HEAD Henry Head was born in 1861 and died in 1940. He graduated from

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Trinity College (Cambridge, England) with a bachelor of arts in natural sciences and from University College Hospital (London, England) with his medical degree in 1892.20 His thesis, delivered in June 1892, was titled “On Disturbance of Sensation, With Especial Reference to the Pain of Visceral Disease.”21 This article, along with a second one in 1900 coauthored with Campbell and titled “The Pathology of Herpes Zoster and Its Bearing on Sensory Localization,” contains Head’s view on dermatomes.22 His later work was almost entirely devoted to the sensory system, at all levels of the nervous system. He experimented on himself by sectioning his superficial radial nerve and meticulously describing the sensory disturbance across time. Head postulated the existence of 2 sensory systems: protopathic and epicritic. He was the editor of Brain from 1910 to 1925 and was knighted in 1927. For the last 20 years of his life, he had Parkinson disease.20 Head used the location of the rash in herpes zoster, studies of patients with visceral nonneurological disorders and spinal cord injuries, and conjecture to make his dermatome maps (Figure 3). His first article began with the discovery of areas of cutaneous tenderness in association with visceral disease; for example, “positions over which the patient experienced pain in gastric disturbances.”21 (p1) This was not referred pain but referred cutaneous tenderness or allodynia (the production of pain from nonnoxious stimuli). He constructed charts showing the distribution of this cutaneous tenderness in various diseases, which others have called “Head zones.” He then proceeded to collect cases of herpetic eruptions and was astonished to find that they agreed in an extraordinary way with the areas of tenderness that [he] had observed in visceral disease.21(p8)

He concluded that there must be some level of the nervous system at which these similar phenomena are organized, debated the possibilities including the cerebral cortex, spinal cord, dorsal roots, and peripheral nerves, and concluded, “[M]y areas correspond to the supply not of roots, but of segments of spinal cord from which the roots in

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L1

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S3

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S1 Fig. 7.

Fig. 8.

Fig. 7. – "L1, first lumbar; L2, second lumbar, &c.; S1, first sacral, &c." Fig. 8. – "L4, fourth lumbar, &c.; S1, first sacral, &c."

Figure 1. William Thorburn’s 1893 dermatome maps. Note the proximal extension of L4 and the assignment of the medial foot to S1. Reprinted with permission from Oxford University Press, Oxford, England.18

part arise.”21(p42) Thus, at first he believed that the dermatomes corresponded to spinal cord segments, not posterior roots. It is instructional to review in some detail Head’s approach to labeling the lumbar dermatomes in his 1893 article. First, the L1 dermatome was determined using a case of sensory loss due to “a fracture of the first and second lumbar vertebrae,”21 (p45) which surgical inspection showed affected the L1 roots but spared the T12 roots. He concluded that the upper border of sensory loss in this case was the upper border of the L1 dermatome. This conclusion ignored the

possibility of the overlap of dermatomes and contradicted his claim in the same article that his areas corresponded to the spinal cord, not the roots. Because this upper border of L1 corresponded to the upper border of one of his zones of cutaneous tenderness, the “gluteocrural area,” Head concluded that the areas were identical and thus took the lower border of the gluteocrural area to be the lower border of the L1 dermatome. After a determination of the S1 to S5 dermatomes, Head next outlined L5 by analysis of cutaneous tenderness in a case of acute inflammation of the right lobe of the pros-

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tate gland. Because the lateral area of the leg was the only portion of this cutaneous zone not already part of a defined dermatome (L1 and S1-S5 were the remaining parts of the zone), Head concluded that it likely represented another dermatome. Because of its adjacency to the sacral skin segments, he concluded that it was L5. This theory introduced another bias; namely, that adjacent skin segments would have adjacent root and spinal segments, a hypothesis that was not true in other segments of his own map (L4 and S2). Using a case of presumed spinal cord injury (the pathologic characteristics were unknown), Head next determined the L4 dermatome. A case of herpeszosterrashwasthenusedtodetermineL3.Headconjecturedthatthis patient’s rash involved 3 dermatomes, L3 to L5. The portion of the rash outside of Head’s already determined L4 andL5segmentswasthentakentorepresent L3. Each dermatome was determined in part by conjecture, ending with L2, which was simply assumed to be the area between L1 and L3. In Head’s 1900 article,22 he extended his work to include the cervical dermatomes and made extensive use of the location of the rash of herpes zoster. The localization of root involvement in his cases of herpes zoster was almost always unknown, except in 16 autopsy cases. Among these 16 cases, only 8 segments were represented, all between T1 and L1. Head had no pathologic confirmation for dermatomes C5 through C8 or for any area below L1; he considered his maps of the arm and leg to be of uncertain accuracy. ANIMAL AND HUMAN EXPERIMENTATION: THE WORK OF SHERRINGTON AND FOERSTER Sir Charles Scott Sherrington (18571952) studied the dermatomes in monkeys using the “method of remaining sensibility.” Several roots above and below a given root were sectioned, and the area of remaining sensibility on the skin was attributed to the unsectioned root. Sherrington published dermatomal maps in 1893 and 1898. 23,24 His medical interests were broad and included important work on cholera and diphtheria antitoxins. He is best

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VII VI V IV III II I

VII

VI IV

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V

Areas of interest in lesions at various levels of the spinal cord from sacral v. to lumbar ii. IV. Sacral i. V. Lumbar v. VI. Lumbar iii.

I. Sacral v. II. Sacral iv. III. Sacral iii. VII. Lumbar ii.

Figure 2. M. Allen Starr’s 1892 dermatome maps. Note the distal extension of L2 (labeled VII) and L3 (labeled VI) and the lack of extension of S1 below the knee.19

known for his work on the physiological characteristics of the neuron, which led to a Nobel Prize in Physiology or Medicine in 1932, shared with E. D. Adrian. Otfrid Foerster applied Sherrington’s approach to people, stating, I have had the opportunity of defining a great number of dermatomes in man by exactly the same method as that used by Sherrington. . . . I need not discuss the circumstances under which such a selected procedure may be undertaken.25(p4)

Born in 1893, he studied medicine at the Universities of Freiburg and Kiel in Germany and at the University of Breslau in Poland. He received his medical degree at 24 years of age and was a neurologist until age 40 years, when he began to practice neurosurgery as well. Robert Wartenberg, MD, said of Foerster, [A]t heart he was a neurophysiological experimenter. He helped his patients, but they had to pay the price by being subjected to physiological experimentation.20(p555)

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Foerster’s published maps did not show the back or portions of the limbs. He concluded that the dermatomes overlapped, that the resection of 1 single root in a human being was never followed by a loss of sensibility (this same conclusion having been reached by Sherrington), that differing sensory modalities had different dermatomes (Head but not Sherrington had believed this), and that sensibility within an entire dermatome appeared to require only 1 rootlet from the entire posterior root to be intact. VERTEBRAL DISK HERNIATION: THE WORK OF KEEGAN AND GARRETT The first report of a herniated disk causing back and leg pain appeared in 1934.26 Starting in 1943 and in a subsequent series of articles, Keegan and Garrett introduced the notion that disk compression of a single nerve root resulted in an area of diminished cutaneous sensibility.27-32 This idea, a tenet of neurological practice today, contradicted the work of Sherrington and Foerster, who believed that no disturbance of sensibility resulted even from the complete section of a single posterior nerve root. The different physiological characteristics of nerve root compression and sectioning may account for these differences. Keegan and Garrett constructed dermatomal maps for the limbs of areas of hyposensitivity (all modalities involved) in patients with surgically verified disk herniations at cervical and lumbar levels. These maps were strikingly different from those of Head and Foerster; the dermatomes were neat bands that always reached the posterior midline and generally ran the entire length of the limb (Figure 4). Similar to Head but unlike Sherrington and Foerster, Keegan and Garrett’s scheme showed no overlap of dermatomes. MODERN ANIMAL PHYSIOLOGY: THE WORK OF DENNY-BROWN, KIRK, AND YANAGISAWA Denny-Brown, E. J. Kirk, and N. Yanagisawa published studies on monkeys starting in 1968 that had a profound influence on the view that

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Figure 3. Sir Henry Head’s 1893 dermatome maps. Minor variations of these maps are frequently reproduced in current clinical texts. Reprinted with permission from Oxford University Press, Oxford, England.21

C2 C2 C3

C4 C5 T1 T2 T3 T4 C 5 T T5 1 T6 T7 T8 T9 T10 T11 T12 L1 C 6

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Figure 4. Jay Keegan and Frederic Garrett’s dermatome maps. These distinctive maps show all dermatomes as bands reaching the posterior midline and running the entire length of the limbs. Reprinted with permission from Wiley-Liss Inc, a subsidiary of John Wiley & Sons Inc, New York, NY.32

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existed prior to their work, that of the dermatome as a static, anatomical structure.33-35 Their findings, although of interest to sensory physiologists, do not seem to be a part of modern neurological teaching. These men found that in monkeys, dermatomes corresponding to the dorsal root ganglia were different from those corresponding to the dorsal roots, that dermatomes could significantly expand in size by physiological without anatomical changes, and that discrete lesions of the spinal cord, even caudal to the level of the root, could dramatically alter the size of the dermatome. They found that spinal cord and neighboring dorsal root ganglia affected the sensory territory of a given ganglion. Initially, the method of remaining sensibility was used to isolate a root, sectioning 3 roots above and 3 roots below. The intact sensory region of the skin was labeled as the corresponding dermatome. Distinct experiments were performed by sectioning the roots just distal or proximal to the ganglia. In both experiments, there was only 1 intact ganglion capable of subserving sensory function of the skin over a region spanning 7 roots. However, the dermatomes were smaller with the distal than with the proximal sectioning. Thus, having neighboring ganglia with spinal cord connections that are intact yet presumably isolated from the skin enlarges the dermatome; that is, neighboring ganglia facilitate sensory transmission of the given ganglion. The finding that subcutaneous injection of strychnine, which interferes with spinal inhibition, resulted in the expansion of an isolated dermatome strengthened this hypothesis. Denny-Brown, Kirk, and Yanagisawa demonstrated that the anatomical territory of a given root could be altered by purely physiological manipulation. Through a series of other experiments, they showed that the Lissauer tract, a superficial, tightly packed bundle of fibers close to the substantia gelatinosa (from which about 75% of its fibers arise), mediated the spinal effects on dorsal root transmission.35 The medial portion of the Lissauer tract facilitates sensory function (lesions in this area

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cause the dermatomes to shrink), and the lateral portion inhibits sensory function (lesions cause dermatomes to expand). The administration of strychnine after medial lesions results in reexpansion of the dermatome. The precise mechanisms involved remain unknown. The view of the dermatomes reached by Denny-Brown, Kirk, and Yanagisawa is that there is no simple correspondence between a given dorsal root and an area of skin; rather, dermatomal sensory loss depends on the anatomical and physiological characteristics of large regions of nervous tissue, multiple adjacent dorsal ganglia, and the nearby spinal cord. Perhaps because of the complexity it implies, their work has not had significant clinical effects and has been completely ignored in modern textbook discussions of dermatomes. However, their view has been supported by subsequent studies. The potential for the Lissauer tract to modulate gross expansions in the receptive fields of dorsal horn interneurons has recently been demonstrated.36 Only minor studies on the dermatomes have subsequently been published. Several clinical studies involving nerve blocks and nerve stimulation have been conducted. Some of the difficulties in interpreting these studies involve the dermatome definition’s ambiguity. The mapping of pain location from nerve root stimulation seems to represent referred pain from deep structures, not cutaneous sensibility.37 Anatomical techniques in rats, including intravenous injection of Evans blue dye followed by electrical stimulation of a spinal nerve’s ventral ramus, results in dye extravasation into the skin in defined patterns.38 It is unclear whether these patterns represent maximal anatomical innervation of a single spinal nerve and to what extent the spinal and adjacent sensory ganglia contribute to this occurrence. Dermatomal evoked potentials have also been explored as a means of derma-

tome mapping in animals.39 The rich history of dermatome mapping will likely continue into the future. Accepted for publication September 24, 2002. Corresponding author and reprints: Steven A. Greenberg, MD, Department of Neurology, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115 (e-mail: [email protected]). REFERENCES 1. Pallie W. The intersegmental anastomoses of posterior spinal rootlets and their significance. J Neurosurg. 1959;16:188-196. 2. Pallie W, Manuel JK. Intersegmental anastomoses between dorsal spinal rootlets in some vertebrates. Acta Anat (Basel). 1968;70:341-351. 3. Schwartz HG. Anastomoses between cervical nerve roots. J Neurosurg. 1956;13:190-194. 4. Moriishi J, Otani K, Tanaka K, Noue S. The intersegmental anastomoses between spinal nerve roots. Anat Rec. 1989;224:110-116. 5. Hosbuchi Y. The majority of unmyelinated afferent axons in human roots probably conduct pain. Pain. 1980;8:167-180. 6. Willis WD, Coggeshall RE. Sensory Mechanisms of the Spinal Cord. New York, NY: Plenum Press; 1991. 7. Warwick R, Williams PL. Gray’s Anatomy. 36th British ed. Philadelphia, Pa: WB Saunders; 1980. 8. Keynes R, Lumsden A. Segmentation and the origin of regional diversity in the vertebrate central nervous system. Neuron. 1990;4:1-9. 9. Keynes RJ, Stern CD. Segmentation in the vertebrate nervous system. Nature. 1984;310:786-789. 10. Lim TM, Jacques KF, Stern CD, Keynes RJ. An evaluation of myelomeres and segmentation of the chick embryo spinal cord. Development. 1991; 113:227-238. 11. Neuhuber WL. Central projections of cervical primary afferents in the rat. In: Zenke W, Neuhuber WL, eds. The Primary Afferent Neuron. New York, NY: Plenum Press; 1990:173-188. 12. Charcot JM. Lectures on the Diseases of the Nervous System [facsimile of the London, England, 1881 ed]. New York, NY: Hafner Publishing; 1962. 13. Mitchell SW. The supply of nerves to the skin. Philadelphia Medical Times. 1874;4:401-403. 14. Mitchell SW. Injuries of nerves and their consequences [facsimile of the 1872 ed]. New York, NY: Dover Publications; 1965. 15. Thorburn W. Cases of injury to the cervical region of the spinal cord. Brain. 1886;9:510-543. 16. Thorburn W. On injuries of the cauda equina. Brain. 1887-1888;10:381-407. 17. Thorburn W. Spinal localizations as indicated by spinal injuries. Brain. 1888-1889;11:289-324. 18. Thorburn W. The sensory distribution of spinal nerves. Brain. 1893;16:355-374. 19. Starr MA. Local anesthesia as a guide in the diagnosis of the lower spinal cord. Am J Med Sci. 1892;104:14-35.

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20. Haymaker W, Schiller F. The Founders of Neurology. 2nd ed. Springfield, Ill: Charles C Thomas Publisher; 1970. 21. Head H. On disturbances of sensation with especial reference to the pain of visceral disease. Brain. 1893;16:1-133. 22. Head H, Campbell AW. The pathology of herpes zoster and its bearing on sensory localization. Brain. 1900;23:353-523. 23. Sherrington CS. Experiments in examination of the peripheral distribution of the fibers of the posterior roots of some spinal nerves, I. Philos Trans R Soc Lond B Biol Sci. 1893;184:641-763. 24. Sherrington CS. Experiments in examination of the peripheral distribution of the fibers of the posterior roots of some spinal nerves, II. Philos Trans R Soc Lond B Biol Sci. 1898;190:45-187. 25. Foerster O. The dermatomes in man. Brain. 1933; 56:1-39. 26. Mixter WJ, Barr JS. Rupture of the intervertebral disc with involvement of the spinal canal. N Engl J Med. 1934;211:210-215. 27. Keegan JJ. Dermatome hypalgesia associated with herniation of intervertebral disk. Arch Neur Psych. 1943;50:67-83. 28. Keegan JJ. Neurosurgical interpretation of dermatome hypalgesia with herniation of the lumbar intervertebral disc. J Bone Joint Surg. 1944; 26:238-248. 29. Keegan JJ. Diagnosis of herniation of lumbar intervertebral disks by neurological signs. JAMA. 1944;126:868-873. 30. Keegan JJ. Dermatome hypalgesia with posterolateral herniation of lower cervical intervertebral disc. J Neurosurg. 1947;4:115-139. 31. Keegan JJ. Relations of nerve roots to abnormalities of lumbar and cervical portions of the spine. Arch Surg. 1947;55:246-270. 32. Keegan JJ, Garrett FD. The segmental distribution of the cutaneous nerves in the limbs of man. Anat Rec. 1948;102:409-437. 33. Denny-Brown D, Kirk E. Hyperesthesia from spinal and root lesions. Trans Am Neurol Assoc. 1968; 93:116-120. 34. Kirk E, Denny-Brown D. Functional variation in dermatomes in the macaque monkey following dorsal root lesions. J Comp Neurol. 1970;139:307320. 35. Denny-Brown D, Kirk EJ, Yanagisawa N. The tract of Lissauer in relation to sensory transmission in the dorsal horn of spinal cord in Macaque monkey. J Comp Neurol. 1973;151:175-200. 36. Wall PD, Lidierth M, Hillman P. Brief and prolonged effects of Lissauer tract stimulation on dorsal horn cells. Pain. 1999;83:579-589. 37. Slipman CW, Plastaras CT, Palmitier RA, Huston CW, Sterenfeld EB. Symptom provocation of fluoroscopically guided cervical nerve root stimulation: are dynatomal maps identical to dermatomal maps? Spine. 1998;23:2235-2242. 38. Takahashi Y, Nakajima Y. Dermatomes in the rat limbs as determined by antidromic stimulation of sensory C-fibers in spinal nerves. Pain. 1996;67: 197-202. 39. Kukulinsky DH, Brown PB. Cat L4-S1 dermatomes determined by signal averaging. Neurosci Lett. 1979;13:79-82.

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