Front. Oral Physiol., vol. 2, pp. 130-145 (Karger, Basel 1976)
The Blood Circulation of the Tongues GÖRAN HELLEKANT
Department of Physiology, Veterinärhögskolan, HIC, Uppsala
Contents Gross Anatomy of the Vessels in the Tongue Arteries Veins Anastomoses Connections between the Right and Left Side Blood Flow of the Tongue Effect of Arterial Occlusion Circulation of the Lingual Papillae Topographical Orientation Filiform Papillae Circumvallate Papillae Foliate Papillae Fungiform Papillae Circulation of the Taste Buds Vascular Innervation of the Tongue Vascoconstrictor Nerves to the Tongue Vasodilator Nerves to the Tongue Summary References
131 l 31 132 132 133 133 134 134 134 136 137 137 138 138 140 140 141 142 143
Since a previous review [HELLEKANT, 1972] on this topic several studies have been published. This new review will serve as a short survey of the vascular anatomy, innervation and physiology of the mammalian tongue
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1 This study was supported by grants from Svenska Maltdrycksforskningsradet, Swedish Medical Council grant No. 2467, Magnus Bergvalls Stiftelse and Knut and Alice Wallenbergs Stiftelse.
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but will also include some recent observations and conclusions which are less well established. It is based on observations obtained in the cat, dog, guinea pig, goat, man, monkey, rabbit, rat and sheep. The tongues of all these species have been classified by DORAN and BAGGET [1971] as being of the intraoral type and morphologically similar. Further, there is little difference between the vascular supply of the tongue of the rabbit and man, according to Görzε and L'ERSE [1969]. This indicates that observations made in one of the species mentioned are, within limitations, valid in another.
Arteries The vascular system on one side in the tongue of the rabbit is schematically shown in figure 1, which is taken from a study of Görzε and L'ERSE 1969]. Figure 1 shows that the lingual artery (3) gives off a dorsal branch, sometimes 2 or 3 dorsal branches in man, (4) and a sublingual (5) branch, whereupon it proceeds as the profund or deep lingual artery (6) to the tip of the tongue. The dorsal lingual artery runs lateral to the large hyoid bone (2), gives rise to a few branches to the epiglottis, palatoglossal arch, tonsil and soft palate and then proceeds in a lateral and apical direction. It anastomoses with branches from the profund artery, and with vessels from the opposite side, but gives off on the average few branches. The profund lingual artery, which is the continuation of the lingual runs anteriously near the frenulum along with the lingual nerve, and gives off vertical branches to the upper surface of the tongue. The distance between each branch diminishes as the artery approaches the tip of the tongue. These vertical branches, together with the branches from the dorsal artery, form two vascular plexuses, a submucosal (8) and a subpapillary one (10). The capillary network of the lingual papillae is chiefly derived from the latter plexus. The region between the two plexuses is considered to be relatively avascular [CUTRIGHr and HuiSucK, 1970]. Near its origin the sublingual artery gives off two branches, a superficial (13) and a deep one (14). These branches anastomose with those of the contralateral sides. Each anastomosis gives off a branch which runs in apical direction in the midline of the tongue. The sublingual artery itself supplies the sublingual salivary gland and ends on the oral side of the gingiva.
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Gross Anatomy of the Vessels in the Tongue
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Fig. 1. Schematic drawing of the blood vessels in the tongue of the rabbit. 1 = The mandible; 2 = the hyoid bone; 3 = A. lingualis; 4 = A. lingualis dorsalis; 5 = A. sublingualis; 6 = A. profunda linguae; 7 = Rr. verticales; 8 = submucosal net; 9 = Rf. perforantes ; 10 = subpapillary net; 11 = vasa papillares; 12 = muscular branches of A. lingualis profunda; 13 = R. communicans superficialis; 14 = R. communicans profundus; 15 = unpaired branch of Rr. communicantes superf.; 16 = muscular branches of R. communicans prof.; 17 = A. submentalis; 18 = V. comítans N. hypxglossi. I = Contralateral anastomoses at the subpapillary net; II = contralateral anstomoses of the Aa. profunda linguae; III = contralateral anstomoses for the Rr. perforantes; IV = contralateral anastomoses of the Rf. communicantes superf. and prof. [Görzε and LIER5E, 1969]. In man, variations of the branching of the lingual artery have been described. Thus, though the lingual artery branches from the external carotid artery in most cases, it may also branch from the superior thyroid artery or from one of the other posterior branches [Smile et al., 1971]. The sublingual artery may origin from the facial artery [AKiyAiA, 1970, HAMPARIAN, 1973].
Anastomoses Arteriovenous anastomoses which form direct communications between arteries and veins are widespread in the body [LIEBow, 1963]. In the tongue such anastomoses have been described by BRowN [1937], DAτELOω [1951],
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Veins The veins run parallel to their corresponding arteries. The deep lingual vein divides in two in the anterior part of the tongue; the two veins then join to form a single vessel. It then proceeds caudally along the ventral side of the corresponding artery.
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PRICHARD and DANIEL [1953] and OHLSSON [1971]. The vessel walls are thick, and the media contains smooth muscle cells and epithelioid cells in large numbers [PRICHARD and DANIEL, 1953]. They have a rich nerve supply [BRowN, 1937] which also seems to include a large sensory portion. In the dog they seem to be located both in the subpapillary plexus and in the lingual papillae [DABELOW, 1951]. The tongue of sheep and goat are similar, in this respect, to that of the dog [PRICHARD and DANIEL, 1953]. In man they are seldom found or absent, according to Μ Rκ [1941] and DABELOW [1951]. In the tongue of the rabbit, guinea pig and cat, CLARA [1927] and DABELOW [1951] found no arteriovenous anastomoses. SAVIY et al. [1971] describe anastomoses between the arteries in man. They found them to be predominant in the tip and the posterior part of the tongue. DENIsOVA [1973] observed many anastomoses and describes three types, termino-terminal, termino-lateral and lateral-lateral.
Blood Flow of the Tongue The rich vascularization that has been described here indicates that the blood supply to the tongue is more abundant than to most other muscular organs of the body. Available data also indicate that the tongue receives more blood than can be expected from its size. MEYER [1970] estimated by the use of isotopes that the flow to the tongue of the dog is about 0.22 ml/ min/g. In the cat ALM and BILL [1973] and HALES [1973] determined the flow to be 0.29 ml/min/g. Observations in the rat [HELLEKANT, 1971b] indicate that the flow varies between 0.2 and 0.3 ml/min/g. This is only about 50 of the flow to the dental pulp of the dog, 0.54 ml/min/g [MEYER, 1970], but is considerably more than the value obtained from skeletal muscle at rest, 0.03 ml/min/g [MELLANDER and JoHANSSON, 1968].
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Connections between the Right and Left Side GUTZE and L'ERSE [1969] state that there are few connections between the vessels of the left and right side except in the tip and the very posterior part of the tongue. In the tip there seems to be connections between the left and right side. Thus in man HUBIER [1968] found contra-lateral anastomoses in the tip in 11 preparations out of 17. He also noticed faint connections in the back of the tongue. In all he found anastomoses in 15 out of 17 cases. Intravital staining through one lingual artery in the rat indicates that the tongue is unilaterally supplied to a large extent [HELLEKANT, 1971 a] though some staining could be observed on the contralateral ventral side of the tip too.
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The vascular bed of the tongue can be used for the diagnosis of circulatory disturbances [DAVms and LANDAU, 1966; MERLEN et al., 1973]. Thus, Görzε [1972] observed changes correlated with diabetes mellitus. Similarly, TsuYA et al., [1971] found a significant correlation between the doses of radiation from the atomic bomb and changes in the circulatory pattern of the lingual mucosal capillaries on the other. Effect of Arterial Occlusion It is generally known that hemorrhage from the tongue is difficult to stop. Observations in the dog by SHEPHERD et al. [1971] show that occlusion of the ipsilateral lingual artery does not stop bleeding from the deep lingual artery. Simultaneous clamping of the ipsilateral lingual and external carotid arteries slows the bleeding from the deep lingual one, but does not arrest it. Only when both the common carotid arteries are occluded does the blood flow stop. The effect of permanent occlusion of some of the vessels to the tongue has also been described. Thus, Görzε and L'ERSE [1969] unilaterally occluded the lingual artery in one rabbit and the external carotid in another for 1 week. They found no light microscopical difference between the two sides. These observations indicate that the occluded side of the tongue, through the anastomoses described, receives enough blood to maintain its morphological characteristics. Further, the vascularization seems to be rich enough to prevent tissue damage in spite of extensive atherosclerosis both in man [DREIZEN et al., 1974] and in rabbit [DREIZEN et al., 1971]. This rich vascularization also underlies the advice of NIcHOLs and CurluG-r [1971] that the tongue be used for injections of emergency drugs. They observed little difference in latency between the maximum effects of intravenous or intralingual injections in monkeys. However, with regard to the function of the taste receptor cells, experiments in the anesthetized rat [HELLEKANT, 1971 a] show that after the ipsilateral carotid artery is occluded the blood flow through only the contralateral external carotid artery is too small to maintain the taste sensitivity of the fungiform taste buds.
Topographical Orientation There are four different kinds of papillae on the mammalian tongue, the filiform, the circumvallate, the foliate and the fungiform papillae. The
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Circulation of the Lingual Papillae
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Fig. 2. Schematic drawing of the vascular network of the filiform papilla in man. An artery (A) and a vein (V) run parallel to the surface in the lamina propria mucosae. A vertical branch (a) is given off below the papilla. The papilla empties through the central venous sinus (vs) which shows a constriction of its wall at the point of entry into the vein (V). pl = Peripheral veins; ak = arterial and vk = venous capillaries in the secondary papillae (SP); o = oral; and p = pharyngeal directions [KUNZE, 1969].
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last bear the taste buds. The filiform papillae cover the dorsum and the sides of the tongue. The fungiform papillae occur principally on the tip and lateral anterior part of the tongue but are also scattered over the dorsum. They bear taste buds on their oral surface. The circumvallate papillae are found in the posterior part of the dorsum. Their number varies from one species to another, but is generally less than five, in man up to 15 [TUCKERΜΑΝ, 1890]. The papilla is surrounded by a groove (fig. 3) the walls of which contain the taste buds. The foliate papillae are situated in the posterolateral part of the tongue in front of the anterior pillars of the soft palate. Their
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taste buds are located in their sides. The circulation of these different papillae will now be described in some detail. The subpapillary plexus described above supplies the papillae.
Fig. 3. Vascular network of the circumvallate papilla in the dog. m = Blood vessels of muscularis; a = arteries; v = veins; k = capillaries. Indian ink injection [DABELOW, 1951].
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Filiform Papillae The filiform papillae constitute the majority of the papillae on the tongue and are the only ones which have no taste buds. In man there are about 500/cm2 [KUNZE, 1969]. Their shape varies from a simple curved coneshaped form in the cat to a rather complicated one in man, as shown in figure 2. The drawing shows that each filiform papilla in man carries about ten secondary papillae. It also illustrates the blood supply. Α small artery, parallel to the surface of the tongue, gives off a branch that enters the primary papilla and then divides. The lumina of the vessels entering the secondary papillae are only half or a third the diameter of those leaving them. The vein that drains the papilla shows a constriction (the arrow in figure 2) which has several contractile elements in its wall [KUNZE, 1969]. In the dog the vascular supply of the filiform papillae occurs in two forms, a more simple one which also shows arteriovenous anastomoses, and a more complicated variant which occurs most abundantly in the vicinity of the circumvallate papillae [DABELOW, 1951].
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Circumvallate Papillae The circumvallate papillae receive their blood supply from the large vessels which arise in the muscularis (fig. 3). The vessels give off numerous capillary loops which rise towards the surface of the papilla. The loops decrease in height near the bottom of the groove. The tissue peripheral to the groove is also supplied by a plexus of vessels. This plexus faces the groove and is somewhat flattened.
Fig. 4. Α cross-section of the posterior margin of the foliate zone of the rabbit tongue. The arrow points to loops in the capillary bed beneath the gustatory epithelium. The large sinusoidal vessel which drains the foliate zone is apparent at the extreme right. The central sinusoidal vessels of the papillae and the subpapillary sinuses are also shown. Indian ink injection [ELLIS, 1959].
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Foliate Papillae In the rabbit the circulatory system of the foliate papillae consists of arterioles, a bilateral system of capillary loops, shunts and anastomosing sinusoids, which are linked to the venous system [ILLIS, 1959]. The arterioles which enter the papilla divide into a series of capillary loops at the level of the taste buds (fig. 4). These capillaries converge toward the superior
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surface of the papilla above the level of the most superficial taste buds, curve toward the surface epithelium and then reverse their direction, forming terminal capillary loops. Finally, as venules they veer toward the center and base of the papilla where they join the large sinuoids which are found centrally in the rabbit but not in primates. These sinusoids are primarily associated with the von Εbner's glands. Even the deep-lying portions of these glands are surrounded by them [ELLIS, 1959]. The taste buds of the papillae are supplied by blood from the capillary loops and not by the sinusoidal system. The capillary supply of these taste buds is not so rich as those of the fungiform and vallate papillae, according to ELLIS [1959]. In the dog [SCHUMACHER and NIKOLOl, 1973] the capillaries within the papillae form a plexus close to the epithelium. They are supplied with one or two precapillary vessels and the blood leaves the papilla through a central vein.
Circulation of the Taste Buds The receptor cells, which transduce the influence of a chemical into a taste, are localized in certain structures, the taste buds. Their localization has already been described. The taste buds in the anterior two thirds of the tongue are innervated by fibers from the chords tympani proper nerve, which is a branch of the facial nerve. Those of the posterior part are supplied by fibers from the glossopharyngeal and vagal nerves. However, those of the foliate papillae may receive fibers from both the chords tympani proper and facial nerves [YAMAMoro and KAWAMURA, 1975]. The message from the taste receptor cells to the brain can be recorded as nerve impulses from these nerves. These impulses provide a good indication of the function of the taste cells. If the blood flow through the lingual arteries is cut off, the chords tympani response disappears within a few minutes [HELLEKANT, 1971a]. This deterioration of response to taste stimulation cannot be attributed to any
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Fungifοrm Papillae In man there are about 100/cm 2 fungiform papillae in the tip and 50/cm2 in the middle of the tongue [KUNZE, 1969]. These papillae have a rich blood supply. In the dog, DABELOW [1951] describes two types with somewhat different vascular pattern (fig. 5). The capillaries entering the base of each papilla are arranged radially. Towards the surface they converge and form rich anastomoses between the taste buds. The taste buds of the fungiform papillae have a more elaborate capillary bed than those of the other types [ELLIS, 1959; SCHUHMACHER and NIKOLOl, 1973].
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effects on the nerve fibers, because their excitability is maintained for a much longer time. The shortness of this period indicates a rather high metabolic rate of the taste receptor cells. Among the possible causes for this effect, oxygen deficit has been suggested as the most important one [HELLEKANT, 1971b]. These observations were obtained in rat. In man, STEINER [1971] reported decreased taste sensitivity in cases of acrocyanosis and other types of peripheral circulatory disturbances, which can be detected by the method of biomicroscopy. The taste sensitivity can not only be affected by decrease of blood flow, but also by increase of blood flow. Thus, the taste response can be enhanced by such an increase [HELLEKANT, 1971b].
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Fig. 5. The two main types of vascular net in the fungiform papillae of the dog. a = Arteries; v = veins; k = capillaries. Indian ink injection [DABELOW, 1951].
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Vascular Innervation of the Tongue The concept that the blood vessels of the tongue, like other structures innervated by the autonomic nervous system, have a reciprocal cholinergic and adrenergic innervation, was proposed by BAYLISS [1923]. Since then it has been established that: (1) there exist vasoconstrictor nerves. These nerves are widely distributed, they are sympathetic in origin and they are exclusively adrenergic; (2) there exist vasodilator nerves which are parasympathetic in origin. They are cholinergic and supply certain regions like the genitalia and probably also the tongue, which is of interest in this context; (3) there are vasodilator nerve fibers to skeletal muscles in certain species [BoLΙΙΙE and FUXE, 1970]. These nerves are of sympathetic origin but cholinergic. ERIcΙ et al., [1952], ECCLES and WALL'S [1974] suggest that such fibers may innervate the tongue in the cat. Vasoconstrictor Nerves to the Tongue It is established that the tongue receives adrenergic sympathetic vasoconstrictor fibers, which when stimulated, increase the resistance of the vessels in the tongue, as shown in the left record on figure 6. In this experiment the tongue of the rat was perfused with its own blood through an external loop while the blood flow and resistance of the lingual artery were recorded.
symg
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Fig. 6. The effects of stimulation of the ipsilateral sympathetic nerve to the tongue of the rat (left) and of the chorda tympani nerve (right) on the vascular resistance in the tongue are shown. The records were obtained during unilateral perfusion of the tongue with the rat's own blood. The upper trace shows the perfusion pressure in the lingual artery, the middle trace the flow rate and the bottom one the blood pressure in one femoral artery. The horizontal bars illustrate electrical stimulation of the peripheral parts of the nerves in question [HELLEKANT, 1972].
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Vasodilator Nerves to the Tongue The existence of cholinergic parasympathetic vasodilator fibers to the tongue has been disputed, though it is well known that electrical stimulation of the peripheral part of the chords tympani nerve, whose efferent portion is of parasympathetic origin, decreases the vascular resistance in a manner shown in the right record of figure 6. It seems that it is generally thought that this decrease is caused by impulses which are elicited in sensory fibers and which travel in an antidromic direction to the tongue. However, this explanation is unlikely to be correct. This is shown by the following experiment. The cell bodies of the sensory fibers in the chords tympani proper nerve are situated in the geniculate ganglion [VILLIGER, 1964]. If the facial nerve is cut between this ganglion and C'S all other fibers in the chords tympani proper will degenerate except the sensory ones. After such degeneration stimulation of the chords tympani proper causes no dilatation of the vessels in the tongue. Figure 7 gives an example of this. In figure 7 the vascular resistance of the tongue was recorded in a similar way as in figure 6. The record shows that stimulation of the chords tympani proper nerve with 40 and 70 Hz, respectively, which in a normal animal gives a strong vasodilation, had no effect on the vascular resistance of the tongue. We have repeated these experiments in a number of animals with similar results. In these animals the sensory innervation remain. This can be demonstrated by recording the response to taste stimulation or mechanical stimulation. Thus it seems that antidromic impulses in the sensory fibers cannot explain the well-known vasodilation in the tongue [Ετττcτ and Uvνλs, 1952 ; ECCLES and WALL'S, 1974]. Further, efferent nerve impulse [FIELLEKANT, 1971c] have been recorded in the chords tympani proper nerve. Some of this impulse activity seems to be unrelated to salivary secretion, because it occurs, and can change, without causing secretion [HELLEKANT and HAGSTROM, 1974]. This activity may be related to food intake, e.g., stomach distension [HELLEKANT, 1971d] decreases it. Finally, a widespread adrenergic as well as cholinergic innervation in and along the arteries, arterioles and metaarterioles in the tongue has been
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The ipsilateral sympathetic nerve was then electrically stimulated at the level of the superior cervical ganglion during the time periods indicated by the signal. This resulted in an increased overall vascular resistance in the tongue. In the cat, ALM and BILE, [1973] found a 80 % reduction of blood flow through the tongue after 1 min of stimulation of the cervical sympathetic chain.
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Fig. 7. The effect of stimulation of only the sensory portion of the chords tympani proper nerve on the vascular resistance of the tongue was recorded in a similar way as in figure 6. The frequency of the electrical stimulus applied is shown. No effect on the vascular resistance was recorded by the antidromic impulses. demonstrated histochemically by SCHEICK and BADAWI [1968]. These authors conclude that the number of cholinergic fibers was larger in the tongue than, for example, in the skeletal muscles or the gastrointestinal tract. More direct evidence is perhaps presented by SIGGINS and WEITSEN [1971] who describe pronounced vasodilation after microelectrode stimulation of associated terminal nerves. This vasodilation was still elicited after 2 days of topical treatment with 6-hydroxydopamíne. The cholinergic nature of these fibers were established with histochemical technique. The thiocholine method of KARNOVSKY [1964] and the selective methylene blue technique of Rτcκλι DSON [1969] were used. The observations of SIGGINS and WEITSEN [1971] were obtained in the retrolingual membrane of the frog but it is likely that if cholinergic vasodilation exists in this species it will exist in higher ones also. Similar observations were reported by BERMAN et al. [1972]. In mammals, FAAZGERALD and ALEXANDER [1969] have presented further evidence for the existence of a cholinergic parasympathetic nerve supply to the vessels in the tongue. They studied intramuscular ganglia in the tongue of the cat. They conclude that in the anterior two thirds of the tongue these ganglia can be assigned with confidence to the chords-lingual nerve. The ganglia did not innervate glandular tissue of the tongue. Rather, the fine nerve fibers from these ganglia were traced to nerve plexuses on the walls of the arteries with an external diameter of 150-300 Μm.
This article describes the gross anatomy of the vessels which supply the mammalian tongue. It shows that there is a rich vascular supply. Available data indicate that the lingual
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Summary
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papillae are supplied with a true capillary circulation, which is more abundant in the papillae containing taste buds. The vessels of the tongue are innervated by adrenergic sympathetic vasoconstrictor fibers and it is also very likely that a cholinergic parasympathetic vasodilator influence exists.
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OHLssON, E. G.: Regional blood flow studies with labelled microspheres of different sizes in dogs with and without occlusion of the common bile duct. Eurog. surg. Res. 3: 348-362 (1971). PRICHARD, M. M. L. and DANIEL, P. M.: Arterio-venous anastomoses in the tongue of the dog. J. Anat. 87: 66-74 (1953). RICHARDSON, K. C.: The fine structure of autonomic nerves after vital staining with methylene blue. Anat. Rec. 164: 359 (1969). SAVID, V.; BOGDANOVIC, D.; SΤοsτδ, T., and JELICIY, Ν.: O mοrfoloskim f tοpografskin odlikama jezicne arterije. Stomat. Glasn. 18: 197-203 (1971. SCHEICK E. A. and BADAWI, A. E.: Dual innervation of arteries and arterioles. Z. Zellforsch. 91: 170-177 (1968). SCHUMACHER, G. Η. und NIKOLOl, S. D.: Zur Frage der Blutgefässversorgung der Zunge. Blutgefässversorgung der Zungenschleimhaut beim Hund. Dt. Stomat. 23: 260-266 (1973). SHEPHERD, Ν. J. ; MALONEY, Ρ. L., and Dοκu, H. C.: Control of lingual artery hemorrhage in dogs. Oral Surg. 31: 298-301 (1971). SIGGINS, G. R. and WEITSEN, H. A.: Cytochemical and physiological evidence for cholinergic, neurogenic vasodilation of amphibian arterioles and precapillary sphincters. I. Light microsopy. Microvasc. Res. 3: 308-322 (1971). STEINER, J. E.: Personal commun. 4th Symposium on Olfaction and Taste (1971). TSUYA, A.; WAKANO, Υ., and OTAKE, M.: Capillary microscopic observation on the superficial minute vessels of atomic bomb survivors 1956-1957. Radiat. Res. 46: 199-216 (1971). TuCKERMAN, F.: On the gustatory organs of some of the mammalia. J. Morphol. 4: 152-193 (1890). ΥΑΜΑΜOΤ0, T. and KAWAMURA, Υ.: Dual innervation of the foliate papillae of the rat: an electrophysiological study. Chem. Senses Flavor. 1: 241-244 (1975). VILLIGER, B.: Die periphere Innervation, p. 219 (Wilhelm Engelmann, 1964).
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Dr. G. HELLEKANT, Department of Physiology, Veterinärhögskolan, HIC, S-750 07 Uppsala (Sweden)
The Blood Circulation of the Tongues GÖRAN HELLEKANT
Department of Physiology, Veterinärhögskolan, HIC, Uppsala
Contents Gross Anatomy of the Vessels in the Tongue Arteries Veins Anastomoses Connections between the Right and Left Side Blood Flow of the Tongue Effect of Arterial Occlusion Circulation of the Lingual Papillae Topographical Orientation Filiform Papillae Circumvallate Papillae Foliate Papillae Fungiform Papillae Circulation of the Taste Buds Vascular Innervation of the Tongue Vascoconstrictor Nerves to the Tongue Vasodilator Nerves to the Tongue Summary References
131 l 31 132 132 133 133 134 134 134 136 137 137 138 138 140 140 141 142 143
Since a previous review [HELLEKANT, 1972] on this topic several studies have been published. This new review will serve as a short survey of the vascular anatomy, innervation and physiology of the mammalian tongue
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1 This study was supported by grants from Svenska Maltdrycksforskningsradet, Swedish Medical Council grant No. 2467, Magnus Bergvalls Stiftelse and Knut and Alice Wallenbergs Stiftelse.
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but will also include some recent observations and conclusions which are less well established. It is based on observations obtained in the cat, dog, guinea pig, goat, man, monkey, rabbit, rat and sheep. The tongues of all these species have been classified by DORAN and BAGGET [1971] as being of the intraoral type and morphologically similar. Further, there is little difference between the vascular supply of the tongue of the rabbit and man, according to Görzε and L'ERSE [1969]. This indicates that observations made in one of the species mentioned are, within limitations, valid in another.
Arteries The vascular system on one side in the tongue of the rabbit is schematically shown in figure 1, which is taken from a study of Görzε and L'ERSE 1969]. Figure 1 shows that the lingual artery (3) gives off a dorsal branch, sometimes 2 or 3 dorsal branches in man, (4) and a sublingual (5) branch, whereupon it proceeds as the profund or deep lingual artery (6) to the tip of the tongue. The dorsal lingual artery runs lateral to the large hyoid bone (2), gives rise to a few branches to the epiglottis, palatoglossal arch, tonsil and soft palate and then proceeds in a lateral and apical direction. It anastomoses with branches from the profund artery, and with vessels from the opposite side, but gives off on the average few branches. The profund lingual artery, which is the continuation of the lingual runs anteriously near the frenulum along with the lingual nerve, and gives off vertical branches to the upper surface of the tongue. The distance between each branch diminishes as the artery approaches the tip of the tongue. These vertical branches, together with the branches from the dorsal artery, form two vascular plexuses, a submucosal (8) and a subpapillary one (10). The capillary network of the lingual papillae is chiefly derived from the latter plexus. The region between the two plexuses is considered to be relatively avascular [CUTRIGHr and HuiSucK, 1970]. Near its origin the sublingual artery gives off two branches, a superficial (13) and a deep one (14). These branches anastomose with those of the contralateral sides. Each anastomosis gives off a branch which runs in apical direction in the midline of the tongue. The sublingual artery itself supplies the sublingual salivary gland and ends on the oral side of the gingiva.
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Gross Anatomy of the Vessels in the Tongue
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Fig. 1. Schematic drawing of the blood vessels in the tongue of the rabbit. 1 = The mandible; 2 = the hyoid bone; 3 = A. lingualis; 4 = A. lingualis dorsalis; 5 = A. sublingualis; 6 = A. profunda linguae; 7 = Rr. verticales; 8 = submucosal net; 9 = Rf. perforantes ; 10 = subpapillary net; 11 = vasa papillares; 12 = muscular branches of A. lingualis profunda; 13 = R. communicans superficialis; 14 = R. communicans profundus; 15 = unpaired branch of Rr. communicantes superf.; 16 = muscular branches of R. communicans prof.; 17 = A. submentalis; 18 = V. comítans N. hypxglossi. I = Contralateral anastomoses at the subpapillary net; II = contralateral anstomoses of the Aa. profunda linguae; III = contralateral anstomoses for the Rr. perforantes; IV = contralateral anastomoses of the Rf. communicantes superf. and prof. [Görzε and LIER5E, 1969]. In man, variations of the branching of the lingual artery have been described. Thus, though the lingual artery branches from the external carotid artery in most cases, it may also branch from the superior thyroid artery or from one of the other posterior branches [Smile et al., 1971]. The sublingual artery may origin from the facial artery [AKiyAiA, 1970, HAMPARIAN, 1973].
Anastomoses Arteriovenous anastomoses which form direct communications between arteries and veins are widespread in the body [LIEBow, 1963]. In the tongue such anastomoses have been described by BRowN [1937], DAτELOω [1951],
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Veins The veins run parallel to their corresponding arteries. The deep lingual vein divides in two in the anterior part of the tongue; the two veins then join to form a single vessel. It then proceeds caudally along the ventral side of the corresponding artery.
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PRICHARD and DANIEL [1953] and OHLSSON [1971]. The vessel walls are thick, and the media contains smooth muscle cells and epithelioid cells in large numbers [PRICHARD and DANIEL, 1953]. They have a rich nerve supply [BRowN, 1937] which also seems to include a large sensory portion. In the dog they seem to be located both in the subpapillary plexus and in the lingual papillae [DABELOW, 1951]. The tongue of sheep and goat are similar, in this respect, to that of the dog [PRICHARD and DANIEL, 1953]. In man they are seldom found or absent, according to Μ Rκ [1941] and DABELOW [1951]. In the tongue of the rabbit, guinea pig and cat, CLARA [1927] and DABELOW [1951] found no arteriovenous anastomoses. SAVIY et al. [1971] describe anastomoses between the arteries in man. They found them to be predominant in the tip and the posterior part of the tongue. DENIsOVA [1973] observed many anastomoses and describes three types, termino-terminal, termino-lateral and lateral-lateral.
Blood Flow of the Tongue The rich vascularization that has been described here indicates that the blood supply to the tongue is more abundant than to most other muscular organs of the body. Available data also indicate that the tongue receives more blood than can be expected from its size. MEYER [1970] estimated by the use of isotopes that the flow to the tongue of the dog is about 0.22 ml/ min/g. In the cat ALM and BILL [1973] and HALES [1973] determined the flow to be 0.29 ml/min/g. Observations in the rat [HELLEKANT, 1971b] indicate that the flow varies between 0.2 and 0.3 ml/min/g. This is only about 50 of the flow to the dental pulp of the dog, 0.54 ml/min/g [MEYER, 1970], but is considerably more than the value obtained from skeletal muscle at rest, 0.03 ml/min/g [MELLANDER and JoHANSSON, 1968].
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Connections between the Right and Left Side GUTZE and L'ERSE [1969] state that there are few connections between the vessels of the left and right side except in the tip and the very posterior part of the tongue. In the tip there seems to be connections between the left and right side. Thus in man HUBIER [1968] found contra-lateral anastomoses in the tip in 11 preparations out of 17. He also noticed faint connections in the back of the tongue. In all he found anastomoses in 15 out of 17 cases. Intravital staining through one lingual artery in the rat indicates that the tongue is unilaterally supplied to a large extent [HELLEKANT, 1971 a] though some staining could be observed on the contralateral ventral side of the tip too.
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The vascular bed of the tongue can be used for the diagnosis of circulatory disturbances [DAVms and LANDAU, 1966; MERLEN et al., 1973]. Thus, Görzε [1972] observed changes correlated with diabetes mellitus. Similarly, TsuYA et al., [1971] found a significant correlation between the doses of radiation from the atomic bomb and changes in the circulatory pattern of the lingual mucosal capillaries on the other. Effect of Arterial Occlusion It is generally known that hemorrhage from the tongue is difficult to stop. Observations in the dog by SHEPHERD et al. [1971] show that occlusion of the ipsilateral lingual artery does not stop bleeding from the deep lingual artery. Simultaneous clamping of the ipsilateral lingual and external carotid arteries slows the bleeding from the deep lingual one, but does not arrest it. Only when both the common carotid arteries are occluded does the blood flow stop. The effect of permanent occlusion of some of the vessels to the tongue has also been described. Thus, Görzε and L'ERSE [1969] unilaterally occluded the lingual artery in one rabbit and the external carotid in another for 1 week. They found no light microscopical difference between the two sides. These observations indicate that the occluded side of the tongue, through the anastomoses described, receives enough blood to maintain its morphological characteristics. Further, the vascularization seems to be rich enough to prevent tissue damage in spite of extensive atherosclerosis both in man [DREIZEN et al., 1974] and in rabbit [DREIZEN et al., 1971]. This rich vascularization also underlies the advice of NIcHOLs and CurluG-r [1971] that the tongue be used for injections of emergency drugs. They observed little difference in latency between the maximum effects of intravenous or intralingual injections in monkeys. However, with regard to the function of the taste receptor cells, experiments in the anesthetized rat [HELLEKANT, 1971 a] show that after the ipsilateral carotid artery is occluded the blood flow through only the contralateral external carotid artery is too small to maintain the taste sensitivity of the fungiform taste buds.
Topographical Orientation There are four different kinds of papillae on the mammalian tongue, the filiform, the circumvallate, the foliate and the fungiform papillae. The
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Circulation of the Lingual Papillae
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Fig. 2. Schematic drawing of the vascular network of the filiform papilla in man. An artery (A) and a vein (V) run parallel to the surface in the lamina propria mucosae. A vertical branch (a) is given off below the papilla. The papilla empties through the central venous sinus (vs) which shows a constriction of its wall at the point of entry into the vein (V). pl = Peripheral veins; ak = arterial and vk = venous capillaries in the secondary papillae (SP); o = oral; and p = pharyngeal directions [KUNZE, 1969].
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last bear the taste buds. The filiform papillae cover the dorsum and the sides of the tongue. The fungiform papillae occur principally on the tip and lateral anterior part of the tongue but are also scattered over the dorsum. They bear taste buds on their oral surface. The circumvallate papillae are found in the posterior part of the dorsum. Their number varies from one species to another, but is generally less than five, in man up to 15 [TUCKERΜΑΝ, 1890]. The papilla is surrounded by a groove (fig. 3) the walls of which contain the taste buds. The foliate papillae are situated in the posterolateral part of the tongue in front of the anterior pillars of the soft palate. Their
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taste buds are located in their sides. The circulation of these different papillae will now be described in some detail. The subpapillary plexus described above supplies the papillae.
Fig. 3. Vascular network of the circumvallate papilla in the dog. m = Blood vessels of muscularis; a = arteries; v = veins; k = capillaries. Indian ink injection [DABELOW, 1951].
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Filiform Papillae The filiform papillae constitute the majority of the papillae on the tongue and are the only ones which have no taste buds. In man there are about 500/cm2 [KUNZE, 1969]. Their shape varies from a simple curved coneshaped form in the cat to a rather complicated one in man, as shown in figure 2. The drawing shows that each filiform papilla in man carries about ten secondary papillae. It also illustrates the blood supply. Α small artery, parallel to the surface of the tongue, gives off a branch that enters the primary papilla and then divides. The lumina of the vessels entering the secondary papillae are only half or a third the diameter of those leaving them. The vein that drains the papilla shows a constriction (the arrow in figure 2) which has several contractile elements in its wall [KUNZE, 1969]. In the dog the vascular supply of the filiform papillae occurs in two forms, a more simple one which also shows arteriovenous anastomoses, and a more complicated variant which occurs most abundantly in the vicinity of the circumvallate papillae [DABELOW, 1951].
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Circumvallate Papillae The circumvallate papillae receive their blood supply from the large vessels which arise in the muscularis (fig. 3). The vessels give off numerous capillary loops which rise towards the surface of the papilla. The loops decrease in height near the bottom of the groove. The tissue peripheral to the groove is also supplied by a plexus of vessels. This plexus faces the groove and is somewhat flattened.
Fig. 4. Α cross-section of the posterior margin of the foliate zone of the rabbit tongue. The arrow points to loops in the capillary bed beneath the gustatory epithelium. The large sinusoidal vessel which drains the foliate zone is apparent at the extreme right. The central sinusoidal vessels of the papillae and the subpapillary sinuses are also shown. Indian ink injection [ELLIS, 1959].
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Foliate Papillae In the rabbit the circulatory system of the foliate papillae consists of arterioles, a bilateral system of capillary loops, shunts and anastomosing sinusoids, which are linked to the venous system [ILLIS, 1959]. The arterioles which enter the papilla divide into a series of capillary loops at the level of the taste buds (fig. 4). These capillaries converge toward the superior
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surface of the papilla above the level of the most superficial taste buds, curve toward the surface epithelium and then reverse their direction, forming terminal capillary loops. Finally, as venules they veer toward the center and base of the papilla where they join the large sinuoids which are found centrally in the rabbit but not in primates. These sinusoids are primarily associated with the von Εbner's glands. Even the deep-lying portions of these glands are surrounded by them [ELLIS, 1959]. The taste buds of the papillae are supplied by blood from the capillary loops and not by the sinusoidal system. The capillary supply of these taste buds is not so rich as those of the fungiform and vallate papillae, according to ELLIS [1959]. In the dog [SCHUMACHER and NIKOLOl, 1973] the capillaries within the papillae form a plexus close to the epithelium. They are supplied with one or two precapillary vessels and the blood leaves the papilla through a central vein.
Circulation of the Taste Buds The receptor cells, which transduce the influence of a chemical into a taste, are localized in certain structures, the taste buds. Their localization has already been described. The taste buds in the anterior two thirds of the tongue are innervated by fibers from the chords tympani proper nerve, which is a branch of the facial nerve. Those of the posterior part are supplied by fibers from the glossopharyngeal and vagal nerves. However, those of the foliate papillae may receive fibers from both the chords tympani proper and facial nerves [YAMAMoro and KAWAMURA, 1975]. The message from the taste receptor cells to the brain can be recorded as nerve impulses from these nerves. These impulses provide a good indication of the function of the taste cells. If the blood flow through the lingual arteries is cut off, the chords tympani response disappears within a few minutes [HELLEKANT, 1971a]. This deterioration of response to taste stimulation cannot be attributed to any
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Fungifοrm Papillae In man there are about 100/cm 2 fungiform papillae in the tip and 50/cm2 in the middle of the tongue [KUNZE, 1969]. These papillae have a rich blood supply. In the dog, DABELOW [1951] describes two types with somewhat different vascular pattern (fig. 5). The capillaries entering the base of each papilla are arranged radially. Towards the surface they converge and form rich anastomoses between the taste buds. The taste buds of the fungiform papillae have a more elaborate capillary bed than those of the other types [ELLIS, 1959; SCHUHMACHER and NIKOLOl, 1973].
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effects on the nerve fibers, because their excitability is maintained for a much longer time. The shortness of this period indicates a rather high metabolic rate of the taste receptor cells. Among the possible causes for this effect, oxygen deficit has been suggested as the most important one [HELLEKANT, 1971b]. These observations were obtained in rat. In man, STEINER [1971] reported decreased taste sensitivity in cases of acrocyanosis and other types of peripheral circulatory disturbances, which can be detected by the method of biomicroscopy. The taste sensitivity can not only be affected by decrease of blood flow, but also by increase of blood flow. Thus, the taste response can be enhanced by such an increase [HELLEKANT, 1971b].
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Fig. 5. The two main types of vascular net in the fungiform papillae of the dog. a = Arteries; v = veins; k = capillaries. Indian ink injection [DABELOW, 1951].
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Vascular Innervation of the Tongue The concept that the blood vessels of the tongue, like other structures innervated by the autonomic nervous system, have a reciprocal cholinergic and adrenergic innervation, was proposed by BAYLISS [1923]. Since then it has been established that: (1) there exist vasoconstrictor nerves. These nerves are widely distributed, they are sympathetic in origin and they are exclusively adrenergic; (2) there exist vasodilator nerves which are parasympathetic in origin. They are cholinergic and supply certain regions like the genitalia and probably also the tongue, which is of interest in this context; (3) there are vasodilator nerve fibers to skeletal muscles in certain species [BoLΙΙΙE and FUXE, 1970]. These nerves are of sympathetic origin but cholinergic. ERIcΙ et al., [1952], ECCLES and WALL'S [1974] suggest that such fibers may innervate the tongue in the cat. Vasoconstrictor Nerves to the Tongue It is established that the tongue receives adrenergic sympathetic vasoconstrictor fibers, which when stimulated, increase the resistance of the vessels in the tongue, as shown in the left record on figure 6. In this experiment the tongue of the rat was perfused with its own blood through an external loop while the blood flow and resistance of the lingual artery were recorded.
symg
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Fig. 6. The effects of stimulation of the ipsilateral sympathetic nerve to the tongue of the rat (left) and of the chorda tympani nerve (right) on the vascular resistance in the tongue are shown. The records were obtained during unilateral perfusion of the tongue with the rat's own blood. The upper trace shows the perfusion pressure in the lingual artery, the middle trace the flow rate and the bottom one the blood pressure in one femoral artery. The horizontal bars illustrate electrical stimulation of the peripheral parts of the nerves in question [HELLEKANT, 1972].
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0
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Vasodilator Nerves to the Tongue The existence of cholinergic parasympathetic vasodilator fibers to the tongue has been disputed, though it is well known that electrical stimulation of the peripheral part of the chords tympani nerve, whose efferent portion is of parasympathetic origin, decreases the vascular resistance in a manner shown in the right record of figure 6. It seems that it is generally thought that this decrease is caused by impulses which are elicited in sensory fibers and which travel in an antidromic direction to the tongue. However, this explanation is unlikely to be correct. This is shown by the following experiment. The cell bodies of the sensory fibers in the chords tympani proper nerve are situated in the geniculate ganglion [VILLIGER, 1964]. If the facial nerve is cut between this ganglion and C'S all other fibers in the chords tympani proper will degenerate except the sensory ones. After such degeneration stimulation of the chords tympani proper causes no dilatation of the vessels in the tongue. Figure 7 gives an example of this. In figure 7 the vascular resistance of the tongue was recorded in a similar way as in figure 6. The record shows that stimulation of the chords tympani proper nerve with 40 and 70 Hz, respectively, which in a normal animal gives a strong vasodilation, had no effect on the vascular resistance of the tongue. We have repeated these experiments in a number of animals with similar results. In these animals the sensory innervation remain. This can be demonstrated by recording the response to taste stimulation or mechanical stimulation. Thus it seems that antidromic impulses in the sensory fibers cannot explain the well-known vasodilation in the tongue [Ετττcτ and Uvνλs, 1952 ; ECCLES and WALL'S, 1974]. Further, efferent nerve impulse [FIELLEKANT, 1971c] have been recorded in the chords tympani proper nerve. Some of this impulse activity seems to be unrelated to salivary secretion, because it occurs, and can change, without causing secretion [HELLEKANT and HAGSTROM, 1974]. This activity may be related to food intake, e.g., stomach distension [HELLEKANT, 1971d] decreases it. Finally, a widespread adrenergic as well as cholinergic innervation in and along the arteries, arterioles and metaarterioles in the tongue has been
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The ipsilateral sympathetic nerve was then electrically stimulated at the level of the superior cervical ganglion during the time periods indicated by the signal. This resulted in an increased overall vascular resistance in the tongue. In the cat, ALM and BILE, [1973] found a 80 % reduction of blood flow through the tongue after 1 min of stimulation of the cervical sympathetic chain.
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0
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Fig. 7. The effect of stimulation of only the sensory portion of the chords tympani proper nerve on the vascular resistance of the tongue was recorded in a similar way as in figure 6. The frequency of the electrical stimulus applied is shown. No effect on the vascular resistance was recorded by the antidromic impulses. demonstrated histochemically by SCHEICK and BADAWI [1968]. These authors conclude that the number of cholinergic fibers was larger in the tongue than, for example, in the skeletal muscles or the gastrointestinal tract. More direct evidence is perhaps presented by SIGGINS and WEITSEN [1971] who describe pronounced vasodilation after microelectrode stimulation of associated terminal nerves. This vasodilation was still elicited after 2 days of topical treatment with 6-hydroxydopamíne. The cholinergic nature of these fibers were established with histochemical technique. The thiocholine method of KARNOVSKY [1964] and the selective methylene blue technique of Rτcκλι DSON [1969] were used. The observations of SIGGINS and WEITSEN [1971] were obtained in the retrolingual membrane of the frog but it is likely that if cholinergic vasodilation exists in this species it will exist in higher ones also. Similar observations were reported by BERMAN et al. [1972]. In mammals, FAAZGERALD and ALEXANDER [1969] have presented further evidence for the existence of a cholinergic parasympathetic nerve supply to the vessels in the tongue. They studied intramuscular ganglia in the tongue of the cat. They conclude that in the anterior two thirds of the tongue these ganglia can be assigned with confidence to the chords-lingual nerve. The ganglia did not innervate glandular tissue of the tongue. Rather, the fine nerve fibers from these ganglia were traced to nerve plexuses on the walls of the arteries with an external diameter of 150-300 Μm.
This article describes the gross anatomy of the vessels which supply the mammalian tongue. It shows that there is a rich vascular supply. Available data indicate that the lingual
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Summary
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papillae are supplied with a true capillary circulation, which is more abundant in the papillae containing taste buds. The vessels of the tongue are innervated by adrenergic sympathetic vasoconstrictor fibers and it is also very likely that a cholinergic parasympathetic vasodilator influence exists.
References
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}{ELLEKANT
The Blood Circulation of the Tongue
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Dr. G. HELLEKANT, Department of Physiology, Veterinärhögskolan, HIC, S-750 07 Uppsala (Sweden)
