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Year: 1995

Neural elements in dental pulp and dentin

Nair, P N

Nair, P N. Neural elements in dental pulp and dentin. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995,80(6):710-9.Postprint available at:http://www.zora.unizh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich.http://www.zora.unizh.ch

Originally published at:Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995, 80(6):710-9

Nair, P N. Neural elements in dental pulp and dentin. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995,80(6):710-9.Postprint available at:http://www.zora.unizh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich.http://www.zora.unizh.ch

Originally published at:Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995, 80(6):710-9


Abstract

This article addresses the structural and quantitative aspects of human tooth innervation and brieflyconsiders the functions and clinical relevance of tooth axons. The classification of peripheral axons, thepulpal and dentinal innervation, and the theories of dentin sensitivity are discussed. Quantitative studieson tooth innervation are also reviewed. Human premolars receive about 2300 axons at the root-apex ofwhich about 13% are myelinated and 87% are nonmyelinated fibers. Most apical myelinated axons arefast-conducting A delta-fibers with their receptive fields located at the pulpal periphery and inner dentin.These fibers are probably activated by a hydrodynamic mechanism and conduct impulses that areperceived as a short well-localized sharp pain. Most C-fibers are slow-conducting fine sensory afferentswith their receptive fields located in the pulp and transmit impulses that are experienced as dull poorlylocalized and lingering pain. In addition to the nociceptive alarm signaling, the intradental sensory axonsmay play a regulatory role in the maintenance and repair of the pulpodentinal complex.

Vol. 80 No. 6 December 1995

ENDODONTICS E di to r : R i c h a r d E. W a l t o n


P. N . Ramachandran Nair , Zurich, Swi tze r land INSTITUTE OF ORAL STRUCTURAL BIOLOGY, CENTRE OF DENTAL AND ORAL MEDICINE AND MAXILLOFACIAL SURGERY, UNIVERSITY OF ZURICH

This article addresses the structural and quantitative aspects of human tooth innervation and briefly considers the functions and clinical relevance of tooth axons. The classification of peripheral axons, the pulpat and dentinal innervation, and the theories of dentin sensitivity are discussed. Quantitative studies on tooth innervation are also reviewed. Human premolars receive about 2300 axons at the root-apex of which about 13% are myelinated and 87% are nonmyelinated fibers. Most apical myelinated axons are fast-conducting A8-fibers with their receptive fields located at the pulpal periphery and inner dentin. These fibers are probably activated by a hydrodynamic mechanism and conduct impulses that are perceived as a short well-localized sharp pain. Most C-fibers are slow-conducting fine sensory afferents with their receptive fields located in the pulp and transmit impulses that are experienced as dull poorly localized and lingering pain. In addition to the nociceptive alarm signaling, the intradental sensory axons may play a regulatory role in the maintenance and repair of the pulpodentinal complex. (ORAL SURG ORAL MED ORAL PATHOL ORAL RADIOt ENDOD 1995;80:710-9)

In the second century AD, Galen descr ibed the t r igemina l nerve as the third cranial nerve.1 No further p rogress was ach ieved dur ing the next 1600 years in our unders tanding o f the nelwe supply to the teeth. The t r igeminal nerve, today known as the fif th (V) cranial nerve, media tes all sensory impulses f rom the teeth to the central nervous system. The maxi l l a ry di- v i s ion (V2) suppl ies the upper teeth as the super ior a lveolar nerves. The mand ibu la r nerve (V3) d iv ides into the buccal , l ingual , and inferior a lveolar nerves. The latter, pass ing through the mand ibu la r canal, supply all the lower teeth. However , the incisors ~ and the lower molars 3 rece ive supplementa l nerve fibers f rom branches o f the m y l o h y o i d nerve. The l ingual , buccal , and aur icu lo tempora l nerves are also shown to p rov ide l imi ted innervat ion to the teeth. 3-6 Trans- med ian c rossover is an impor tant supplementary source o f innervat ion to the canines and the i n c i s o r s ] The lat ter are be l i eved to cause c o m m o n fai lures of

Presented at the Second Annual Connecticut Symposium on En- dodontic Biology. Received for publication Feb. 27, 1995; returned for revision June 23, 1995; accepted for publication July 11, 1995. Copyright �9 1995 by Mosby-Year Book, Inc. 1079-2104/95/$5.00 + 0 7/15/68045

710

l a n e I. Class i f ica t ion of m a m m a l i a n nerve fibers

Type Diameter Speed Function

Ac~ 12-22/am 70-120 m/s Motor: propfioception -[3 5-12 ~m 30-70 m/s Sensory: touch pressure --/ 3-6/am 15-30 m/s Motor: muscle spindles -8 2-5/am 12-30 m/ Sensory: sharp pain B <3/am 3-15 m/s Preganglionic autonomic C <2/am 0.5-2 m/s Sensory: dull pain

Postganglionic autonomic

anesthesia in c l in ica l dentistry. An unders tanding of these supplementa l innervat ions is impor tant to achieve comple te dental anes thes ia in some patients.

CLASSIFICATION OF PERIPHERAL NERVE FIBERS The conduct ion ve loc i ty o f nerve fibers is a func-

t ion of the axon diameterS; one o f the c lass i f icat ions of per iphera l axons (Table I) is based on this relat ionship. The group A and B fibers are myel i - nated, and their respect ive d iameters include the thickness o f mye l in sheaths. Group A is subdivided into c~, [3, % and ~ fibers in descend ing order of size, Group C a r e the smallest , nonmye l ina ted axons. As the process o f conduct ion is d i f ferent in nonmyel i - nated and mye l ina t ed axons, 9 the mathemat ica l rela-

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Nair 711 Volume 80, Number 6

Fig. 1. Transmission electron micrographic montage of intraradicular bundle of nerve fibers contains both myelinated (AN) and nonmyelinated (CN) axons. Note absence of perineurium around axon bundle. Rect- angular demarcated area is magnified in Fig. 2. (FI, fibroblasts; SC, Schwann cells.) (Original magnification x6800.)

tionship between the diameter and the velocity are not the same in both groups. In nonmyelinated axons the impulses move along the axons in the form of waves by what is known as continuous conduction, whereas the signals in myelinated fibers are trans- mitted as saltatory conduction 1~ in which the impulses jump from node of Ranvier to node of Ranvier (the Latin saltare means to leap). As a result, the

velocity of signal conduction in myelinated fibers increases in direct proportion to the diameter of the fibers, u whereas the increase in conduction velocity in nonmyelinated fibers is roughly pro- portional to the square root of the axonal diameter. 9 Only the smallest of group A (mostly A~ and few -[3, Fig. 1) and group C fibers (Fig. 2) innervate human teeth.

712 Nair ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY December 1995

Fig. 2. Magnified view of rectangular block in Fig. 1 shows fine structural details of nonmyelinated nerve fibers (CN) distributed among the myelinated axons (AN), Note wide variation in size of nonmyelinated axons. (SC, Schwann cells.) (Original magnification xl 1,500.)


PULPAL INNERVATION Nerve fibers enter teeth via apical foramina in the

form of bundles. 12 Unlike other peripheral nerves, the intradental nerves are devoid of perineuriems13; therefore the term fascicles is not generally used to describe tooth nerves. It probably was Arwil154 who first demonstrated the ultrastructure of both myelinated and nonmyelinated axons in human teeth. The axons are believed to pass through the root canal and arborize coronally to form the subodontoblastic plexus of Rashkow.55

DENTINAL INNFRVATION It is now generally accepted that the dentin is in-

nervatedJ 6 However, the question as to whether the nerve fibers end at the inner dentin or extend up to the outer dentin still is unresolved. The axons leave the plexus of Rashkow, 15 lose the myelin sheath, pass between the odontoblasts, and some of them reach the inner dentin as nonmyelinated axons. 17 These fibers are frequently found in the dentin surrounding pulpal horns, and their number declines toward the tooth apex.56, 58 With the use of the axonal transport technique, Byers and Dong 58 found nerve fibers in more than 50% of the tubules in inner cuspal dentin of monkey teeth. Dense innervation was also reported for the inner coronal dentin of rat molars 59 and feline teeth. 2~ Although the autoradiographic studies clearly demonstrated the presence of nerve fibers in the inner third of the mammalian dentin, they also revealed that various types of dentin and regions within are not uniformly innervated. Byers 17 states: "the innervation of tubular dentin (orthodentin) is graded, with the greatest innervation adjacent to the tip of the pulp h o r n . . , and fewest in the dentin of roots." In- terradicular and tertiary dentin is believed to be noninnervated. For obvious reasons the axonal transport technique cannot be used to study human tooth innervation. Transmission electron microscopy con- vincingly revealed the presence of intradentinal nerve fibers in animal 22' 23 and human 24-26 coronal dentin.

On the basis of these findings, it is believed that the coronal dentin is probably more densely innervated in order to register external stimuli to which the crown is exposed after tooth eruption. Alternatively, healthy root dentin that is protected in a bony socket from external stimuli is believed to be only sparsely innervated. However, an ultrastructural study on human third molars 27 showed the presence of nerve fibers in the radicular predentin. A recent electron microscopic study 28 showed numerous nerve fibers in predentin and few (but indisputable) axons in mineralized human root dentin (Fig. 3). Dense innervation of radicular predentin was also reported in a most recent im-

munoelectron-microscopic labeling study. 29 Such ultrastructural evidence clearly disagrees with the conclusions reached earlier on the basis of autoradiographic findings 17 that the radicular dentin is not or is only sparsely innervated.

It has long been debated whether the nerve fibers extend to the dentoenamel/cementum junction. Most currently available evidence suggests that axons do not traverse a distance beyond 0.2 mm into the coronal 17 and radicular dentin. 28 However, Fleche La et al. 3~ believed that they had found nerve fibers in "coronal dentinal tubules located near the dentoenamel junction." However, it should be pointed out that (1) their only high magnification electron micro- graph (x90,000) was not supported by overview pic- tures of lesser magnifications, (2) the outer leaflets of the plasma membranes of the odontoblastic process and a neighboring structure designated as a nerve fibril did show continuity, and (3) no ultrastructural differences could be discerned between the odontoblastic process and the supposed nerve fiber, thereby suggesting that the latter was more likely to be a col- lateral branch of the odontoblastic process than a nerve fiber.

THEORIES OF DENTIN SENSITIVITY Dentin is one of the most sensitive tissues, sug-

gesting a rich innervation. However, no nerve fibers have yet been unequivocally demonstrated in middle and outer dentin. Therefore the pathways of activation of sensory nerve fibers located in inner dentin or pulpal periphery have been the subject of debate for sev- eral decades, which has lead to the evolution of three theories.

The conduction theory proposes that the nerve endings in dentinal tubules are directly activated by external stimuli. This view rests on the still unsub- stantiated assumption that the nerve fibers extend to the dentinoenamel/cementum junction. The theory is further eroded by the clinical observation that application of local anesthetics to cut and exposed dentin does not block the pain sensation 31 and chemical stimuli by pain-inducing agents has not been found to cause pain. 32

The transduction theory postulates that the odontoblastic processes mediate external stimuli to the nerve endings located in the peripheral pulp. How- ever, synaptic contacts between odontoblastic processes and axons have not been demonstrated. On the basis of early electron microscopic observations, Frank 33 suggested the existence of junctional com- plexes between the odontoblastic processes and the nerve fibers; Byers 17 and Holland 34 concluded that no synapses or tight or gap junctions exist between them.


Fig. 3. Nerve fibers (NF) in mineralized dentin (A) and in outer predentin (B) with magnifications in left and right insets respectively. (OB, ododotoblasts; NU, nucleus; OP, odontoblastic process; MD, mineralized dentin; PD, predentin.) (Original magnification x5960; B, 8'850; insets: in A, x14,900; in B, x12,800.) (From Nair, Schweiz Mschr Zahnmed 1993, 103:965-72. Reprinted with permission.)


The hydrodynamic theory 35' 36 suggests that nerve impulses are initiated by fluid movement within the dentinal tubules as a consequence of external stimuli. Dentinal tubules contain tissue fluid diffusing from the pulp that under normal physiologic conditions flows slowly outward. 37, 38 If this fluid moves rapidly through the dentinal tubules, it is assumed to activate the free nerve endings located in the inner dentin and around the odontoblasts. Fresh overwhelming evidence continues to emerge in support of the hydrodynamic mechanism. 39 It only remains to be demonstrated in vivo that intratubular fluid movement occurs in response to the application of various nociceptive stimuli to confirm the hydrodynamic theory as a physiologic fact.

QUANTITATIVE STUDIES Quantitative studies on various classes of intraden-

tal nerve fibers are scarce. The available data relate mostly to rodent, 4~ feline, 41-43 canine, 44' 45 bovine,44 and simian 46 teeth. Similar data on human intradental nerve fibers are extremely rare. 47-50

Number of myelinated axons There are five studies in which myelinated axons

of human teeth have been quantified and that provide data on human permanent anterior teeth. Similar data are still unavailable on human molars. The pioneer- ing light microscopic work of Graf and Bj6rlin 47 was on limited numbers of incisors, canines, and premolars. They reported 991 (n = 1) myelinated axons at the apex of a left maxillary central incisor, 536 • 245 (n = 4) for maxillary lateral incisors, 600 • 447 (n = 4) for maxillary canines, and 581 • 503 (n = 3) for assorted premolars. Johnsen and Johns 48 reported 359 ___ 46 (n = 7) for assorted permanent incisors and 361 _+ 82 (n = 13) for unspecified permanent canines. Reader and Foreman 49 found an average of 256 myelinated axons in four young premolars.

Johnsen et al. 5~ studied 49 human mandibular first premolars from subjects ranging from 11 to 71 years of age. They divided their subjects into younger (<15 years) and elder (15 years or older) groups. The youngersubjectshadanaverageof305 • 125 (n = 25) apical myelinated axons compared with 500 • 153 (n = 24) for the elder group. This would imply that about 40% of the myelinated axons found in adult human mandibular premolars grow into the teeth after the subjects have attained 15 years of age. But there is only very low positive correlation 5a between the number of apical myelinated axons and the age of the subject concerned. Nerves are believed to grow into permanent human teeth between the ages of 10 to 15 years. It is widely known that the root canal in general and the apical third in particular gets much

Table II. Number (2• s) of intraradicular nerve fibers at the juxta-apical level of human premolars

Myelinated* Nonmyelinated~" Tooth type 2 +- s (n) 2 +- s (n)

Maxil lary 4 340 +- 186 (20) 2684 +_ 980 (6) Maxil lary 5 244 _+ 68 (3)

Mandibular 4 280 +- 129 (22) 1569 --- 600 (5) Mandibular 5 317 --- 153 (22) 1609 +-+- 1023 (5)

Overall 312 -+ 149 (67) 2000 -+ 1023 (16)

*Data summarized from Nair et al. (1992). 51 tData summarized from Nair and Schroeder (1995). 5z (n) the number of teeth involved.

narrower after 15 years of age. If the radicular pulpal specimens are gained by cracking the teeth and dis- secting the soft tissue as was done in the study, there is every likelihood that such specimens from older teeth could be unintentionally retrieved more coronally. This is where the canals are usually wider and easier to dissect but carry a significantly higher number of nerve fibers because of intraradicular branching of axons. 51

Taking those sampling aspects into consideration it was attempted 51 to obtain statistically reliable tooth-specific and site-specific data on the number of intraradicular myelinated axons of human premolars. From a total of 67 healthy adolescent premolars, the myelinated axons (Fig. 1) were counted from three standardized horizontal radicular levels, namely the juxta-apical, midroot, and subcervical levels. The 67 teeth had an average of 312 _+ 149 myelinated nerve fibers at the juxta-apical level (Ta- ble II) within a range of 18 to 728 axons. The contralateral and ipsilateral differences in means among the four groups of premolars were not significant (!7 < 0.05).

Number of nonmyelinated axons There are four quantitative studies on nonmyeli-

hated nerve fibers of human teeth. 47, 49, 50, 52 The early work of Graf and Bj6rlin 47 used a light microscope that cannot adequately resolve the majority of nonmyelinated axons. Therefore it is not surprising that they found fewer nonmyelinated nerve fibers than myelinated axons. Reader and Foreman 49 used electron microscopy and found an average of 670 nonmyelinated axons in each of four premolars of an adolescent. Johnsen et al. 5~ reported an average of 1478 ___ 626 nonmyelinated axons in subjects below 15 yearsof age and 1830 • 1020 in subjects above 15 years with no statistically significant difference. Most recently Nair and Schroeder 52 determined the number of nonmyelinated axons by counting fibers that could be located and reconstructed by standardized com-

% 2 0 0

1 8 0 o Maxillary 4 / �9 Mandi.bular 4 / %

1 6 0 o')

(D t - o t -

1 4 0 >

n "

120

1 0 0


i . . . . . . I I

JA MR SC Fig. 4. Relative increase in number of myelinated axons at midroot and subcervical levels to those at juxta-apical level of human premolars. Number of myelinated axons increase substantially during intraradicular passage. (From Nair et al. Anat Embryol 1992. 186:563-71. Reprinted with permission.)

posite electron micrographs from the juxta-apical level of healthy human premolars (Table II). The 16 teeth investigated had an average of 2000 _ 1023 nonmyelinated axons (range, 534 to 3912). On the basis of statistically larger studies, 5~ 52 it is reason- able to conclude that human premolar receive about 2000 nonmyelinated axons at the tooth apex.

Intraradicular arborization of axons Very little is known about intraradicular branching

of tooth axons. It is generally assumed that the axons pass coronally and undergo little branching in the root canal. 53 The principle site of arborization of tooth axons is believed to be the crown. 17 However, recent studies28, 29 show that radicular dentin is more densely innervated than was previously believed (Fig. 3). It has recently been shown 51 that the myelinated axons branch profusely during intraradicular passage (Fig. 4). Similar data on nonmyelinated axons are unavailable.

Fiber-size It is now generally accepted that the great majority

(>93% 51) of apical myelinated axons of human teethS0, 51 are AS fibers that show a unimodel distribution in fiber sizes. Only a minor fraction (<7% 51) of the axons are in the A[3 range but do not form a

distinct group. These larger axons represent an extended tail of a slightly left-skewed AS distribution (Fig. 5, A). The nonmyelinated C fibers are much smaller and have an overall average diameter of 0.5 ~tm. 52 However, the frequency distribution of the fiber sizes reveal a distinctly left-skewed curve peak- ing around 0.25 ~tm and an overextended tail stretch- ing beyond 2 tam (Fig. 5, B).

Sympathetic innervation Intradental nonmyelinated axons are a mixture of

sensory and autonomous sympathetic fibers. His- tochemical studies 54-56 have established the presence of sympathetic innervation around pulpal blood vessels in mammalian teeth. However, quantitative data on the relative proportion of these two classes of nonmyelinated fibers are still unavailable. Some limited deductions can be drawn from the unilateral sympathectomy on cat canine teeth. 4e It was estimated that 5% to 13% of all nonmyelinated axons of feline mandibular canine teeth are sympathetic fibers.

FUNCTIONAL SIGNIFICANCE AND CLINICAL RELEVANCE

Recently Figdor 31 reviewed the neurophysiologic advances of tooth sensitivity and their relevance to clinical dentistry. Only 13% of the nerve fibers that


enter human premolars are myelinated (Table II); 93% are AS-fibers and the remaining 7% are Al3-fibers. 51 Although Al3-fibers reportedly have a propri- oceptive character, 57 they are considered to be func- tionally similar to AS-fibers. 58 Therefore all myelinated axons entering human teeth are considered as sensory afferents with their receptive field located at the pulp/dentin interface and the inner dentin. The free endings of these nerve fibers located around the odontoblastic body and the inner dentin are probably activated by the hydrodynamic mechanism 35, 36 in which the sudden movements of fluid within dentinal tubules arising out of thermal, traumatic, and osmotic stimuli cause an initial, short latent, well-localized, and sharp pain. Such activation occurs during thera- peutic interventions such as drilling and air-blasting of dentin or consumption of sweet and sour foods by patients with open dentinal tubules.

About 87% of all axons that enter human premolars are nonmyelinated C fibers. 52 The great majority of them are believed to be sensory afferents. How- ever, they are slow conductors with the receptive field located in the pulp. These axons are activated by in- flammatory mediators, prolonged application of heat, and other noxious injuries to the pulpal tissue. Such stimuli arising out of the pulp are clinically difficult to localize and are perceived as a slow, dull, and long-lasting toothache. The nonmyelinated fibers are also known to be very much resistant to tissue anox- ia58, 59 that enables them to conduct nociceptive impulses even when the pulp tissue is damaged and the myelinated axons are out of commision as a result of anoxic conditions. The ability of these nerve fibers to survive and function under such conditions would explain the clinical enigma of teeth that do not respond to cold carbon dioxide testing (-79~ but evince undeniable pain to endodontic instrumenta- tion. 31

Regulatory role. Tooth axons arborize extensively in the coronal pulp. 6~ The inner dentinal wall of human tooth/crown has an estimated density of 50,000 to 80,000 tubules per mm2. 61 The dentin is innervated with the highest density believed to be around pulpal horns where nearly 50% of the tubules contain neural elements. 18 This implies that the finite number of myelinated axons entering the human tooth apex 5~ 51 probably arborize into a large number of thin nerve fibers at the pulpodentinal junction in the crown.

Defense against injury has both biologic and evo- lutionary importance. However "vas t numbers of (nerve) fibers are not required for detecting injury, as evidenced by the effectiveness of small numbers of testicular afferents in signaling pain. ''62 Therefore nociceptive functional demands alone are unlikely to

Frequency (%)

60

40

20

0 I i I

2 4 6 8 D iameter of nerve fibers (IJm)

Frequency (%)

18-

f i Maxillary 4 15- f \~ . . . . Mandibular4

r '~t 12- ' ~ ......... Mandibular5

: l

6-9- ~ . . . 7 Overall

i I i I I

o o.s 1 1.5 2 2.s Diameter of nerve fibers (pm)

Fig. 5. Frequency distribution curves of diameter spectra of myelinated axons (axon + myelin sheath) at the juxta- apical level of seven second mandibular human premolars (finer lines). Two similar curves in broken lines represent contralateral teeth from the same subject. Curve drawn in thick line represents all individuals. (From Nair et al. Anat Embryol 1992.186:563-71. Reprinted with permission.) B, Diameter spectra of nonmyelinated axons at juxta-apical level of three human premolars. Thick line curve represents all individuals. Left skewed distribution shows more than 68% of all axons falling below 0.5 lam (From Nair and Schroeder. Anat Embryol 1995;192:35-41. Reprinted with permission.)

explain the presence of the vast number of tooth afferents. Stimulation of sensory endings not only results in orthodromic passage of impulses toward the central nervous system but also evokes antidromic volleys of action potentials along the peripheral branches (axon reflex63), leading to the release of bi- ologically active neuropeptides. 64, 65 Such intradental


p e p t i d e r g i c n e r v e f ibe r s are s h o w n to r egu l a t e m i c r o -

c i r cu la t ion , 66 m e d i a t e i n f l a m m a t i o n , 67 a n d are c l o s e l y

a s s o c i a t e d w i t h a reas o f tertiarY den t i n f o r m a t i o n . 68

T h e r e f o r e in add i t i on to the vi ta l ro le o f n o c i c e p t i v e

a l a r m s igna l ing , the s e n s o r y a x o n s o f m a m m a l i a n

t ee th m a y a lso be i n v o l v e d in the r e g u l a t i o n o f p h y s -

i o log i c m a i n t e n a n c e and r epa i r o f pu lpa l and den t i n a l

t i s sues . 69

In c o n c l u s i o n , m u c h o f the r e c e n t a d v a n c e s in the

n e u r o a n a t o m y a n d p h y s i o l o g y o f t o o t h i n n e r v a t i o n

h a v e b e e n b e n e f i c i a l to pa t i en t ca re as t h e y e n h a n c e

the c l i n i c i a n ' s abi l i ty to d i a g n o s e and t rea t t oo th p a i n

in a r a t iona l way . N e v e r t h e l e s s , it still r e m a i n s to be

e x p l a i n e d w h y the h u m a n t o o t h is e q u i p p e d w i t h s u c h

a vas t n u m b e r o f s e n s o r y n e r v e f ibers .

I am indebted to Mrs. Esther Keller for excellent tech- nical assistance and to Dr. David Figdor, Melbourne, Aus- tralia, and Dr. Patrick Sequeira, Chain, Switzerland for critical reading of this manuscript.

REFERENCES

I. Singer C. A short history of anatomy and physiology from the Greeks to Harvey. 1st ed. New York: Dover, 1957:52-8.

2. Madeira M, Percinoto C, Silva M. Clinical significance of supplemental innervation of the lower incisor teeth: a dissec- tion study of the myelohyoid nerve. ORAL SURG ORAL MED ORAL PATHOL 1978;46:608-14.

3. Frommer J, Mele FA, Monroe CW. The possible role of the mylohoid nerve in mandibular posterior teeth sensation. J Am Dent Assoc 1972;85:113-7.

4. Carter RB, Keen EN. The intramandibular course of the inferior alveolar nerve. J Anat 1971;108:433-9.

5. Sutton RN. The practical significance of mandibular acces- sory foramina. Aust Dent J 1974;19:167-73.

6. Rood JP. The analgesia and innervation of mandibular teeth. Br Dent J 1976;140:237-8.

7. Anderson KV, Pearl GS. Transmedian innervation of canine tooth pulp in cat. Exp Neurobiol 1974;44:281-8.

8. Erlanger J, Gasser HS. Electrical signs of nervous activity. Philadelphia: University Press, 1937.

9. Morell P, Norton WT. Myelin. Sci Am 1980;242:74-89. 10. Lillie KS. Factors affecting the transmission and recovery in

the passive iron wire model. J Gen Physiol 1925;7:463-507. 11. Hursh JB. The conduction velocity and diameter of nerve fi-

bres. Am J Physiol 1939;127:131-9. 12. Hunter J. The natural history of the teeth of humans. 1st ed.

Dordracis: A. Bluss6 & Sons, 1773. 13. Pishinger A, Stockinger L. Die Nerven der menschlichen

Zahnpulpa. Z Zellforsch Mikrosk Anat 1968;89:44-61. 14. Arwill T. The innervation of the teeth: a study by the light and

electron microscopy. Ume~t, Sweden: University of Umeft; 1958. Thesis.

15. Raschkow I. Meletemata circa mammalium dentium evolu- tionem. Vratislaviae, Slovakia: University of Vratislaviae; 1835. Dissertation.

16. Fearnhead RW. Histological evidence for the innervation of human dentine. J Anat 1957;91:267-77.

17. ByersMR. Dental sensory receptors. IntRevNeurobiol 1984; 25:39-94.

18. Byers MR, Dong WK. Autoradiographic location of sensory nerve endings in dentin of monkey teeth. Anat Rec 1983; 205:441-54.

19. Byers MR, Kish SJ. Delineation of somatic nerve endings in

rat teeth by autoradiography by axon-transported protein. J Dent Res 1976;55:419-25.

20. Byers MR, Mathews B. Autoradiographic demonstration of ipsilateral and contralateral sensory nerve endings in cat dentin, pulp, and periodontium. Anat Rec 1981 ;201:249-60.

21. Holland GR. The incidence of dentinal tubules containing more than one process in the cuspal dentine of cat canine teeth. Anat Rec 1981;200:437-42.

22. Arwill T, Edwall L, Lilja J, Olgart L, Sevensson S-E. Ultra- structure of nerves in the dentinal-pulp border zone after sensory and autonomic nerve transection in the cat. Acta Odont Scand 1973;31:273-81.

23. Corpron RE, Avery JK. The ultrastructure of intradental nerves in developing mouse molars. Anat Rec 1973;175:585- 606.

24. Arwill T. Studies on the ultrastructure of dental tissues: II, the predentine-pulpal border zone. Odont Rev 1967;18:191- 208.

25. Byers MR, Neuhaus S J, Gehrig JD. Dental sensory receptor structure in human teeth. Pain 1982;13:221-35.

26. Frank RM. Etude an microscope Iectroniqaue de l'odon- toblaste et du canalicule dentinaire human. Arch Oral Biol 1966;11:179-9.

27. Lilja J, Fagerberg-Mohlin B. Dentinal innervation of im- pacted human third molars. Scand J Dent Res 1984;92:485-8.

28. Nair PNR. Innervation of root dentine in human premolars. Schweiz Monatsschr Zahnmed 1993;103:965-72.

29. Maeda T, Honma S, Takano Y. Dense innervation of human radicular dental pulp as revealed by immunocytochemistry for protein gene-product 9.5. Arch Oral Biol 1994;39:563-8.

30. Fleche La RG, Frank RM, Steuer P. The extent of human od- ontoblast process as determined by transmission electron microscopy: the hypothesis of a retractable suspensor system. J Biol Buccale 1985;13:293-305.

31. Figdor D. Pain of dentinal and pulpal origin. Ann Roy Aust Coil Dent Surg 1994;12:131-42.

32. Br~innstrrm M. The elicitation of pain in human dentine and dental pulp by chemical stimuli. Arch Oral Biol 1962;7:59- 62.

33. Frank RM. Attachment sites between the odontoblasts, its process and the nerve. Arch Oral Biol 1968;13:833-4.

34. Holland RG. Odontoblasts and nerves: just friends. Proc Finn Dent Soc 1986;82:179-89;

35. Gysi A. An attempt to explain the sensitiveness of dentine. Br J Dent Sci 1900;43:865-8.

36. Brfinnstrrm M. Sensitivity of dentine. ORAL SLIRG ORAL MED ORAL PATHOL 1966;21:517-26.

37. Linden L, Br~instrrm M. Fluid movements in dentine and pulp: an in vivo study of flow produced by chemical solution on exposed dentine. Odont Rev 1967;18:227-36.

38. Pashley DH, Nelson R, Pashley EL. In vivo fluid movement across dentine in the dog. Arch Oral Biol 1981;26:707- 10.

39. Ahlquist M, Franzrn O, Coffey J, Pashley D. Dental pain evoked by hydrodynamic pressures applied to exposed dentin in man: a test of the hydrodynamic theory of dentin sensitivity. J Endodon 1994;20:130-4.

40. Naftel JP, Beruanke JM, Qian X-B. Quantitative study of the apical nerve fibers of adult and juvenile rat molars. Anat Rec 1994;238:507-16.

41. Holland GR, Robinson PP. The number and size of the axons at the apex of the cat's canine tooth. Anat Rec l 983;205:215- 22 .

42. Noga BR, Holland GR. Sympathetic innervation at the apex of the cat's canine tooth: a quantitative study. Anat Anz 1983; 153:137-48.

43. Hoffmeister B, Schendel K. Analyse markhaltiger und mark- loser Axone des Unterkiefers der Katze. Dtsch Zahn 1986;41:863-7.

44. Graf W, Hjlmquist U. Caliber spectra of dental nerves in dogs and cattle. J Comp Neurol 1955;103:345-53.

45. Hirvonen TJ. A quantitative electron microscopic analysis of


the axons at the apex of the canine tooth pulp in the dog. Acta Anat (Base 1) 1987;128:134-9.

46. Beul tmann KW, Karlsson, Edie J. Quantitative ultrastructure of intradental nerve fibers in marmosets. Arch Oral Biol 1972;17:645-60.

47. Graf W, Bj6rlin G. Diameters of nerve fibers in human tooth pulp~ J A m Dent Assoc 1951;43:186-93.

48. Johnsen D, Johns S. Quantitation of the nerve fibers in the primary and permanent canine and incisor teeth in man. Arch Oral Biol 1978;23:825-9.

49. Reader AI, Foreman DW. An ultrastructural quantitative in- vestigation of human intradental innervation. J Endodon 1981;7:493-9.

50. Johnsen DC, Harshbarger J, Rymer HD. Quantitative assess- ment of neural development in human premolars. Anat Rec 1983;205:421-9.

51. Nair PNR, Luder HU, Schroeder HE. The number and size- spectra of myelinated nerves in human premolars. Anat Em- bryol 1992;92:123-8.

52. Nair PNR, Schroeder HE: Number and size-spectra of nonmyelinated axons of human premolars. Anat Embryol (Berl) 1995;192:35-41.

53. Engstr6m H, Ohman A. Studies on the innervation of human teeth. J Dent Res 1960;39:799-809.

54. Kukletova M, Zahradka J, Lukas Z. Monamineric and cholinergic nerve fibres in the human dental pulp. Histoche- mie 1968;16:154-8.

55. Pohto P, Antilia R. Innervation of blood vessels in the dental pulp. Int Dent J 1972;22:228-39.

56. Pohto P. Sympathetic adrenergic innervation of permanent teeth in the monkey (Macaca irus). Acta Odont Scand 1972; 30:117-26.

57. Dong WK, Chudler EM, Martin RF. Physiological properties ofintradental mechanoreceptors. Brain Res 1985;334:389-95.

58. Narhi MVO, Iyv~isjarvi E, Virtanen A, Huopaniemi I, Nagas- sapa D. The role of intradental A- and C-type nerve fibers in dental pain mechanism. Proc Finn Dent Soc 1992;88(suppl 1):507-16.

59. N~irhi MVO. The characteristics of intradental sensory units and their responses to stimulation. J Dent Res 1985;64:564-71.

60. Byers MR. Trigeminal arborization of individual sensory axons in dental pulp of rat molars. Brain Res 1985;345: 181-5.

61. Schellenberg U, Krey G, Boshardt D, Nair PNR. Numerical density of dentinal tubules at the pulpal wall of permanent human premolars and third molars. J Endodon 1992; 18:104-9.

62. Kruger L. Morphological features of thin sensory afferent fi- brest a new interpretation of nociceptor function. Prog Brain Res 1988;74:253-7.

63. Langley JN. Antidromic action. J Physiol 1923;57:428-46. 64. Raab WHM. Temperature related changes in pulpal micro-

circulation. Proc Finn Dent Soc 1992;88(suppl I):469-79. 65. Kerezoudis NP, Olgart LM, Edwall L. Evans blue extravasa-

tion in rat dental pulp and oral t issues induced by electrical stimulation of the inferior alveolar nerve. Arch Oral Biol 1993;38:893-901.

66. Gazelius B, Edwall B, Olgart LM, Lundberg JM, Hokfelt T, Fisher JA. Vasodialatory effects and coexistence of calcitonin gene-related peptide (CGRP) and substance P in sensory nerves of cat dental pulp. Acta Physiol Scand 1987;130:33- 40.

67. Olgart LM. Function of peptidergic nerves. In: Inoki R, Kudo T, Olgart LM, eds. Dynamic aspects of dental pulp. London: Chapman & Hall, 1990:349-62.

68. Taylor PE, Byers MR. An immunohis tochemical study of the response of nerves containing calcitonin gene-related peptide to microabscess formation and healing in rat molars. Arch Oral Biol 1990;35:629-38.

69. Silverman JD, Kruger L. An interpretation of dental innervation based upon the pattern of calcitonin gene-related peptide immunoreact ive thin sensory axons. Somatosens Res 1987; 5:157-75.

Reprint requests: Dr. P.N.R. Nair Institute of Oral structural Biology Centre for Dental and Oral Medicine University of Zurich Plattenstrasse 11 CH-8028 Zurich Switzerland

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