The Course, Relations and Distribution of the Inferior Alveolar Nerve and Its Branches in the Cat

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1 The Course, Relations and Distribution of the Inferior Alveolar Nerve and Its Branches in the Cat P. P. ROBINSON Department of Physiology (Oral Biology), The Medical School, University Walk, Bristol BS8 1 TD, England ABSTRACT The course, relations and distribution of the inferior alveolar nerve and its branches in the cat are described. The nerves have been studied by dissection, histologically and by using electrophysiological techniques. Dissection revealed a basic pattern on which some individual variation was superimposed. The inferior alveolar nerve has three branches supplying the alveolar process (alveolar branches), one branch supplying the canine and incisor region (caninelincisor branch) and four mental branches (posterior, main and 2 anterior). Fibres supplying the teeth were found in all except the mental branches. Pulpal, periodontal and buccal gingival margin fibres from an individual tooth generally travelled together, but often in more than one branch. Branched axons supplying both tooth pulp and an area of mental skin were found. The axons branched at the point of separation of the appropriate mental nerve from the main trunk. A cutaneous midline overlap of 1-2 mm was found, but there was no transmedian innervation of tooth pulps. The inferior alveolar nerve, a branch of the mandibular division of the trigeminal nerve, contains afferent fibres from the ipsilateral lower lip, areas of oral mucous membrane, and mandibular teeth. There is also evidence that sympathetic vasoconstrictor fibres travel within this nerve (Anderson and Linden, '77; Ogilvie, '69). Thomas ('46) examined histologically the inferior alveolar nerve in 13 cats and noted the presence of up to 17 separate nerve bundles within the canal in the region of the first premolar, although many of these bundles consisted of only a few fibres. No information was obtained to establish which tissues were innervated by the individual branches. The present study was undertaken to provide detailed information on the course and distribution of the inferior alveolar nerve and its branches. This information provides a basis for electrophysiological experiments concerning sensory mechanisms of the teeth and their surrounding structures, for which the cat is a commonly used animal model. This information was also essential for subsequent studies on the effects of denervation of selected oro-facial tissues. METHODS The inferior alveolar neurovascular bundle ANAT. REC. (1979) 195: was examined in 10 fresh, unfixed specimens by dissection under a surgical microscope. The outer plate of the mandible was removed with dental burs and the connective tissue sheath surrounding the nerves and vessels was divided. The course and relations of these structures were noted, and the branching points of the nerves recorded in relation to the roots of the teeth. In four animals the neurovascular bundle was examined bilaterally. The common carotid arteries and external jugular veins were injected with pigmented latex (Tompsett, '70) shortly after death. This made it possible to distinguish between blood vessels and fine nerve bundles. In 14 further preparations in 10 cats action potentials were recorded from the inferior alveolar nerve and its branches during stimulation of various tissues, to ascertain the distribution of the nerve bundles. Adult cats weighing kg with fully erupted permanent teeth were used. Anaesthesia was induced using intraperitoneal sodium pentobarbitone (42 mg/kg) and maintained by doses of 3 mgkg given as required through a cannula in the great saphenous vein. Body temperature was maintained at t 0.2"C Received Feb. 6, '79. Accepted Apr. 24, '

2 266 P. P. ROBINSON by an electric blanket controlled from a peritoneal thermistor. The trachea was cannulated and the head stabilised by means of a bar fixed to the frontal bone with 2 self-tapping screws. The inferior alveolar nerve was exposed and dissected in a pool of warm light liquid paraffin B.P. enclosed by skin flaps raised from over the mandible. Compound action potentials were recorded from the inferior alveolar nerve and its branches, using bipolar platinum wire (0.15 mm diam.) electrodes and a Tektronix 2A61 preamplifier. Mechanical stimuli were applied to shaved skin and to mucous membrane using a blunt probe and to the periodontal tissues of the teeth by pressing on their crowns. Electrical stimuli were applied to the pulps of the teeth. Antidromic action potentials were also recorded from the pulps of the teeth during stimulation of each of the nerve branches. For recording from the canine teeth, the electrodes used were those described by Horiuchi and Matthews ('74). For the incisors, premolars and molars, which were examined in 7 preparations, the electrodes consisted of mm diameter silver wire leads placed into cavities filled with a mixture of silver powder and silver chloride (Horiuchi and Matthews, '74). Two cavities were cut into dentine in each tooth, one near the tip of the cusp and the other near the gingival margin. The cavities were prepared in the premolar and molar teeth using an inverted cone size lh bur rotating slowly under Ringer's solution, and in the incisors using a hand-rotated 0.3 mm diameter twist drill also under Ringer's solution. The pulpal origin of responses recorded with these electrodes was confirmed by the observation that they disappeared after sectioning the pulp in the root of the tooth with a chip of razor blade. These electrodes were also used for pulpal stimulation. Electrical stimuli of up to 10.0 V and 0.1 ms duration were used for nerve and pulpal stimulation. In 3 further animals, electrodes were placed in both lower canine teeth and all 6 incisors, and the inferior alveolar nerve was examined bilaterally for evidence of transmedian innervation of the pulps. In 10 other experiments evidence of transmedian innervation of the first incisor only was investigated. One animal was perfused with 4% formaldehyde in Millonig's phosphate buffer. The right side of the mandible was removed and divided transversely into 4 blocks which were de- calcified in 10% E.D.T.A. and dehydrated in alcohol. The blocks were then double embedded in low viscosity nitrosecellulose and wax. Transverse sections (10 wm) were cut on a sledge microtome and the sections stained with haematoxylin and eosin. The sections provided details of the undisturbed relationships of the structures in the mandibular canal. RESULTS At the mandibular foramen the inferior alveolar nerve was a single bundle with the inferior alveolar artery and vein lying inferior to it. Within the ramus the vessels crossed over the lateral aspect of the nerve to lie superior to it with the vein or veins usually lying lateral to the artery. Within the mandible the nerve divided into several branches which conformed to a basic pattern with some individual variation. Three branches supplied the alveolar process (alveolar branches) ; one supplied the canine and incisor regions (canine/ incisor branch); and there were four mental branches (posterior, main and 2 anterior). Interconnecting fibres were often seen between these principle branches. The origins of the branches in relation to the teeth are shown in figure 1. These are mean positions and varied from these points by up to 6 mm in any 1 specimen. There was no apparent bilateral symmetry. Fibres from an individual tooth and the adjacent buccal gingival margin travelled together. Thus, a branch described as carrying afferents from a particular tooth contained pulpal, periodontal and buccal gingival margin fibres. Each branch will now be considered separately. Posterior alveolar This was the most proximal branch of the main trunk, splitting from its superior aspect approximately 5 mm anterior to the mandibular foramen. It was approximately 0.1 mm in diameter and contained afferents from the molar, second premolar and occasionally first premolar teeth. Middle alveolar This branch (-0.1 mm diameter) left the superior aspect of the main trunk beneath the distal root of the molar tooth. It passed for- ' In a preliminary communication (Robinson, '78) the posterior, middle and anterior alveolar nerves were referred to as first, second and third alveolar nerves respectively.

3 INFERIOR ALVEOLAR NERVE IN THE CAT 267 Canine/ Incisor Posterior Mentol 0 5cm Fig. 1 Branches of the inferior alveolar nerve within the mandibular canal. This diagram is to scale ex. cept that the nerve bundles have been separated and their diameters enlarged for clarity. The main and posterior mental nerves leave through the main mental foramen (MMF) and posterior mental foramen (PMF), respectively. The level of the histological sections in figure 4 are indicated. a b C Fig. 2 Receptor fields to mechanical stimulation: (a) anterior alveolar, (b) posterior mental, (c) main mental and (d) anterior mental nerves. The dotted line represents the midline. The lip has been displaced downwards to reveal the mucous membrane of the buccal sulcus.

4 268 P. P. ROBINSON Fig. 3 Responses recorded in the first incisor (R) during electrical stimulation of the main mental nerve (S) at its foramen. In each record five successive sweeps have been superimposed. A Response in the first incisor with the inferior alveolar nerve sectioned within the ramus - section a. B Response in the first incisor with the inferior alveolar nerve sectioned at the branching point of the main mental nerve and a bundle supplying the first incisor - section b. wards high in the inferior alveolar canal towards the first premolar which it supplied. In half of the specimens it also carried fibres from the third incisor and canine teeth. Anterior alveolar This left the superior surface of the main trunk in the region of the mesial root of the molar tooth and passed anteriorly in the medial part of the canal, often medial to the inferior alveolar artery. It was approximately 0.15 mm in diameter and supplied the canine and third incisor teeth. It also carried mechanoreceptor afferents from the skin and mucous membrane adjacent to the canine and third incisor (fig. 2a). Electrical stimulation of this nerve produced a large compound action potential in the canine tooth, the amplitude of which was approximately 30% of that recorded with stimulation of the whole inferior alveolar nerve trunk at the mandibular foramen. Occasionally it carried fibres from the first and second incisors and first premolar teeth. Posterior and main mental These branches left the lateral aspect of the main trunk, the posterior mental (-0.2 mm diameter) leaving beneath the distal root of the molar, and the main mental (-0.25 mm diameter) beneath the distal root of the second premolar. They left the mandible through the posterior and main mental foramina, respectively, to supply the skin of the chin and lip and the mucous membrane on the labial side of the alveolar process including the buccal gingival margin. The areas innervated by these nerves overlapped markedly, the total extent of their receptor fields being from the midline to near the corner of the mouth (figs. Fig. 4 Transverse sections of the mandibular canal, at the levels indicated in figure 1, viewed with the medial aspect of the canal on the right side of the section. x 50. a Only the main trunk and posterior alveolar nerves are present at this level. b The posterior alveolar nerve has divided into many small bundles, some within bony canals. The middle alveolar nerve has left the main trunk from its superior surface. c The posterior mental nerve has left the lateral surface and the anterior alveolar the superior surface of the main trunk. d The main mental nerve has left the lateral surface of the main trunk; in this specimen it is in two bundles. e The main mental nerves have passed upwards in the canal towards the main mental foramen. The main trunk has divided into its terminal branches; the anterior mental and canine incisor nerves.

5 INFERIOR ALVEOLAR NERVE IN THE CAT Abbreviations T, Inferior alveolar main trunk PA, Posterior alveolar nerve MA, Middle alveolar nerve AA, Anterior alveolar nerve PM, Posterior mental nerve MM, Main mental nerve AM, Anterior mental nerve CI, Caninefincisor nerve Figure 4

6 270 P. P. ROBINSON 2b,c). In their distribution outside the mental foramina, these branches carried no pulpal fibres. However, occasionally a few pulpal afferents joined these branches within the mandible. In four specimens evidence for fibres branching to supply both tooth and skin or mucous membrane was sought. The posterior and main mental nerves were stimulated just outside the mental foramina. The central connections of the nerves remained intact and recordings were made from nearby teeth. In two preparations an antidromic action potential was recorded from a tooth in response to orthodromic stimulation of a mental nerve. This response was not affected by sectioning the inferior alveolar nerve in the ramus. When the level of section was moved progressively forwards, however, a point was reached at which the response was abolished. In both preparations the response disappeared only when the position of section coincided with the separation of the mental nerve from the main trunk. In one preparation the branching involved the canine pulp and the posterior mental nerve and consisted of two all-or-none components. These were lost when the nerve was cut at fractionally different positions. The other was a single all-or-none response recorded in the first incisor when the main mental nerve was stimulated (fig. 3). Anterior mental The main trunk of the inferior alveolar nerve divided beneath the mesial root of the first premolar to form two terminal branches, the caninelincisor nerve (-0.15 mm diameter) and anterior mental nerve (-0.15 mm diameter). The anterior mental passed inferior to the apex of the canine and divided, leaving the sloping anterior surface of the mandible through superior and inferior anterior mental foramina. It supplied a central strip of skin and mucous membrane, extending from the third incisor region to 1-2 mm across the midline (fig. 2d). It contained no pulpal or periodontal afferents. Caninehncisor This branch carried fibres from all three incisors and the canine. In some animals the canine fibres and incisor fibres left in separate bundles with the canine fibres leaving the main trunk more proximally. Transmedian innervation The cutaneous innervation in the anterior mental nerve crossed the midline by 1-2 mm, but there was no evidence of transmedian innervation of tooth pulps. Averaging procedures could produce an apparent shortlatency response to nerve stimulation in the contralateral first incisor. This remained unchanged after section of the root pulp with a chip of razor blade. These potentials were apparently picked up from nerves outside the tooth (Matthews and Lisney, '78). No response could be recorded in the contralateral inferior alveolar nerve when stimuli of 10.0 V and 0.1 ms duration were applied to the pulps of the teeth. Histology The transverse sections of the mandible revealed the undisturbed relationships of these branches and also the presence of occasional very small bundles of fibres not readily identifiable during dissection (fig. 4). The continuity of each branch between the levels shown was established by examination of successive sections. Nerve bundles often divided to form two or more sub-bundles in close apposition. (See main mental nerve fig. 4d.l DISCUSSION These results provide information not previously available on the detailed anatomy of the inferior alveolar nerve and its branches in the cat. All of the branches contained fibres from two or more adjacent tissues; for example, the anterior alveolar branch contained afferents from pulp, periodontal ligament, mucous membrane and skin. The nerves supplying one tooth did not all travel in one branch of the main trunk; for example, canine fibres were present in the caninelincisor, anterior alveolar and occasionally middle alveolar branches. There was also marked overlap in the distribution of the mental branches. The histological material revealed several very small branches that were not found in the microdissections. The distribution of these was not established. Lisney and Matthews ('78) demonstrated that some inferior alveolar nerve fibres branch to supply mucous membrane and the pulp of a nearby tooth. Branched fibres of this type would account for the action potentials sometimes recorded from teeth during stimulation of a mental nerve. In the present experiments the branching point of the axons was found to be at the point of separation of the mental nerve from the main trunk. The intramandibular course of the inferior alveolar nerve in man has been studied by dissection in cadavers by Olivier ('271, Starkie

7 INFERIOR ALVEOLAR NERVE IN THE CAT 271 and Stewart ('31) and by Carter and Keen ('71). Olivier ('271, who dissected 50 specimens, found a single nerve bundle within the canal in 66% of his cases, a result substantiated by Carter and Keen ('71). Starkie and Stewart ('31) found that the nerve divided into several branches immediately after entering the mandibular canal to form what they termed an alveolar plexus which supplied the teeth and alveolar process. The pattern described by Starkie and Stewart suggests some similarities between the anatomy of the nerve in man and cat. A cutaneous midline overlap of 1-2 mm was found. This was much less extensive than that seen in the perioral region of cats by Darian- Smith et al. ('65). No evidence could be obtained for fibres crossing the midline to supply contralateral teeth, either by dissection or electrophysiological experiments. Dissection of very small fibres in the region of the fibrous symphysis was, however, difficult. A similar result was also obtained in electrophysiological experiments by Matthews and Lisney ('781, although some evidence has been reported (Anderson and Pearl, '74; Pearl et al.,'77) which is claimed to demonstrate a transmedian innervation extending as far as the canine tooth in cats. Starkie and Stewart ('31) demonstrated fibres crossing the midline to supply teeth in the incisor region in four human specimens. These authors were unable to find evidence of transmedian innervation of teeth in other species, including the cat. In man there is also evidence for transmedian innervation of the pulps of central, and occasionally lateral incisors, based on their failure to become anaesthetised with unilateral regional anaesthesia (Stewart and Wilson, '28; Rood, '77). This apparent difference between cat and man may be related to the mobile fibrous midline symphysis present in the cat. It is also possible that the incisor tooth pulps receive a secondary innervation via an alternative pathway such as the lingual or mylohyoid nerves (Stewart and Wilson, '28; Carter and Keen, '71) or the cervical plexus (Sutton, '74). These possibilities are being examined in a further series of experiments. ACKNOWLEDGMENTS I should like to thank Professor D. J. Anderson and Dr. B. Matthews for their advice and encouragement during the course of these experiments. I am also grateful to Mr. I. Rogers for the preparation of the histological sections. This work was carried out during the tenure of a Medical Research Council Training Fellowship. LITERATURE CITED Anderson, D. J., and R. W. A. Linden 1977 Sympathetic modulation of intraoral mechanoreceptor activity. J. Dent. Res., 56: D125 (Abstract). Anderson, K. V., and G. S. Pearl 1974 Transmedian innervation of canine tooth pulp in cats. Exp. Neurol., 44: Carter, R. B., and E. N. Keen 1971 The intramandibular course of the inferior alveolar nerve. J. Anat., 208: Darian-Smith, K., P. Mutton and R. Proctor 1965 Functional organization of tactile cutaneous afferents within the semilunar ganglion and trigeminal spinal tract of the cat. J. Neurophysiol., 28: Horiuchi, H., and B. Matthews 1974 Evidence on the origin of impulses recorded from dentine in the cat. J. Physiol., 243: Lisney, S. J. W., and B. Matthews 1978 Branched afferent nerves supplying tooth pulp in the cat. J. Physiol., 279: Matthews, B., and S. J. W. Lisney 1978 Do primary afferents from tooth pulp cross the midline? Brain Res., 258: Ogilvie, R. W The vasomotor innervation of the cat's lower right canine tooth pulp. Anat. Rec., 163: 237 (Abstract). Olivier, E Le canal dentaire inferieur et son nerf chez adulte. Annls. Anat. path. Anat. norm. med-chir., 4: Pearl, G. S., K. V. Anderson and H. S. Rosing 1977 Anatomical evidence revealing extensive transmedian innervation of feline canine teeth. Exp. Neurol., 54: Robinson, P. P The inferior alveolar nerve in the cat. J. Dent. Res., 58: 1274 (Abstract). Rood, J. P The nerve supply of the mandibular incisor region. Brit. Dent. J., 143: Starkie, C., and D. Stewart 1931 The intramandibular course of the inferior dental nerve. J. Anat., 65: Stewart, D., and S. L. Wilson 1928 Regional anaesthesia and innervation of the teeth. Lancet, 215: Sutton, R. N The practical significance of mandibular accessory foramina. Aust. Dent. J., 19: Thomas, B. 0. A An analysis of the inferior alveolar and mental nerves in the cat. J. Comp. Neur., 84: Tompsett, D. H Anatomical Techniques. Second, ed. E. & S. Livingstone, London.