Clin Anat 07 Spinal Segmental Bone Innervation

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REVIEW

The Evidence for the Spinal SegmentalInnervation of Bone

JASON J. IVANUSIC*

Department of Anatomy and Cell Biology, University of Melbourne, Victoria, Australia

Dermatomes and myotomes are areas of skin and muscle, respectively, thatare innervated by single spinal segmental nerves, and reflect a principle of or-ganization that appears in just about every clinical textbook available today.The evidence for the existence of dermatomes and myotomes has a long andsubstantial history. A lesser known, but similar principle exists for the skeletalsystem. The term sclerotome was first used in the non-embryological sense

by Inman and Saunders ([1944] J. Nerv. Ment. Dis. 99:660667) to define aregion of bone and periosteum that is innervated by a single spinal segment.It is used by clinicians in many healthcare settings to aid in the diagnosis anddescription of a variety of deep and/or skeletal tissue pathologies and painsyndromes. In this article, the evidence for the existence of the sclerotomes isdescribed in detail. Early clinical studies that define the sclerotomes, evidencefrom studies of the development of skeletal innervation, and the contributionsof anatomical and physiological investigations are explored. It is suggestedthat there is in fact little direct evidence for the existence of discrete spinalsegmental innervation patterns for the skeleton. Clin. Anat. 20:956960,2007. VVC 2007 Wiley-Liss, Inc.

Key words: sclerotomes; segmental innervation of bone; skeletal innervation

INTRODUCTION

Dermatomes and myotomes are areas of skin and mus-

cle, respectively, that are innervated by single spinal seg-

mental nerves, and reflect a principle of organization that

appears in just about every clinical textbook available

today. Whilst textbook descriptions are often simplistic (for

example, they fail to account for considerable overlap in

territories innervated by adjacent spinal nerves), they are

used widely by clinicians in many healthcare settings to aid

in the diagnosis and description of a variety of conditions.

The evidence for the existence of dermatomes and myo-tomes has a long and substantial history (Warwick et al.,

1989; Greenberg, 2003).

A lesser known, but similar principle exists for the skele-

tal system. The term sclerotome was first used in the non-

embryological sense by Inman and Saunders (1944) to

define a region of bone and periosteum that is innervated

by a single spinal segment. This definition appears as a sec-

ondary meaning in (some) medical dictionaries. The pri-

mary use of the term by most anatomists and clinicians is

in descriptions of the ventromedial part of the embryologi-

cal somite, which ultimately forms the axial skeleton (see

Evidence From Developmental Studies). This embryologi-

cal definition cannot extend to the adult because the group

of cells that constitute the somite do not exist beyond the

embryonic stage, and the definition of Inman and Saunders

cannot be applied to the early stages of development

because the innervation of skeletal tissue is yet to fully de-

velop. To avoid ambiguity in the present review, the term

sclerotome is used to define a region of bone and perios-

teum innervated by a single spinal segment. When referring

to the embryological meaning, the term embryological

sclerotome is used. The same convention is applied to the

terms dermatome and myotome.A number of clinicians have used the sclerotomes, as

defined by Inman and Saunders (1944), in early discus-

*Correspondence to: Dr. Jason Ivanusic, Department of Anatomyand Cell Biology, University of Melbourne, Melbourne, VIC 3010,Australia. E-mail: [email protected]

Received 25 March 2007; Revised 15 August 2007; Accepted 4September 2007

Published online 22 October 2007 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/ca.20555

VVC 2007 Wiley-Liss, Inc.

Clinical Anatomy 20:956960 (2007)


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sions of backache (Rose, 1954; Wilson, 1967), cancer

(Klingon, 1961, 1964), fibrositis (Yunus et al., 1981), herni-

ated discs (Inman and Saunders, 1947), referred and deep

pain (Southworth and Krohn, 1950), nerve blocks to treat

pain (Dobney and Belam, 1963), and more recently, in dis-

cussions of bone disorders such as melorheostosis (Murray

and McCredie, 1979; North and McCredie, 1987) and thali-

domide induced malformations (McCredie, 1977; McCredieet al., 1984; McCredie and Willert, 1999). Chiropractors

today use published maps of sclerotomes in describing

deep, scleratogenous pain (Banner-Therapy-Products-

Inc., 2007). However, upon reviewing the literature, few

studies of the spinal segmental innervation of bone

could be found. In this article, the evidence for the exis-

tence of the sclerotome is reviewed. It is suggested that

there is in fact little direct evidence for the existence of the

sclerotome.

CLINICAL OBSERVATIONS

Dejerine (1914) was the first to construct a map of the

spinal segmental innervation of the bony skeleton. His work

was based on two principles. The first was the observation

that cutaneous (skin) and deep (muscle, tendon, bone, and

periosteum) sensitivity to pressure could, in cases of certain

central and peripheral nervous lesions, be dissociated

because an anesthetized area of skin may overly deeper tis-

sue that was not anesthetized, or vice versa. For example,

a C5 lesion causing cutaneous anesthesia over a bone,

without coincident deep anesthesia beneath the area of

anesthetized skin, indicated to Dejerine that the deep tissue

in that region was not innervated by the C5 spinal segment.

The second was meticulous cadaver dissection of spinal

nerves from their radicular origin. It is important to note

however, that much of the pressure Dejerine applied to

deep structures must have stimulated afferent fibers in

muscle, tendon and ligaments, rather than in periosteum

and bone alone. There are only a few sites in which boneand periosteum are in close apposition to skin without other

structures in between. Furthermore, it is difficult to con-

ceive that such a defined representation of the innervation

territory of single spinal nerves could be achieved by follow-

ing the fibers within a single spinal nerve through a periph-

eral plexus (e.g., lumbosacral plexus), multiple peripheral

nerves, and the very fine branches that innervate bone and

periosteum.

Kellgren (1939) reported a similar map by examining

the distribution of referred pain following injections of hypo-

tonic saline into deep tissues such as ligaments, tendons,

joint capsules, and muscles. When these deep tissues were

injected, the author noted that the pain experienced by

subjects was referred to cutaneous and muscular areas

associated with defined dermatomes or myotomes, andproposed that the innervation of the deep tissue must have

the same spinal segmental origin as the dermatome or

myotome that the pain was referred to. Using this tech-

nique, Kellgren carefully identified the spinal segmental

innervation patterns for deep tissue throughout the whole

body. The similarity between Kellgrens and Dejerines

maps confirms that what Dejerine mapped was most likely

the innervation of muscle, tendon and ligaments, not bone

and periosteum alone. Furthermore, at no stage was the

term sclerotome used in the study of Kellgren, and no claim

was made that this map was representing the segmental

innervation of bone and periosteum, yet some recent

reports quote this work when defining the sclerotomes. A

notable example is the published chiropractic charts of the

sclerotomes (Banner Therapy Products Inc., 2007). The

term sclerotome was not actually defined until later. This

highlights the notion that the use of the term sclerotome

has become somewhat ambiguous. In many cases, it has

been used to imply the spinal segmental innervation ofdeep tissues, including muscle, tendon, joint capsule, and

ligament as well as bone and periosteum, but this is an

incorrect use of the term.

Inman and Saunders (1944) were in fact the first to use

the term sclerotome in the non-embryological sense. They

studied the distribution of referred pain to non-bony tissues

in patients with focal bone lesions and a group of volunteers

that submitted to direct periosteal stimulation (scratching

with a fine needle), and reported a map of the spinal seg-

ments that were known to innervate the areas of referred

pain for each stimulus site, in a manner similar to that of

Kellgren. However, the distribution of referred pain is diffi-

cult to document accurately because it is generally

described as diffuse and dull, and often perceived over a

number of dermatomes or myotomes. In fact, Inman andSaunders acknowledged that: Our knowledge of the pre-

cise segmental innervation of the sclerotomal areas cannot

at the moment be given with any great precision. They

also commented that their aim was to map the extent of

scleratogenous pain, not to produce a segmental map, con-

trary to the opinions of future authors.

There exist a number of confounding issues regarding

the sclerotomes as derived from these early clinical obser-

vations. The first issue is that it is unclear as to how many

points on the bony skeleton were actually sampled in these

studies. It is difficult to imagine how these stimuli could be

applied to the whole skeleton when deep tissues such as

ligaments, tendons, and muscles overly bone at most points

in the skeleton. The second issue is the notion that when

stimuli were applied specifically to skeletal tissues, theywere applied to the periosteum (by pressure or scratching)

and not to the inside of bone. We are now aware that pri-

mary afferent fibers exist within bone (Bjurholm et al.,

1988; Hill and Elde, 1991; Mach et al., 2002), and that

they may be activated with many different stimulus types

(Furusawa, 1970; Seike, 1976). The segmental innervation

of the bone as opposed to the periosteum is yet to be

defined at all. A third point of contention is that most of

these studies were based on mapping the distribution of

referred or deep pain, but because pain of these types is so

dull and diffuse, it is difficult to ascribe the origin of the

pain to a single dermatome or myotome and thus to a sin-

gle spinal segment. Finally, referred pain is most likely an

indication of common segmental spinal cord mechanisms. It

is probable that spinal and supraspinal circuits influencedthe extent of referred pain perceived by subjects in these

studies, confounding the results reported. The accuracy of

the sclerotomes presented in these early studies was there-

fore questionable, and in line with the perceived lack of clin-

ical importance at the time, led to their exclusion in the

literature for many years. It should be emphasized that the

sclerotome maps marketed at present (aimed mainly at

chiropractic use e.g., Banner Therapy Products Inc., 2007)

are based on these early clinical observations. As a result,

they show only vague areas of deep, radiating or referred

pain, and not specific skeletal territories supplied by single

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spinal nerves. A more concise method for mapping the scle-

rotomes would result in a more effective use of the principle

in the clinical setting.

A number of more recent reports of patients with bone

disorders such as melorheostosis (Murray and McCredie,

1979; North and McCredie, 1987) and thalidomide induced

malformations (McCredie, 1977; McCredie et al., 1984;

McCredie and Willert, 1999) have cited the sclerotomes toexplain the pathology they observed. Thalidomide is well-

known for its anti-angiogenic and immuno-modulatory

properties, but was also used as an antiemetic agent to

control nausea in pregnant females in the 1960s (Perri and

Hsu, 2003; Franks et al., 2004). However, babies born to

mothers that had taken thalidomide developed gross

deformities involving skin, muscle, and skeletal structures.

Of the skeletal deformities, reductions of the limbs involving

malformation of the long bones were most obvious

(McCredie, 1977; McCredie et al., 1984; McCredie and

Willert, 1999). McCredie (1974) hypothesized that this was

a result of toxic damage to neural crest cells (the segmen-

tally organized precursors of peripheral sensory neurons).

She predicted that if a segment of neural crest fails to de-

velop, then one would expect the skeletal structures sup-plied by the sensory nerves derived from that segment to

be missing (or at least malformed), possibly because of

impaired neurotrophic influences. McCredie retrospectively

examined the radiographs of limb reductions in thalidomide

babies, and observed that most limb reductions could be

approximated by theoretically subtracting a single sclero-

tome, as mapped by Inman and Saunders (1944), from a

complete appendicular skeleton (McCredie, 1977; McCredie

et al., 1984; McCredie and Willert, 1999). She argued that

the sclerotomes provided a mechanism by which one could

explain the effects of thalidomide poisoning, and therefore

that they must indeed exist. However, there is some debate

as to whether thalidomide affects neural crest cells directly,

or causes secondary neuropathy related to an effect on tar-

get tissues (de Iongh, 1990). In addition, Strecker and Ste-phens (1983) showed that physically blocking the early de-

velopment of peripheral nerves did not result in any limb

reductions at all. DAmato et al. (1994) further showed that

thalidomide is a potent inhibitor of angiogenesis, and

Strecker and coworkers (Stephens et al., 2000; Stephens

and Fillmore, 2000) subsequently suggested that thalido-

mide inhibits the transcription of genes that drive angiogen-

esis. Therefore, it appears that the observed malformations

might result from a lack of blood supply to the developing

limb, not from a direct toxic effect on developing segmental

sensory neurons. This suggests that McCredies hypothesis

regarding the importance of the segmentally organized

neural crest cells in thalidomide teratogenicity may have

been overstated, and raises the possibility that the implied

existence of the sclerotomes may not be real.Melorheostosis is a disease that is characterized by

abnormal longitudinal growth of sclerotic tissue in long

bones. Murray and McCredie (1979) and North and McCre-

die (1987) loosely correlated the distribution of sclerotic tis-

sue in patients with the distribution of single sclerotomes,

as defined by Inman and Saunders (1944). They noted that

in some cases, cutaneous disturbances associated with a

single dermatome of the same segmental origin were also

present, reinforcing the notion that single spinal segments

could be associated with defined skeletal tissue territories.

An important feature of these studies is that melorheostosis

presents in the adult, and thus the pathological distribution

of the sclerotic tissue can be compared with the sclerotome

maps of Inman and Saunders (1944) with more confidence

than thalidomide induced limb reductions. Nonetheless, a

clearer understanding of how segmental innervation pat-

terns of skeletal tissues in both the embryo and the adult

are organized is required to support the hypotheses that

these authors present, and are indeed necessary to rein-force the idea that sclerotomes do exist in a form useful to

such discussion.

EVIDENCE FROM DEVELOPMENTALSTUDIES

The relationship between developing, segmentally

organized sensory and motor neurons in the embryo and

spinal segmental innervation patterns of skin and muscle in

the adult is well documented (Krull, 2001; Wang and Scott,

2002). Primary afferent neurons that innervate skin are

derived from neural crest cells that migrate away from the

developing neural tube and undergo significant proliferation

adjacent to primitive somites. Motorneurons originate in the

basal plate of the developing neural tube and their develop-

ing axons project into the primitive somites. Somites are

organized in a segmental manner, so when the peripheral

processes of neural crest cells, or axons of developing

motorneurons, extend into the adjacent somites they pro-

vide a template for the segmentation of these neurons. The

somites subsequently differentiate into three regions: an

embryological dermatome, embryological myotome, and

embryological sclerotome. The embryological dermatome

develops into axial skin and the embryological myotome

develops into both axial and appendicular muscle tissue, all

of which retain the segmental innervation patterns imposed

by the developing neurons. Skin of the limbs develops from

tissues associated with the outgrowth of the limb bud, so

the peripheral processes of developing neural crest cellshave to extend beyond the somite, and out to the develop-

ing limb bud to innervate their final target tissue. There is

significant evidence that this outgrowth is mediated by

either neurotrophic factors and/or contact guidance mecha-

nisms, and that the segmentation is maintained when the

processes travel over such long distances (Davies and

Lumsden, 1990; Wang and Scott, 2002). Thus, it appears

that the spinal segmental innervation patterns of skin and

muscle of the adult develop in part from patterns imposed

by somites during embryonic development.

If the embryonic development of the innervation of skel-

etal structures follows the same principles that exist for

skin and muscle, then it would seem reasonable to presume

that developing neurons in the embryo might also impose

segmental innervation patterns on the adult skeleton (andmanifest as sclerotomes). In the development of the axial

skeleton, neural crest cells extend peripheral processes into

the surrounding embryological sclerotome, forming the ba-

sis for segmental innervation of the axial skeleton, including

the vertebra and ribs. However, this is somewhat compli-

cated because each embryological sclerotome is split: its

cranial part forms the caudal part of the vertebra above,

and its caudal part forms the cranial part of the vertebra

below (Balling et al., 1992). This implies that in the adult, a

single spinal segmental nerve should innervate two adja-

cent vertebrae. This is not acknowledged in the maps of

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Dejerine (1914). Furthermore, Kellgren (1939) and Inman

and Saunders (1944) did not document segmental innerva-

tion patterns for axial tissues at all, and therefore offer no

clarification on the matter. The case for the appendicular

skeleton is also unclear. Peripheral processes of neural crest

cells extend into the mesenchyme of the limb bud

(Cameron and McCredie, 1982) which subsequently forms

the bones of the developing limb (Olsen et al., 2000). How-ever, the extent to which the developing primary afferent

fibers maintain segmental innervation patterns in develop-

ing limb bones is yet to be determined. Until these issues

are resolved, some caution should be practiced before pre-

suming that the development of segmentally organized

nerves in the embryo imposes a segmental innervation pat-

tern on adult skeletal tissues, as it appears to for cutaneous

and muscular tissue. The evidence to imply that this might

form the basis of the sclerotomes does not as yet exist.

ANATOMICAL AND PHYSIOLOGICALINVESTIGATIONS IN ANIMAL STUDIES

It is relatively easy to study the connections between a

single spinal nerve and either skin or muscle in animal stud-

ies. Connectivity has been established with electrophysio-

logical recordings of spinal nerve activity evoked by stimu-

lation of skin or muscle (Dykes and Terzis, 1981), muscle

activity evoked by electrical stimulation of single spinal

nerves (Browne, 1950; Thage, 1965), application of neuro-

anatomical tracers to skin and muscle (Takahashi et al.,

2003), and by dye extravasation following electrical stimu-

lation of single spinal nerves (Takahashi and Nakajima,

1996). Using these techniques, it has been possible to

define territories innervated by single spinal nerves and

then reconstruct a concise map representing the innerva-

tion patterns of many spinal nerves in skin and muscle.

Maps of dermatomes and myotomes produced in this way

are very similar to maps produced from clinical (and experi-mental) observations in human studies (Warwick et al.,

1989; Greenberg, 2003), and have provided empirical evi-

dence that spinal segmental innervation patterns do indeed

exist for skin and muscle. However, examining the connec-

tivity between the bony skeleton and spinal nerves is diffi-

cult, because bone is a very hard, mineralized tissue that is

difficult to work with. Most of the techniques applied to

establishing dermatomes and myotomes are not appropri-

ate for the determination of sclerotomes. A single study has

attempted to address the issue of the segmental innerva-

tion of bony tissue using anatomical techniques. Gajda

et al. (2004) placed a retrograde tracer (DiI) under the per-

iosteum of the rat tibia, which is easy to expose because of

its close proximity to the skin, and reported labeled neuro-

nal cell bodies in the dorsal root ganglia confined predomi-nantly to spinal cord levels L3 and L4. The author of the

present paper has observed similar results following injec-

tions of another retrograde tracer (Fast Blue) into either

the medullary cavity or epiphyses, in addition to the perios-

teum, of the rat tibia (Ivanusic, unpublished observations).

However, using this approach, it would be very difficult and

time consuming to place the tracer into enough points in

the skeleton to be able to reconstruct the whole sclerotomal

map. No other anatomical or physiological studies of con-

nectivity between single spinal nerves (or spinal cord seg-

ments) and bone could be found in the literature. It is clear

that anatomical and physiological techniques need to be

exploited further to study the sclerotomes. In particular,

empirical mapping of connectivity between single spinal

segmental nerves and bony tissues, as has been done for

skin and muscle, is required to confirm the existence of the

sclerotomes.

CONCLUDING REMARKS

The sclerotomes are used by clinicians in many health-

care settings to aid in the diagnosis and description of a va-

riety of deep and/or skeletal tissue pathologies and pain

syndromes. However, we are currently relying on early clin-

ical or experimental observations of referred mechanisms of

deep pain to approximate the sclerotomes. The maps

reported in the early literature are not complete, and they

should be interpreted with consideration of limits in the

techniques used. They show only vague areas of deep, radi-

ating or referred pain, and not specific skeletal territories

supplied by single spinal nerves. Further to this, a definitive

description of the sclerotomes in the adult is complicated by

the lack of knowledge regarding the development of skele-

tal innervation in the embryo. We do not have the evidence

to imply that the development of segmentally organized

nerves imposes a segmental innervation pattern on skeletal

tissues, as it appears to for cutaneous and muscular tissue.

Finally, there is little evidence based on anatomical and

physiological studies of the sort have been instrumental in

confirming the existence of segmental innervation patterns

in skin and muscle. Thus there appears to be little direct

evidence for the existence of the sclerotomes. It is pro-

posed that the nature of the segmental innervation of bony

tissue requires further attention. In particular, more detail

of the anatomical and physiological connections between

single spinal nerves and bone is required. Like the derma-

tomes and myotomes presented in many of the textbooks

today, this will reflect the true patterns of segmental inner-

vation of skeletal tissue in the adult, and provide a defini-tive basis upon which discussions of the sclerotomes can be

based in the future.

ACKNOWLEDGMENTS

The author thanks Dr. Pascal Carrive and Dr. Marius

Fahrer for their assistance in the translation of Dejerines

monograph (Dejerine, 1914).

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Clin Anat 07 Spinal Segmental Bone Innervation