the history of me arch of neurol

8/14/2019 The History of me Arch of Neurol

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SECTION EDITOR: CHRISTOPHER G. GOETZ, MD

The History of Dermatome MappingSteven A. Greenberg, MD

D ermatome maps are commonly used in clinical neurology. These maps are valuablefor the localization of varied sensory phenomena in patients with neurological dis-orders. 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 physi-ology. In particular, the work of Derek Denny-Brown and his colleagues demonstrates that pat-terns 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 rostralspinal cord. Arch Neurol. 2003;60:126-131

The word dermatome refers to a corre-spondence between the skin and the ner-vous system. Ambiguity exists with re-gard to theaspect ofskin function involved(distinct cutaneous sensations), preciseneural structure mapped (spinal nerve,dorsal root, dorsal horn, or spinal seg-ment), and nature of the correspondence(anatomical, physiological, overlapping,ordegreeof individualvariation).Some of thedifficulties in the construction of derma-tome maps have resulted from nontrivialdifferences in these 3 aspects of the defi-nition. Dermatomes defined by cutane-ousareas of hypersensitivity to light touchmay not be the same as those defined byareas of hyposensitivity. Dorsal horn andspinal nerve lesions may not produce thesame areas of sensory disturbance. Whether the nature of the correspon-dence is anatomical rather than physi-ological with specific conditions is cru-cial . Despite a general ly assumedanatomical definition of the dermatome,the maps in current use have been con-structed mostly by physiological meth-ods. The ability of thecentralnervous sys-tem to modulate the activity of primarysensory neurons through suppression, fa-cilitation, and reorganizationsuggests thatdermatomes maynot represent static ana-tomical relationships.

Theambiguityconcerningwhichneu-ralstructurescorrespond to theskin invari-ousmaps isnottrivial. Intersegmentalanas-tomoses exist among posterior spinalrootlets, allowing forsensoryneuronswitha ganglioncell at one level toenter thespi-nal cord at a different level. 1-4 In addition,ventral roots contain afferents, the func-tion of which remains uncertain. 5,6 Thus,dorsal roots, dorsal root ganglia, and spi-nal nervesmay differ intheir supplyofskin.Theconcept ofspinalcordsegments is alsoproblematic. 7-10 The spinal cord is not seg-mented in the embryo; according to War-wickandWilliams, 7(p117) it isonly the par-axial mesoderm alongside the notochordwhich is physically segmented. Cutane-ous afferents can descend as much as 10segments after entering the spinal cord. 11The existence of uniformly spaced poste-rior spinal rootlets exiting along theentirelength of the spinal cord is often ignoredin favor ofanorganizational schemeat thelevel of the dorsal root.

PATTERNS OF SENSORYDISTURBANCES: THE WORK

OF CHARCOT AND MITCHELL

JeanMartin Charcot (1825-1893), the firstEuropean tooccupya chairof clinicalneu-rology, and his contemporary Silas WeirMitchell (1829-1914), an American medi-calandliterary scholar whohasbeen com-pared with Benjamin Franklin,were both

From the Department of Neurology, Division of Neuromuscular Disease, Brigham andWomens Hospital, Harvard Medical School, Boston, Mass.

HISTORY OF NEUROLOGY

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concerned with sensory localizationin clinical neurology, although notprimarily at the level of the spinalnerve roots.Charcot, whodescribedand named amyotrophic lateral scle-rosis and contributed to our under-standing of the group of inheritedneuropathies termedCharcot-Marie-Tooth disease, commented on pat-

terns of sensory disturbance in pa-tients with spinal cord injuries andpatients with hysteria. He noted (asCharles Brown-Sequard had) thecrossedhemianesthesia presentwithunilateralspinalcordlesionsboundedaboveonalevelwiththespinallesionbya welldefined horizontal line,andbounded very exactly in front by themedianline. 12(p104) Charcotdidseemto err, however, in his belief thatsuch crossed phenomena existedwith lesions at the levelof thecaudaequina. In an example of the conse-

quences ofa lesionon the right sideat the level of the third sacral nerve,he listedright motor paralysis affecting little morethan the leg and foot; preservationof the sense of feeling on this side . . . ;complete or nearly complete anes-thesia of the corresponding parts of theleft side with retention of voluntarymovement. 12(pp121-122)

In patients with hysteria, hecommented on nonphysiologicalsensory disturbances such as uni-lateral hemianesthesia in all sen-

sory modalities, including vision,hearing, and taste.Mitchell,whotreated many pa-

tientswith injuriesduringtheAmeri-can Civil War, provided exhaustivestudies on patients with peripheralnerve injuries and made many keenobservations. Contrary to popularmedical belief at the time, he notedthat sensory and motor nerve fila-ments, after leaving thespinalnerve,likely remain in discrete physiologi-cal bundles rather than becomingrandomly interspersed.The fascicu-

lar nature of peripheral nerve anat-omy is now an essential element of clinical and electrodiagnostic meth-ods, explaining whyproximal nervelesionsoccasionally exhibit the sameinitial manifestations as more distalones. Mitchell also noted the over-lap of cutaneous nerve territoriesand the value of anatomical pat-terns of nerve distribution. He em-phasized the need for cutaneous

nerve anatomy . . . to bemade anewandpredicted, [W]eshall sooncometo understand correctly how muchof the skin each great nerve sup-plies . . .13(p403) Despite his meticu-lous and lasting descriptions of theclinical consequences of nerve inju-ries, he also erred when extrapolat-ing to physiological theory:

I am unwilling to look upon pain as adistinctsense withafferent tracks pecu-liar to itself. . . . It becomes more andmoreprobable that pain is thecentralex-pression of a certain grade of irritationin any centripetal nerve. 14(p40)

CLINICAL OBSERVATION INSPINAL CORD DISEASE ANDEARLY DERMATOME MAPS:THE WORK OF THORBURN

AND STARR

In a series of case studies, WilliamThorburn, a surgical registrar to theManches te r Royal Inf i rmary(Manchester, England), reportedpatterns of sensory disturbances inpatients with spinalcord lesions thatallowed him to publish some of theearliest dermatome maps. 15-18 In his1886 and 1887 articles, he re-ported his findings in patients withcervical cord lesions, and in 1888,in patients with cauda equina le-sions.These reports focused asmuchon the motor deficits as the sensorydeficits. By the time he wrote his1893 article, his work on derma-tomes had matured, and he pub-lished detailed maps of the lumbarand sacral dermatomes ( Figure 1 ).Thorburn wasquite aware that cer-tain serial sections of the nervoussystemwere responsiblefor theder-matomes andnoted,[I]t remains tobe proved whether these sectionsare spinal segments, nerve roots, orother serial arrangements. 18(p356)

M.Allen Starr,a professor at theCollege of Physicians and Surgeons(New York, NY), also studied pa-tientswith cauda equina lesions andconstructed maps of the lumbarandsacraldermatomes that were similarto those of Thorburn ( Figure 2 ).19

CLINICAL OBSERVATIONIN VISCERAL DISEASE AND

HERPES ZOSTER: THE WORKOF SIR HENRY HEAD

Henry Head was born in 1861 anddied in 1940. He graduated from

Trinity College (Cambridge, En-gland)witha bachelorofarts innatu-ral sciencesandfromUniversityCol-legeHospital (London,England)withhismedical degree in1892. 20 Histhe-sis, delivered in June 1892, was titledOn Disturbance of Sensation, WithEspecialReferenceto thePainofVis-ceral Disease. 21 This article, along

with a second one in 1900 coau-thoredwithCampbellandtitledThePathology of Herpes Zoster and ItsBearing on Sensory Localization,contains Heads view on derma-tomes. 22 His laterworkwas almosten-tirelydevoted to the sensory system,at alllevelsof thenervous system.Heexperimentedon himself by section-ing his superficial radial nerve andmeticulously describing the sensorydisturbance across time. Head pos-tulatedtheexistenceof2 sensory sys-tems: protopathic and epicritic. He

was the editor of Brain from 1910 to1925 and was knighted in 1927. Forthe last20years ofhis life, hehad Par-kinson disease. 20

Head used the location of therash in herpes zoster, studies of pa-tients with visceral nonneurologicaldisorders andspinalcordinjuries,andconjecture to make his dermatomemaps( Figure 3 ).His firstarticle be-ganwith thediscovery ofareasofcu-taneoustendernessinassociationwithvisceral disease; for example, posi-tions over which the patient experi-

enced painin gastricdisturbances.21

(p1) This was not referred pain butreferred cutaneous tenderness or al-lodynia (the productionofpain fromnonnoxious stimuli). He con-structedcharts showingthedistribu-tion of this cutaneous tenderness invarious diseases, which others havecalled Head zones. He then

proceeded to collect cases of herpeticeruptions andwasastonished to findthatthey agreed inanextraordinaryway withtheareas of tenderness that [he]had ob-served in visceral disease. 21(p8)

He concluded that there mustbe some level of the nervous sys-temat which these similar phenom-ena are organized, debated the pos-sibilities including the cerebralcortex, spinalcord, dorsalroots,andperipheral nerves, and concluded,[M]y areas correspond to the sup-ply not of roots, but of segments of spinal cord from which the roots in




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part arise. 21(p42) Thus, at first he be-lieved that the dermatomes corre-spondedto spinalcord segments,notposterior roots.

It is instructional to review insome detailHeadsapproach to label-

ing the lumbar dermatomes in his1893 article. First, the L1 derma-tomewas determined using a case of sensory loss due to a fracture of thefirst andsecond lumbarvertebrae, 21(p45) which surgicalinspectionshowedaffected the L1 roots but spared theT12 roots.He concluded that theup-per border ofsensory loss in this casewas the upper border of the L1 der-matome.Thisconclusionignored the

possibility of the overlap of derma-tomes and contradicted his claim inthe same article that his areas corre-sponded to the spinal cord, not theroots. Because this upper border of L1 corresponded to the upper bor-

der of one of his zones of cutaneoustenderness, the gluteocrural area,Head concluded that the areas wereidenticalandthus took thelowerbor-der of thegluteocrural area to be thelower border of the L1 dermatome.

After a determination of theS1to S5 dermatomes, Head next out-lined L5 by analysis of cutaneoustenderness in a case of acute inflam-mation of the right lobe of the pros-

tate gland. Because the lateral areaof the leg was the onlyportionof thiscutaneous zone not already part of a defined dermatome (L1andS1-S5were the remaining parts of thezone),Head concluded that it likelyrepresented another dermatome. Be-cause of its adjacency to the sacralskin segments, he concluded that it

was L5. This theory introduced an-other bias;namely, thatadjacent skinsegments would have adjacent rootand spinal segments, a hypothesisthat was not true in other segmentsof his own map (L4 and S2).

Usinga case ofpresumedspinalcordinjury(thepathologiccharacter-isticswereunknown),Headnext de-terminedtheL4dermatome.Acaseof herpeszosterrashwasthenusedtode-termineL3.Headconjecturedthatthispatientsrashinvolved3dermatomes,L3toL5.Theportionoftherashout-

side ofHeadsalreadydetermined L4andL5segmentswasthentakentorep-resentL3.Eachdermatomewasdeter-mined in part by conjecture, endingwith L2, which was simply assumedto be the area between L1 and L3.

In Heads 1900 article, 22 he ex-tended his work to include the cer-vical dermatomes and made exten-siveuse ofthe location ofthe rashof herpeszoster. Thelocalizationof rootinvolvement in his cases of herpeszoster was almost always unknown,except in 16 autopsy cases. Among

these 16cases,only 8 segmentswererepresented, all between T1 and L1.Head had no pathologic confirma-tion for dermatomes C5 through C8or for any area below L1; he consid-ered his maps of the arm and leg tobe of uncertain accuracy.

ANIMAL AND HUMANEXPERIMENTATION:

THE WORK OF SHERRINGTONAND FOERSTER

Sir Charles ScottSherrington (1857-1952) studied the dermatomes in

monkeys using the method of re-maining sensibility. Several rootsabove and below a given root weresectioned, and the area of remain-ing sensibility on the skin was at-tributed to the unsectioned root.Sherrington publisheddermatomalmaps in 1893 and 1898. 23,24 Hismedical interestswere broad andin-cluded important work on choleraanddiphtheria antitoxins. He is best

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

S1

L2 L2

L5

S2

S3

L3

L4

L5

S1

S3

Fig. 7. Fig. 8.

L1

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




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known for his work on the physi-ological characteristics of the neu-ron, which led to a Nobel Prize in

Physiology or Medicine in 1932,shared with E. D. Adrian.OtfridFoerster appliedSherring-

tons approach to people, stating,

I have had the opportunity of defininga great number of dermatomes inman by exactlythe same method as thatused by Sherrington. . . . I need notdis-cuss the circumstances under whichsuch a selected procedure may be un-dertaken. 25(p4)

Born in 1893, he studied medi-cine at the Universities of Freiburgand Kielin Germany and at the Uni-

versity of Breslau in Poland. He re-ceivedhismedicaldegreeat 24 yearsofage andwasa neurologist untilage40 years, when he began to prac-tice neurosurgery as well. Robert Wartenberg, MD, said of Foerster,

[A]t heart he was a neurophysi-ological experimenter.He helped hispa-tients, but they had to pay the price bybeing subjected to physiological experi-mentation. 20(p555)

Foersters published maps didnot show thebackor portions of thelimbs. He concluded that the der-matomes overlapped, that the resec-tion of 1 single root in a humanbeing was never followed by a lossof sensibility (this same conclusionhaving been reached by Sherring-ton), that differing sensory modali-

tieshaddifferentdermatomes (Headbut not Sherrington had believedthis), and that sensibility within anentire dermatome appeared to re-quire only 1 rootlet from the entireposterior root to be intact.

VERTEBRAL DISKHERNIATION: THE WORK

OF KEEGAN AND GARRETT

The first report of a herniated diskcausing back and legpain appearedin 1934. 26 Starting in 1943 and in asubsequentseries of articles, Keegan

and Garrett introduced the notionthat disk compression of a singlenerve root resulted in an area of di-minished cutaneous sensibility. 27-32This idea, a tenet of neurologicalpractice today, contradicted thework of Sherrington and Foerster,whobelieved that no disturbanceof sensibility resulted even from thecomplete section of a single poste-rior nerve root. Thedifferent physi-ological characteristics of nerve rootcompression andsectioning mayac-count for these differences.

KeeganandGarrettconstructeddermatomal maps for the limbs of areas of hyposensitivity (all modali-ties involved) in patients with surgi-cally verified disk herniations at cer-vical and lumbar levels. These mapswere strikingly different from thoseof Head and Foerster; the derma-tomes were neat bands that alwaysreached the posterior midline andgenerally ranthe entire length of thelimb( Figure4 ).Similar toHeadbutunlike Sherrington and Foerster,KeeganandGarretts schemeshowed

no overlap of dermatomes.

MODERN ANIMALPHYSIOLOGY: THE WORKOF DENNY-BROWN, KIRK,

AND YANAGISAWA

Denny-Brown, E. J. Kirk, and N.Yanagisawa published studies onmonkeys starting in 1968 that had aprofound influence on the view that

Areas of interest in lesions at various levels of the spinal cord from sacral v. to lumbar ii.

I. Sacral v.II. Sacral iv.

III. Sacral iii.VII. Lumbar ii.

IV. Sacral i.V. Lumbar v.

VI. Lumbar iii.

VI

VII

VII

VIV

IVIIIIII

VI

IV

V

VI V

Figure 2. M. Allen Starrs 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




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existedprior to their work, thatofthedermatome as a static, anatomicalstructure. 33-35 Their findings, al-though of interest to sensory physi-ologists, do not seem to be a part of modern neurological teaching.

These men found that in mon-keys, dermatomes correspondingto the dorsal root ganglia were dif-

ferent from those corresponding tothe dorsal roots, that dermatomescould significantly expandin size byphysiological without anatomicalchanges, and that discrete lesionsof the spinal cord, even caudal tothe level of the root, could dramati-cally alter the size of the derma-tome. They found that spinal cordand neighboring dorsal root gan-glia affected the sensory territoryof a given ganglion.

Initially, themethod of remain-ing sensibility was used to isolate a

root, sectioning 3 roots above and3 roots below.The intact sensory re-gion of the skin was labeled as thecorresponding dermatome. Dis-tinct experiments were performedbysectioning the roots just distal orproximal to the ganglia. In both ex-periments, there was only 1 intactganglioncapable of subserving sen-sory function of the skin over a re-gion spanning 7 roots.However, thedermatomes were smaller with thedistal than with the proximal sec-tioning. Thus, having neighboring

ganglia with spinal cord connec-tions that are intact yet presumablyisolated from the skin enlarges thedermatome; that is,neighboringgan-glia facilitate sensory transmissionof the given ganglion. The findingthatsubcutaneousinjection ofstrych-nine,whichinterfereswith spinal in-hibition, resulted in the expansionof an isolated dermatome strength-enedthishypothesis. Denny-Brown,Kirk, and Yanagisawa demonstratedthat theanatomicalterritory ofagivenroot couldbealtered bypurelyphysi-

ological manipulation.Through a series of other ex-periments, they showedthat theLis-sauer tract, a superficial, tightlypacked bundle of fibers close to thesubstantia gelatinosa (from whichabout 75% of its fibers arise), medi-ated thespinal effects on dorsal roottransmission. 35 The medial portionof the Lissauer tract facilitates sen-sory function (lesions in this area

C4

D2

D4

D6C6

D8D2

D10 C8

D12L2

C3 C3 C4 C6D2D4

D6

D8

D2

D10

C8

D12L2

SAC 3

L2

L4

SAC 1

L5

SAC 4

SAC 2

L1D1

L3

C5D1

D3D5

D7

C7

D9

D11

C7

D3

C5

D5

D3

D7

D9

D11C7L1

D1

L3

L5L4

SAC 1

Figure 3. Sir Henry Heads 1893 dermatome maps. Minor variations of these maps are frequentlyreproduced in current clinical texts. Reprinted with permission from Oxford University Press, Oxford,England.21

VENTRALAXIAL LINEOF ARM

C2

C3

C 6

C 8

C 8 L

2

L 3

L 4

L 5

C 7

C 7

T 1 T

1

C 5 C

5

VENTRAL AXIALLINE OF LEG

C5C4

T1T2

T3T4T5T6T7T8

S1

C6

T9T10T11

L1

S 2

T12

C7T1

T3

T5T7T9

T11L1

L3L5

S2

C6C8T2T4

T6T8

T10T12L2L4

S1

S1

S2

S2

L5 L

4S1

S1

C5C4

C3

C2

Figure 4. Jay Keegan and Frederic Garretts dermatome maps. These distinctive maps show alldermatomes 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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cause the dermatomes to shrink),and the lateral portion inhibits sen-soryfunction (lesions cause derma-tomes to expand). The administra-tion of strychnine after mediallesionsresults in reexpansion of thedermatome. The precise mecha-nisms involved remain unknown.

The view of the dermatomes

reached by Denny-Brown, Kirk, andYanagisawa is that there is no simplecorrespondencebetween a givendor-sal root and an area of skin; rather,dermatomalsensory loss dependsonthe anatomical and physiologicalcharacteristicsof largeregionsofner-vous tissue, multipleadjacent dorsalganglia, and the nearby spinal cord.Perhaps because of thecomplexity itimplies, their work has not had sig-nificant clinical effects and has beencompletely ignored in modern text-book discussions of dermatomes.

However, their view has been sup-portedbysubsequentstudies.The po-tential for the Lissauer tract tomodu-lategrossexpansionsin thereceptivefieldsofdorsalhorn interneuronshasrecently been demonstrated. 36

Only minor studies on theder-matomes have subsequently beenpublished. Several clinical studiesinvolving nerve blocks and nervestimulation have been conducted.Some of thedifficulties in interpret-ing these studies involve the derma-tome definitions ambiguity. Themappingofpain locationfrom nerveroot stimulation seems to repre-sent referred pain from deep struc-tures, not cutaneous sensibility. 37Anatomical techniques in rats, in-cluding intravenous injection of Evans blue dye followed by electri-cal stimulation of a spinal nervesventral ramus, results in dyeextrava-sation into the skin in defined pat-terns. 38 It is unclear whether thesepatternsrepresent maximal anatomi-cal innervation of a single spinalnerve and to what extent the spinaland adjacent sensory ganglia con-tribute to this occurrence. Derma-tomal evoked potentials have alsobeen explored as a means of derma-

tomemapping in animals. 39 Therichhistory of dermatome mapping willlikely continue into the future.

Acceptedfor publicationSeptember24, 2002.

Corresponding author andreprints: Steven A. Greenberg, MD,Department of Neurology, Brighamand Womens Hospital, 75 FrancisSt, Boston, MA 02115 (e-mail:[email protected]).

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