- Email: [email protected]
Organization and vasculature of human periodontal ligament mechanoreceptors
Arch
oral Bid.
Vol. 17, pp. 913-921, 1972. Pergmon
Press.
Printed inGreat Britain.
ORGANIZATION AND VASCULATURE OF HUMAN PERIODONTAL LIGAMENT MECHANORECEPTORS C.
J. GRIFFINand HELENSPAIN
Histology Department,
The University of Sydney, Australia
Summary-Periodontal nerve plexuses were studied with the light and electron-microscope. A Type I mechanoreceptor containing a single myelinated nerve fibre and unmyelinated nerve fibres and a Type II mechanoreceptor consisting of myelinated nerve fibres and unmyelinated end-rings were identified in human periodontal ligament. Each receptor had a primary and secondary capsule. Capsular cells formed a reticulum between these capsules. Encapsulated terminal arterioles, metarterioles and capillaries vascularized the neural complex. Type I receptor appeared to receive its blood supply by diffusion whereas Type II receptor had a direct blood supply. A metarteriole pierced the capsule of a Type II receptor and might be responsible for spontaneous discharges synchronous with the electrocardiogram. INTRODUCTION ENCAPSULATED periodontal
mechanoreceptors have been described by GRIFFINand SPAIN(1972) and by GRIFFIN (1972). One type consisted of an oval encapsulated nerve ending, which was derived from a single myelinated nerve fibre; the other type consisted of unmyelinated nerve fibres surrounding myelinated nerve fibres. The first type appeared to correspond to the end-knob nerve ending described by LEWINSKYand STEWART(1937) in human periodontium and the second type of nerve ending resembled the end-rings described by VAN DER SPRENKEL(1936) in the periodontal membrane of young mice. The purpose of this paper is to describe the vasculature of these end-organs and their relationship. MATERIAL
AND
METHOD
These have been described previously (GRIFFIN, 1972). Briefly, pieces of periodontium were scraped from eleven freshly extracted human teeth and were fixed with osmium tetroxide in phosphate buffer pH 7-4. They were dehydrated in acetone and embedded in Araldite. Thick sections were stained with toluidine blue and examined with the light microscope for periodontal nerve plexuses and encapsulated end-organs. These end-organs when identified were then cut in serial ultrathin sections at 4 pm intervals. The ultrathin sections were cut with an LBK ultramicrotome and stained on the grid with uranyl acetate for 1 hr. Electron micrographs and observations were made on an Hitachi HS 7 electron microscope. RESULTS
Light microscopy
Two types of encapsulated end-organs were identified in human periodontal ligament (Figs. 1-5) and have been termed Type I and Type II receptors. 913 A.O.B. 17/6--A
914
C. J. GRIFFIN AND HELEN SPAIN
Type I receptor. Type I end-organ consisted of a single myelinated nerve fibre and unmyelinated nerve fibres surrounded by the cell bodies and processes of capsular cells (Figs. 14). The myelinated nerve fibres of these receptors had diameters between 3 and 1.5 pm whilst the widest diameters of the end-organ, including its capsule, were between 7 and 12 pm. When followed in serial sections (Figs. 14) the myelinated nerve fibres of these receptors lost their myelin sheaths. The end-organ then consisted of unmyelinated nerve fibres surrounded by a capsule. Type II receptor. Type II end-organs consisted of two or more myelinated nerve fibres, unmyelinated nerve fibres and the cell bodies and processes of capsular cells (Figs. 1, 2 and 5). The myelinated nerve fibres had diameters between 2 and 3 pm and the widest diameters of these encapsulated complexes were between I5 and 20 pm. The unmyelinated nerve fibres of these end-organs encircled the myelinated nerve fibres. These endings, when followed in serial sections, were seen to be derived from a single myelinated nerve fibre which divided into two or more terminal encapsulated nerve fibres (Fig. 5). Periodontal neroe trunk. The main nerve trunk of the periodontal nerve plexus consisted of twenty or more myelinated nerve fibres and unmyelinated nerve fibres. In the serial sections, myelinated nerve fibres were seen to leave this complex and pass into the surrounding periodontal tissue to terminate as either Type I or the Type II end-organs (Fig. 5). Capsuhr complexes. Type I and Type II end-organs were surrounded by a primary capsule consisting of the cell bodies and processes of capsular cells. However, in certain cases, Type I and Type II receptors were enclosed in a secondary capsule (Figs. 1 and 2). This secondary capsule seemed to be continuous with the surrounding dense periodontal connective tissue. Cell bodies and processes of the primary and secondary capsules appeared to form a reticulum in which both Type I and Type II end-organs were enclosed. The primary capsules of the Type I end-organ were usually separated from the secondary capsule by a considerable amount of tissue or lymph space (Figs. 1 and 2). On the other hand, the primary capsules of theType II receptor were intimately related to the secondary capsule (Figs. 1 and 2). Vasculature. Blood vessels of the arteriolar type were intimately associated with the secondary capsules of Type I and Type II receptors (Figs. 1 and 2). A blood vessel of the arteriolar type was also intimately related to the primary capsule of Type II receptor (Fig. 5). Veins, presumably collecting veins, formed arcades surrounding Type I and Type II end-organs (Figs. 1 and 5). Electron microscopy Type I receptor. The Type 1 receptor consisted of a single myelinated nerve and unmyelinated nerve fibres surrounded by the cell processes of the capsular cells (Fig. 6). A septum, consisting of the cytoplasmic process of a capsular cell, partially separated the myelinated nerve fibre from the unmyelinated elements. The unmyelinated nerve fibres divided into minute terminal branches. What appeared to be the distal part of a Type I receptor was also seen (Fig. 6). This complex was also divided into several segments by the nucleus and cell processes of capsular cells.
ORGANIZATION
AND
VASCULARIZATION
OF PERIODONTAL
RECEPTORS
915
Large unmyelinated nerve fibres and unmyelinated nerve fibres, dividing into minute terminal branches, comprised the distal portion of the end-organ. The myelinated nerve fibres were approximately 2 *5 pm in diameter, whereas the largest unmyelinated nerve fibres were approximately 1.1 pm. The minute terminal axons had diameters between 0 - 3 and 0 * 15 pm. No blood vessels were seen intracapsularly. Type ZZreceptor. The Type II receptor contained blood vessels of the capillary type (Fig. 7). Capsular cell processes and exposed nerve endings were in close proximity to the blood vessel. A blood vessel of the metarteriolar type was also seen to enter the capsule of a Type II receptor (Fig. 8). The tunica media of this blood vessel consisted of an interrupted layer of smooth muscle cells. On one side of the metarteriole was the dense fibrous tissue of the periodontal ligament whilst on the other side were enclosed nerve endings of the receptor (lacuna endings). Terminal arteriole. The afferent arteriole observed with the light microscope was seen to be an encapsulated blood vessel with a single layer of smooth muscle cells. These smooth muscle cells appeared to effect tight junctions with endothelial cells (Figs. 9 and 10). According to RHODIN(1967), these vessels correspond to terminal arterioles.
DISCUSSION Two types of receptors constructed on a common organizational theme may be identified in human periodontal ligament. The Type I receptor appears to be a discrete unit, the fine structure of which has been described by GRIFFINand SPAIN(1972). It appears to correspond to the end-knobs described by LEWINSKYand STEWART(1937). Usually this receptor is surrounded by a considerable amount of tissue space (Figs. 1 and 2) and, because of this, might slip out of the way of a stimulating force. It is therefor considered that this receptor might be a rapidly adapting unit. Type II receptor is somewhat more complex. It is derived from a single myelinated nerve fibre which divides into two or more terminal encapsulated myelinated nerve fibres (GRIFFIN, 1972). The primary capsule of this end-organ was more intimately related to the secondary capsule than that of the Type I receptor and on this basis it might be a slowly adapting unit. On the other hand, there was an appreciable amount of tissue space between the neural elements of the end-organ (Figs. 1, 2 and 5). The myelinated nerve fibres of the ending appeared to lose their myelin sheaths in a staggered fashion and to terminate as unmyelinated nerve fibres encircling adjacent myelinated nerve fibres (Figs. 1 and 2). This arrangement might indicate that, if the parent fibre was displaced along its course, the end-organ might discharge. The periodontal nerve plexuses appear to receive their blood supply from blood vessels of the terminal arteriolar type (Figs. 1, 2 and 9). On entering the plexus, the afferent terminal arteriole appears to be encapsulated by cell processes of capsular cells (Fig. 9). A feature of this bloodvessel is the presence of myo-endothelial junctions (Figs. 9 and 10). RHODIN (1967) found numerous myo-endothelial junctions in the terminal arterioles of the fascia of the rabbit medial thigh muscles. He considered that, although these junctions might serve to stabilize the microvascular wall, they were
916
C.
J. GRIFFIN AND
HELEN SPAIN
more probably pathways for the exchange of metabolites, more specifically bloodborne transmitter substances. In the present study, we have not been able to demonstrate the innervation of terminal arterioles and metarterioles. However, there is general agreement that the smooth muscle cells of arteries and arterioles receive both an afferent and efferent innervation (RHODIN, 1967; GRIGOR EVA, 1962; FULTONand LUTZ, 1942; FALCK, 1962). RHODIN (1967) showed that nerve axons follow closely the adventitial aspect of the media of arterioles, terminal arterioles and precapillary sphincters of the rabbit medial thigh muscle and demonstrated nerve endings within smooth muscle cells of terminal arterioles which contained granulated vesicles. He considered that there was a more intimate nervous control of terminal arterioles than is the case with larger arterioles. NICOLL (1964) observed rhythmical active vasomotion of the terminal arterioles of the bat’s wing which appeared to be independent of nervous control because this activity was not significantly affected when the nerve to the area was stimulated. However, what appears to be significant in the present study is that metarterioles enter the capsule of the Type II receptor (Fig. 5). Their proximity to lacuna endings (Fig. 8) suggests that these vessels could be responsible for spontaneous discharges. In the periodontium of the dog, HANNAM(1969b) recorded spontaneous discharges synchronous with the electrocardiogram. On the light and electron microscopic evidence, it would appear that the Type II periodontal ligament receptors have a direct blood supply (Figs. 5 and 8) and that endoneural capillary blood vessels pass between the neural elements. On the other hand the Type I receptor probably receives its nutrition by diffusion of substances from surrounding capillary vessels. R&urn&-Les plexus des nerfs parodontaux sont Ctudits en microscopic optique et Clectronique. Un type 1 de r&epteurs mkaniques contenant une seule fibre nerveuse myeliniste et des fibres non myclinis&s et un type II comportant des fibres nerveuses my~linis&s et des noeuds terminaux non my&linisCs ont pu &tre identifib dans le ligament. Chaque rt5cepteur a une capsule primaire et secondaire. Des cellules capsulaires forment un reticulum entre ces capsules. Des artCrioles terminals encapsul&s, des mCtartCrioles et des capillaires vascularisent le complexe neural. Le r&epteur de type I semble recevoir sa vascularisation par diffusion, alors que le type 11 est directement vascularis Une m&arteriole perce la capsule du rkepteur de type II et peut &tre responsable des d&charges spontan&.s synchrones des tlectrocardiogrammes.
Zusammenfassung-Lichtund elektronenmikroskopisch wurde der parodontale Nervenplexus untersucht. Ein Mechanorezeptor vom Typ I mit einer einzelnen markhaltigen Nervenfaser und mit marklosen Nervenfasern sowie ein Mechanorezeptor vom Typ II, aus markhaltigen Nervenfasern und marklosen Endringen bestehend, wurden im menschlichen Desmodont identitiziert. Jeder Rezeptor besaD eine primtire und eine sekundlre Kapsel. Die Kapselzellen bildeten zwischen den Kapseln ein Retikulum. Eingekapselte Endarteriolen, Metarteriolen und Kapillaren vaskularisierten den neuralen Komplex. Der Rezeptor vom Typ I schien seine Blutversorgung auf dem Wege der Diffusion zu erhalten, wlhrend der Rezeptor vom Typ II direkt mit Blut versorgt wurde. Eine Metarteriole durchdrang die Kapsel des Typ II-Rezeptors und diirfte fiir die synchron mit dem Elektrokariogramm erfolgenden spontanen Entladungen verantwortlich sein.
ORGANIZATION AND VASCULARIZATIONOF PERIODONTALRECEPl-ORS
917
REFERENCES FALCK, B. 1962. Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta physiol. &and. 56, Suppl. 197. FULTON, G. P. and LUTZ, B. R. 1942. Smooth muscle motor units in small blood vessels. Am. J.
Physiol. 135, 531-534. GRIFFIN, C. J. 1972. The fine structure
of end-rings in human periodontal
ligament.
Archs oral Biol.
17, 785-797. GRIFFIN, C. J. and SPAIN, H. 1972. The fine structure of periodontal nerve plexuses in man. In: The MaxiNo-Mandibular Apparatus. Proc. Internat. Anat. Congr. Leningrad 1970. In press. HANNAM, A. G. 1969b. Spontaneous activity in dental mechanosensitive units in the dog. Archs oral
Biol. 14, 793-801. LEWINSKY, W. and STEWART, D. 1937. The innervation
of the periodontal
membrane.
J. Anat. 71,
98-102. GRIGOR’ EVA, T. A. 1962. The Innervation of Blood Vessels, p. 1.53. Pergamon Press, Oxford. NICOLL, P. A. Autoregulation of Blood Flow, p. 245. Am. Heart Ass., Monograph 8, New York. RHODIN, J. 1967. The ultrastructure of mammalian arterioles and precapillary sphincters. J. ultrastruct. Res. 18, 181-223.
PLATES l-4
OVERLEAP
C.
918
J. GIUFF~NAND
HELEN SPAIN
PLATE 1 FIG. 1. Photomicrograph of portion of a periodontal nerve plexus. Arteriolar type blood vessel, bv.; collecting vein, cv.; Type I mechanoreceptors, 1; Type II mechanoreceptors, 2; primary capsule, pc.; secondary capsule, SC.; end-ring, r. Toluidine blue. x 1800 FIG. 2. Photomicrograph of portion of a periodontal nerve plexus 4 pm from Fig. 1. Arteriolar type blood vessel, bv. ; Type I mechanoreceptors, 1; Type II mechanoreceptors, 2; secondary capsule, SC.; tissue space between primary and secondary capsules of Type I receptors Sl ; tissue space between Type II mechanoreceptors and secondary capsule, S2. Toluidine blue. x 1800 FIG. 3. Photomicrograph mechanoreceptors.
of portion of a periodontal nerve plexus showing Type I Type I mechanoreceptors, 1. Toluidine blue. x 1800
FIG. 4. Photomicrograph of portion of a periodontal nerve plexus 4 pm from Fig. 3. Type I mechanoreceptors, 1. Toluidine blue. x 1800 FIG. 5. Photomicrograph of portion of a periodontal nerve plexus. Nerve trunk, nt.; myelinated nerve fibres leaving trunk, a; Branching of myelinated nerve fibre to form the proximal part of Type II mechanoreceptors, 2. blood vessel of arteriolar type, bv.; collecting vein, cv. Toluidine blue. x 1000
PLAn
A.O.B.
I
f.p. 918
PLATE 2
ORGANIZATION AND VASCULARIZA’IION OF PERIODONTAL RECEPTORS
PLATE2 FIG. 6. Electron micrograph of type I mechanoreceptor. Myelinated nerve fibre, A; unmyelinated nerve fibres, am; terminal unmyelinated nerve fibres, t.a.m.; capsular cell processes, CP. ; septa, S. ; tissue space, TS. Osmium tetroxide, uranyl acetate. x 13,250 FIG. 7. Electron micrograph of Type. II mechanoreceptor. Lumen of capillary, L; endothelial cell cytoplasm, En. C. ; capsular cell processes, CP. ; exposed nerve endings, E.N.; endoneurium, E.; nucleus Schwann cell, NS.; nucleus of capsular cell, CN.; collagen fibrils, CF. Osmium tetroxide, uranyl acetate. y: 17,200
919
920
C. J. GRIFFIN AND HELEN SPAIN
PLATE 3 FIG. 8. Montage of metarteriole
and capsule of Type II receptor (electron micrographs). Nucleus of endotheiial &I. N.E.; smooth muscle cell cytoplasm, SMC.; capsular cell process, CF.; secondary capsule, SC.; collagen fibrils of periodontal ligament, CP.; lacuna endings, LE.; endoneurium, E. Osmium tetroxide. uranyl acetate. x 15,000
PLATE 3 A.O.B.
f.p. 920
_-
PLATE 4
ORGANIZATIONAND VAKWLARlZAT’lON OF PERIODONTALRECEPTORS
PLATE 4 FIG. 9. Electron micrograph of terminal arteriole. Nucleus of capsular cell, NC.; capsular cell process, CP.; nucleus of endothelial cell, N.E.; smooth muscle cell, SMC.; probable myo-endothelial cell junctions, arrows. Osmium tetroxide, uranyl acetate. x 14,700 FIG. 10. Electron micrograph showing detail of myo-endothelial cell junction. Lumen, L.; endothelial cell junction, EJ.; endothehai cell, E.; smooth muscle cell cytoplasm, SMC.; myo-endothelial cell junction, ME. Osmium tetroxide, uranyl acetate. x 38,400
921
oral Bid.
Vol. 17, pp. 913-921, 1972. Pergmon
Press.
Printed inGreat Britain.
ORGANIZATION AND VASCULATURE OF HUMAN PERIODONTAL LIGAMENT MECHANORECEPTORS C.
J. GRIFFINand HELENSPAIN
Histology Department,
The University of Sydney, Australia
Summary-Periodontal nerve plexuses were studied with the light and electron-microscope. A Type I mechanoreceptor containing a single myelinated nerve fibre and unmyelinated nerve fibres and a Type II mechanoreceptor consisting of myelinated nerve fibres and unmyelinated end-rings were identified in human periodontal ligament. Each receptor had a primary and secondary capsule. Capsular cells formed a reticulum between these capsules. Encapsulated terminal arterioles, metarterioles and capillaries vascularized the neural complex. Type I receptor appeared to receive its blood supply by diffusion whereas Type II receptor had a direct blood supply. A metarteriole pierced the capsule of a Type II receptor and might be responsible for spontaneous discharges synchronous with the electrocardiogram. INTRODUCTION ENCAPSULATED periodontal
mechanoreceptors have been described by GRIFFINand SPAIN(1972) and by GRIFFIN (1972). One type consisted of an oval encapsulated nerve ending, which was derived from a single myelinated nerve fibre; the other type consisted of unmyelinated nerve fibres surrounding myelinated nerve fibres. The first type appeared to correspond to the end-knob nerve ending described by LEWINSKYand STEWART(1937) in human periodontium and the second type of nerve ending resembled the end-rings described by VAN DER SPRENKEL(1936) in the periodontal membrane of young mice. The purpose of this paper is to describe the vasculature of these end-organs and their relationship. MATERIAL
AND
METHOD
These have been described previously (GRIFFIN, 1972). Briefly, pieces of periodontium were scraped from eleven freshly extracted human teeth and were fixed with osmium tetroxide in phosphate buffer pH 7-4. They were dehydrated in acetone and embedded in Araldite. Thick sections were stained with toluidine blue and examined with the light microscope for periodontal nerve plexuses and encapsulated end-organs. These end-organs when identified were then cut in serial ultrathin sections at 4 pm intervals. The ultrathin sections were cut with an LBK ultramicrotome and stained on the grid with uranyl acetate for 1 hr. Electron micrographs and observations were made on an Hitachi HS 7 electron microscope. RESULTS
Light microscopy
Two types of encapsulated end-organs were identified in human periodontal ligament (Figs. 1-5) and have been termed Type I and Type II receptors. 913 A.O.B. 17/6--A
914
C. J. GRIFFIN AND HELEN SPAIN
Type I receptor. Type I end-organ consisted of a single myelinated nerve fibre and unmyelinated nerve fibres surrounded by the cell bodies and processes of capsular cells (Figs. 14). The myelinated nerve fibres of these receptors had diameters between 3 and 1.5 pm whilst the widest diameters of the end-organ, including its capsule, were between 7 and 12 pm. When followed in serial sections (Figs. 14) the myelinated nerve fibres of these receptors lost their myelin sheaths. The end-organ then consisted of unmyelinated nerve fibres surrounded by a capsule. Type II receptor. Type II end-organs consisted of two or more myelinated nerve fibres, unmyelinated nerve fibres and the cell bodies and processes of capsular cells (Figs. 1, 2 and 5). The myelinated nerve fibres had diameters between 2 and 3 pm and the widest diameters of these encapsulated complexes were between I5 and 20 pm. The unmyelinated nerve fibres of these end-organs encircled the myelinated nerve fibres. These endings, when followed in serial sections, were seen to be derived from a single myelinated nerve fibre which divided into two or more terminal encapsulated nerve fibres (Fig. 5). Periodontal neroe trunk. The main nerve trunk of the periodontal nerve plexus consisted of twenty or more myelinated nerve fibres and unmyelinated nerve fibres. In the serial sections, myelinated nerve fibres were seen to leave this complex and pass into the surrounding periodontal tissue to terminate as either Type I or the Type II end-organs (Fig. 5). Capsuhr complexes. Type I and Type II end-organs were surrounded by a primary capsule consisting of the cell bodies and processes of capsular cells. However, in certain cases, Type I and Type II receptors were enclosed in a secondary capsule (Figs. 1 and 2). This secondary capsule seemed to be continuous with the surrounding dense periodontal connective tissue. Cell bodies and processes of the primary and secondary capsules appeared to form a reticulum in which both Type I and Type II end-organs were enclosed. The primary capsules of the Type I end-organ were usually separated from the secondary capsule by a considerable amount of tissue or lymph space (Figs. 1 and 2). On the other hand, the primary capsules of theType II receptor were intimately related to the secondary capsule (Figs. 1 and 2). Vasculature. Blood vessels of the arteriolar type were intimately associated with the secondary capsules of Type I and Type II receptors (Figs. 1 and 2). A blood vessel of the arteriolar type was also intimately related to the primary capsule of Type II receptor (Fig. 5). Veins, presumably collecting veins, formed arcades surrounding Type I and Type II end-organs (Figs. 1 and 5). Electron microscopy Type I receptor. The Type 1 receptor consisted of a single myelinated nerve and unmyelinated nerve fibres surrounded by the cell processes of the capsular cells (Fig. 6). A septum, consisting of the cytoplasmic process of a capsular cell, partially separated the myelinated nerve fibre from the unmyelinated elements. The unmyelinated nerve fibres divided into minute terminal branches. What appeared to be the distal part of a Type I receptor was also seen (Fig. 6). This complex was also divided into several segments by the nucleus and cell processes of capsular cells.
ORGANIZATION
AND
VASCULARIZATION
OF PERIODONTAL
RECEPTORS
915
Large unmyelinated nerve fibres and unmyelinated nerve fibres, dividing into minute terminal branches, comprised the distal portion of the end-organ. The myelinated nerve fibres were approximately 2 *5 pm in diameter, whereas the largest unmyelinated nerve fibres were approximately 1.1 pm. The minute terminal axons had diameters between 0 - 3 and 0 * 15 pm. No blood vessels were seen intracapsularly. Type ZZreceptor. The Type II receptor contained blood vessels of the capillary type (Fig. 7). Capsular cell processes and exposed nerve endings were in close proximity to the blood vessel. A blood vessel of the metarteriolar type was also seen to enter the capsule of a Type II receptor (Fig. 8). The tunica media of this blood vessel consisted of an interrupted layer of smooth muscle cells. On one side of the metarteriole was the dense fibrous tissue of the periodontal ligament whilst on the other side were enclosed nerve endings of the receptor (lacuna endings). Terminal arteriole. The afferent arteriole observed with the light microscope was seen to be an encapsulated blood vessel with a single layer of smooth muscle cells. These smooth muscle cells appeared to effect tight junctions with endothelial cells (Figs. 9 and 10). According to RHODIN(1967), these vessels correspond to terminal arterioles.
DISCUSSION Two types of receptors constructed on a common organizational theme may be identified in human periodontal ligament. The Type I receptor appears to be a discrete unit, the fine structure of which has been described by GRIFFINand SPAIN(1972). It appears to correspond to the end-knobs described by LEWINSKYand STEWART(1937). Usually this receptor is surrounded by a considerable amount of tissue space (Figs. 1 and 2) and, because of this, might slip out of the way of a stimulating force. It is therefor considered that this receptor might be a rapidly adapting unit. Type II receptor is somewhat more complex. It is derived from a single myelinated nerve fibre which divides into two or more terminal encapsulated myelinated nerve fibres (GRIFFIN, 1972). The primary capsule of this end-organ was more intimately related to the secondary capsule than that of the Type I receptor and on this basis it might be a slowly adapting unit. On the other hand, there was an appreciable amount of tissue space between the neural elements of the end-organ (Figs. 1, 2 and 5). The myelinated nerve fibres of the ending appeared to lose their myelin sheaths in a staggered fashion and to terminate as unmyelinated nerve fibres encircling adjacent myelinated nerve fibres (Figs. 1 and 2). This arrangement might indicate that, if the parent fibre was displaced along its course, the end-organ might discharge. The periodontal nerve plexuses appear to receive their blood supply from blood vessels of the terminal arteriolar type (Figs. 1, 2 and 9). On entering the plexus, the afferent terminal arteriole appears to be encapsulated by cell processes of capsular cells (Fig. 9). A feature of this bloodvessel is the presence of myo-endothelial junctions (Figs. 9 and 10). RHODIN (1967) found numerous myo-endothelial junctions in the terminal arterioles of the fascia of the rabbit medial thigh muscles. He considered that, although these junctions might serve to stabilize the microvascular wall, they were
916
C.
J. GRIFFIN AND
HELEN SPAIN
more probably pathways for the exchange of metabolites, more specifically bloodborne transmitter substances. In the present study, we have not been able to demonstrate the innervation of terminal arterioles and metarterioles. However, there is general agreement that the smooth muscle cells of arteries and arterioles receive both an afferent and efferent innervation (RHODIN, 1967; GRIGOR EVA, 1962; FULTONand LUTZ, 1942; FALCK, 1962). RHODIN (1967) showed that nerve axons follow closely the adventitial aspect of the media of arterioles, terminal arterioles and precapillary sphincters of the rabbit medial thigh muscle and demonstrated nerve endings within smooth muscle cells of terminal arterioles which contained granulated vesicles. He considered that there was a more intimate nervous control of terminal arterioles than is the case with larger arterioles. NICOLL (1964) observed rhythmical active vasomotion of the terminal arterioles of the bat’s wing which appeared to be independent of nervous control because this activity was not significantly affected when the nerve to the area was stimulated. However, what appears to be significant in the present study is that metarterioles enter the capsule of the Type II receptor (Fig. 5). Their proximity to lacuna endings (Fig. 8) suggests that these vessels could be responsible for spontaneous discharges. In the periodontium of the dog, HANNAM(1969b) recorded spontaneous discharges synchronous with the electrocardiogram. On the light and electron microscopic evidence, it would appear that the Type II periodontal ligament receptors have a direct blood supply (Figs. 5 and 8) and that endoneural capillary blood vessels pass between the neural elements. On the other hand the Type I receptor probably receives its nutrition by diffusion of substances from surrounding capillary vessels. R&urn&-Les plexus des nerfs parodontaux sont Ctudits en microscopic optique et Clectronique. Un type 1 de r&epteurs mkaniques contenant une seule fibre nerveuse myeliniste et des fibres non myclinis&s et un type II comportant des fibres nerveuses my~linis&s et des noeuds terminaux non my&linisCs ont pu &tre identifib dans le ligament. Chaque rt5cepteur a une capsule primaire et secondaire. Des cellules capsulaires forment un reticulum entre ces capsules. Des artCrioles terminals encapsul&s, des mCtartCrioles et des capillaires vascularisent le complexe neural. Le r&epteur de type I semble recevoir sa vascularisation par diffusion, alors que le type 11 est directement vascularis Une m&arteriole perce la capsule du rkepteur de type II et peut &tre responsable des d&charges spontan&.s synchrones des tlectrocardiogrammes.
Zusammenfassung-Lichtund elektronenmikroskopisch wurde der parodontale Nervenplexus untersucht. Ein Mechanorezeptor vom Typ I mit einer einzelnen markhaltigen Nervenfaser und mit marklosen Nervenfasern sowie ein Mechanorezeptor vom Typ II, aus markhaltigen Nervenfasern und marklosen Endringen bestehend, wurden im menschlichen Desmodont identitiziert. Jeder Rezeptor besaD eine primtire und eine sekundlre Kapsel. Die Kapselzellen bildeten zwischen den Kapseln ein Retikulum. Eingekapselte Endarteriolen, Metarteriolen und Kapillaren vaskularisierten den neuralen Komplex. Der Rezeptor vom Typ I schien seine Blutversorgung auf dem Wege der Diffusion zu erhalten, wlhrend der Rezeptor vom Typ II direkt mit Blut versorgt wurde. Eine Metarteriole durchdrang die Kapsel des Typ II-Rezeptors und diirfte fiir die synchron mit dem Elektrokariogramm erfolgenden spontanen Entladungen verantwortlich sein.
ORGANIZATION AND VASCULARIZATIONOF PERIODONTALRECEPl-ORS
917
REFERENCES FALCK, B. 1962. Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta physiol. &and. 56, Suppl. 197. FULTON, G. P. and LUTZ, B. R. 1942. Smooth muscle motor units in small blood vessels. Am. J.
Physiol. 135, 531-534. GRIFFIN, C. J. 1972. The fine structure
of end-rings in human periodontal
ligament.
Archs oral Biol.
17, 785-797. GRIFFIN, C. J. and SPAIN, H. 1972. The fine structure of periodontal nerve plexuses in man. In: The MaxiNo-Mandibular Apparatus. Proc. Internat. Anat. Congr. Leningrad 1970. In press. HANNAM, A. G. 1969b. Spontaneous activity in dental mechanosensitive units in the dog. Archs oral
Biol. 14, 793-801. LEWINSKY, W. and STEWART, D. 1937. The innervation
of the periodontal
membrane.
J. Anat. 71,
98-102. GRIGOR’ EVA, T. A. 1962. The Innervation of Blood Vessels, p. 1.53. Pergamon Press, Oxford. NICOLL, P. A. Autoregulation of Blood Flow, p. 245. Am. Heart Ass., Monograph 8, New York. RHODIN, J. 1967. The ultrastructure of mammalian arterioles and precapillary sphincters. J. ultrastruct. Res. 18, 181-223.
PLATES l-4
OVERLEAP
C.
918
J. GIUFF~NAND
HELEN SPAIN
PLATE 1 FIG. 1. Photomicrograph of portion of a periodontal nerve plexus. Arteriolar type blood vessel, bv.; collecting vein, cv.; Type I mechanoreceptors, 1; Type II mechanoreceptors, 2; primary capsule, pc.; secondary capsule, SC.; end-ring, r. Toluidine blue. x 1800 FIG. 2. Photomicrograph of portion of a periodontal nerve plexus 4 pm from Fig. 1. Arteriolar type blood vessel, bv. ; Type I mechanoreceptors, 1; Type II mechanoreceptors, 2; secondary capsule, SC.; tissue space between primary and secondary capsules of Type I receptors Sl ; tissue space between Type II mechanoreceptors and secondary capsule, S2. Toluidine blue. x 1800 FIG. 3. Photomicrograph mechanoreceptors.
of portion of a periodontal nerve plexus showing Type I Type I mechanoreceptors, 1. Toluidine blue. x 1800
FIG. 4. Photomicrograph of portion of a periodontal nerve plexus 4 pm from Fig. 3. Type I mechanoreceptors, 1. Toluidine blue. x 1800 FIG. 5. Photomicrograph of portion of a periodontal nerve plexus. Nerve trunk, nt.; myelinated nerve fibres leaving trunk, a; Branching of myelinated nerve fibre to form the proximal part of Type II mechanoreceptors, 2. blood vessel of arteriolar type, bv.; collecting vein, cv. Toluidine blue. x 1000
PLAn
A.O.B.
I
f.p. 918
PLATE 2
ORGANIZATION AND VASCULARIZA’IION OF PERIODONTAL RECEPTORS
PLATE2 FIG. 6. Electron micrograph of type I mechanoreceptor. Myelinated nerve fibre, A; unmyelinated nerve fibres, am; terminal unmyelinated nerve fibres, t.a.m.; capsular cell processes, CP. ; septa, S. ; tissue space, TS. Osmium tetroxide, uranyl acetate. x 13,250 FIG. 7. Electron micrograph of Type. II mechanoreceptor. Lumen of capillary, L; endothelial cell cytoplasm, En. C. ; capsular cell processes, CP. ; exposed nerve endings, E.N.; endoneurium, E.; nucleus Schwann cell, NS.; nucleus of capsular cell, CN.; collagen fibrils, CF. Osmium tetroxide, uranyl acetate. y: 17,200
919
920
C. J. GRIFFIN AND HELEN SPAIN
PLATE 3 FIG. 8. Montage of metarteriole
and capsule of Type II receptor (electron micrographs). Nucleus of endotheiial &I. N.E.; smooth muscle cell cytoplasm, SMC.; capsular cell process, CF.; secondary capsule, SC.; collagen fibrils of periodontal ligament, CP.; lacuna endings, LE.; endoneurium, E. Osmium tetroxide. uranyl acetate. x 15,000
PLATE 3 A.O.B.
f.p. 920
_-
PLATE 4
ORGANIZATIONAND VAKWLARlZAT’lON OF PERIODONTALRECEPTORS
PLATE 4 FIG. 9. Electron micrograph of terminal arteriole. Nucleus of capsular cell, NC.; capsular cell process, CP.; nucleus of endothelial cell, N.E.; smooth muscle cell, SMC.; probable myo-endothelial cell junctions, arrows. Osmium tetroxide, uranyl acetate. x 14,700 FIG. 10. Electron micrograph showing detail of myo-endothelial cell junction. Lumen, L.; endothelial cell junction, EJ.; endothehai cell, E.; smooth muscle cell cytoplasm, SMC.; myo-endothelial cell junction, ME. Osmium tetroxide, uranyl acetate. x 38,400
921