auriculo-temporal nerve. The secretory response to various cholinesterase
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1 Quarterly Journal of Experimental Phy8iology (1974) 59, THE SECRETORY INNERVATION OF THE PAROTID GLAND OF THE CAT: AN UNEXPECTED COMPONENT. By J. EKSTROM and N. EMMELIN. From the Institute of Physiology, University of Lund, Sweden. (Received for publication 24th May 1973) After section and degeneration of the auriculo-temporal nerve in cats, parotid secretion could still be elicited by injecting eserine into the gland, by application of citric acid to the tongue or by electrical stimulation of afferent oral nerves, and choline acetyltransferase activity could be demonstrated in extracts of the gland. The secretion obtained was not mediated via sympathetic nerves, although electrical stimulation of such nerves caused some secretion from most glands. Cholinergic secretory fibres mainly or wholly responsible for the remaining secretion after section of the auriculo-temporal nerve were traced along the internal maxillary artery. It has been known for a long time that the secretory innervation of the parotid gland is more complicated in humans and dogs than the usual textbook accounts of it [see Babkin, 1950]. In dogs, for instance, some secretion can be elicited reflexly even after section of the auriculo-temporal nerve, and additional cholinergic secretory fibres were recently found in close connection with the internal maxillary artery [Holmberg, 1971]. Some observations in cats suggest that in them too secretory fibres may travel to the parotid gland outside the auriculo-temporal nerve. The secretory response to various cholinesterase inhibitors was found to be greatly diminished after section and degeneration of the auriculo-temporal nerve, but it did not entirely disappear [Emmelin and Stromblad, 1958a], and after this operation some choline acetyltransferase activity remained in the gland [Nordenfelt, 1963]. In histochemical studies Garrett [1966] could still detect some cholinesterase-positive nerves in association with the acini 6 days after sympathectomy and avulsion of the auriculotemporal nerve. Experiments on the effect of denervation and reinnervation of the parotid gland of the cat [Ekstr6m and Emmelin, 1973] showed that some secretion could be elicited reflexly shortly after section of the auriculo-temporal nerve. These observations were the starting-point of the present investigation. Not only had unknown parasympathetic nerves to be considered, but also the sympathetic innervation; it is generally agreed that in dogs -stimulation of sympathetic nerves causes no parotid secretion, but in cats this is a matter of dispute. No parotid secretion on sympathetic stimulation was obtained by v. Wittich [1867] whereas Navrocki [1868] usually saw some secretion and Bradford [1887] described the response as copious. Among more recent investigators Richins and Kuntz [1953] found little or no secretion. Some secretion was recorded by Str6mblad [1955], Ohlin and Stromblad [1958], Cragg [1965] and Nordenfelt [1965], but Fritz and Botelho [1969] obtained neither flow of saliva nor secretory potentials when the cervical sympathetic trunk was stimulated. 11
2 12 Ekstrom and Emmelin METHODS In cats under ether or light buthalitone anaesthesia (2-5 mg/kg intracardially) the right parotid duct was cannulated at its orifice and salivary secretion was induced by pouring a solution of citric acid (10%) on the tongue. Drops of saliva were recorded on a smoked drum; the cannulae used formed about 70 drops from 1 ml. of distilled water. Buthalitone (20 mg/kg) was then given to produce deep anaesthesia and hexamethonium (5 mg/kg) was added. The secretory effects of methacholine (0 5, 1.0 and 2-0 pg/kg) intracardially and of eserine (200,g), injected through the duct into the gland, were recorded. The right auriculo-temporal nerve was cut and in some animals the right superior cervical ganglion was excised as well. After 5 or 7 days secretion in response to citric acid, methacholine and eserine was again studied. The cat was then immediately used acutely or the observations described above were repeated at weekly or monthly intervals until the acute experiment was carried out. For the acute experiment various anaesthetics were tried, given intravenously after ether: chloralose (80 mg/kg), chloralose-urethane ( mg/kg), buthalitone (about 20 mg/kg) and barbitone ( mg/kg). Doses of the anaesthetics were repeated when required. Both parotid ducts were cannulated and sometimes the submaxillary ducts also. Records were made of the secretory effects of: afferent stimulation of the glossopharyngeal, and sometimes also the lingual nerves; efferent stimulation of the auriculo-temporal nerve and the cervical sympathetic trunk; intravenous injections of adrenaline, isoprenaline and phenylephrine. As agents blocking secretion atropine, propranolol and dihydroergotamine were used. At the end of the experiment the parotid glands were removed and their activity of choline acetyltransferase was estimated. A more detailed account of the methods is given in a previous paper [Ekstrom and Emmelin, 1973]. RESULTS The parasympathetic secretory innervation Four types of experiments served to throw light on the parasympathetic innervation. 1. After section of the auriculo-temporal nerve parotid secretion elicited reflexly from the mouth in light anaesthesia was greatly reduced, but some flow could always be obtained. This is shown in Fig. 1, where secretion was evoked by citric acid in the mouth before and 5 days after cutting the nerve. The flow was abolished when the anaesthesia was deepened and hexamethonium injected. It persisted after injection of propranolol (1 mg/kg)+dihydroergotamine (0.2 mg/kg) and it was obtained even if the sympathetic ganglion had been removed when the auriculo-temporal nerve was cut. The flow ceased after injection of a small dose of atropine (0.1 mg/kg). 2. A secretory response to eserine, although greatly diminished, could always be obtained 5 days after cutting the auriculo-temporal nerve (Fig. 1). In 20 cats studied the mean response during the first 15 min after injection of eserine was 44-4±6-8 (mean±s.e.m.) drops before, and 6-3±1-8 drops 5 days after denervation, i.e. a reduction to about 15%. As a measure ofremaining cholinergic neurones this figure was probably too high, since there was usually some supersensitivity after 5 days; the response to methacholine 1 ug/kg had in these cats increased from 0-6±0 2 to 2-3±0*6 drops. A response to eserine was maintained even if the operation also included extirpation of the superior cervical ganglion;
3 Parotid Secretion in Cats in 23 cats thus treated the response to eserine was drops before, and 934±1-8 drops after the combined operation. This indicates that cholinergic fibres present after auriculo-temporal nerve section were not supplied from the sympathetic ganglion. B C6 E 13 B Cr E FIG. 1. Secretory effects of citric acid, poured on the tongue throughout the two left sections of the tracing, and of eserine (E), 200 jig injected through the salivary duct. Upper panels: before, and lower panels: 5 days after section of the auriculo-temporal nerve. Records from above: minute marks, signal, drops of saliva. The experiments started in light buthalitone anaesthesia (3 mg/kg). The dose of buthalitone was increased to 20 mglkg at B. C6: hexamethonium 5 mg/kg. 3. In the acute experiments parotid secretion could be elicited by afferent stimulation of the glossopharyngeal or lingual nerves even when the auriculotemporal nerve had been cut. Miller [1913] found that in decerebrate cats secretion can be elicited from the parotid and submaxillary glands by afferent stimulation of the glossophanrygeal and lingual nerves. The responses were, however, very small. This was the reason why various anaesthetics were tried in the present investigation in an attempt to find a procedure suitable for such experiments. Some secretion was obtained under chloralose or barbitone and more under buthalitone or chloralose-urethane anaesthesia. The last-mentioned type of anaesthesia was preferred to buthalitone because of its longer duration of action. Generally it was observed that glossopharyngeal stimulation caused more parotid than submaxillary secretion, while the opposite was true for lingual nerve stimulation and, further, ipsilateral responses were more
4 14 Ekstrom and Emmelin pronounced than contralateral ones; in many cases no responses at all were obtained from the gland of the other side. These observations confirmed those of Miller [1913] RG LG LG $LG RG AT LG IMA LG i 5 FIG. 2. Acute experiment in chloralose-urethane anaesthesia. The right auriculo-temporal nerve had been cut 4 months earlier. Records from above: minute marks, signal, drops of saliva from right, from left parotid gland. RG: afferent stimulation of right glossopharyngeal nerve, LG: of left nerve. AT: stimulation of left auriculo-temporal nerve, S: of left sympathetic trunk, IMA: on left internal maxillary artery. Arrows: no. 1: section of left auriculo-temporal nerve; 2: of left sympathetic trunk; 3: ligation around the left internal maxillary artery; 4: injection of atropine 0-1 mg/kg, and 5: of propanolol 2 mg/kg. 'tr' on the records means that a trace of saliva was obtained. For electrical stimulations: 20/s, 6V (on the artery only 3V) and a duration of 1-5 msec. Figure 2 shows an acute experiment 4 months after section of the right auriculo-temporal nerve. Stimulation of the right glossopharyngeal nerve showed that a marked reinnervation of the right parotid gland had taken place. In this cat the response was, in fact, about as large as that of the left gland to stimulation of the left glossopharyngeal nerve. It was used as a control; it remained fairly constant throughout the acute experiment. The Fig. shows that section of the left auriculo-temporal nerve markedly lowered the response of the left gland to glossopharyngeal stimulation, but some effect was still obtained, just as some response had been obtained to eserine 4 months earlier after section of the right nerve. Section of the left cervical sympathetic trunk did not affect the size of the remaining response, although sympathetic stimulation was found to have a secretory effect. Figure 2 shows in addition that a ligature tied round the left internal maxillary artery and surrounding tissue further reduced the secretory response to afferent stimulation but did not wholly extinguish it. Atropine, on the other hand, abolished the minute persisting response as well as the small response of the contralateral gland which had so far been obtained. Before atropine it could be shown that stimulation of the artery on the glandular side of the ligature evoked some secretion.
5 Parotid Secretion in Cats A response to afferent glossopharyngeal stimulation immediately after ipsilateral section of the normal auriculo-temporal nerve was obtained in 17 out of 24 cats. Very roughly estimated the response was usually hardly more than 10% of the original effect. In 6 of the 17 cats atropine was given and found to abolish the small response. In the other 11 cats a ligature was tied round the internal maxillary artery; in 3 of these cats glossopharyngeal stimulation now lost its secretory effect, in the other 8 it was reduced but there was still a minute response left which atropine abolished. In 3 of the 17 cats in which glossopharyngeal stimulation caused secretion after section of the auriculo-temporal nerve, the lingual nerve was also excited; a small response could be elicited reflexly in this way also. When the acute experiment was carried out 5 to 7 days after section of the auriculo-temporal nerve it could also be shown that secretion could be evoked from the thus 'denervated' glands by afferent glossopharyngeal stimulation. 4. The activity of choline acetyltransferase was found to be very muchreduced 5 and 7 days after section of the auriculo-temporal nerve, but some activity remained. In 4 cats studied after 5 days the parotid glands of the operated side had an activity of 20-9±10.0% of those of the contralateral glands calculated per whole gland. After 7 days the corresponding figure from 5 cats was 11.1 ±6-6%. The sympathetic secretory innervation In the acute experiments great individual variations were observed in the secretory responses of the normal parotid glands to stimulation of the sympathetic trunk at a frequency of 20/sec. In 3 cats out of 26 studied there was no flow of saliva; the pupil dilated widely in all the cases. At the other extreme was the response of 7 drops during 1 min, obtained in 2 cats. On the average 2 drops were obtained in 1 min. A response of moderate size can be seen in Fig. 2. Like the usually much larger submaxillary secretion evoked by sympathetic stimulation the parotid response appeared after a long latency and often tended to decrease during a stimulation period of several minutes. The parotid flow was not merely due to expulsion of saliva by myoepithelial contraction, for effects could be elicited repeatedly. Nor was it a reflexly evoked response to stimulation of afferent fibres in the sympathetic trunk or in the adjacent vagus nerve, for it remained undiminished after section of the auriculotemporal nerve or injection of atropine (0.1 mg/kg). It is concluded that the parotid gland of the cat usually has a sparse supply of sympathetic secretory fibres, and this is in agreement with pharmacological observations, indicating that secretory cells in the gland have some adrenoreceptors. Unlike the submaxillary gland of the cat which has oc-receptors and responds to phenylephrine with a usually abundant secretion, the parotid gland seems to be supplied wholly or mainly with a-receptors. Adrenaline (10-20,ug/kg) and isoprenaline ( ,ug/kg) were found to cause a small, late secretory response. In the case of isoprenaline this flow continued for many minutes; it was larger the larger the effect of sympathetic nerve stimulation. These effects were antagonized by propranolol (1-2 mg/kg). Such an effect is shown in Fig. 2. In 2 cats of 15
6 16 Ekstr6m and Emmelin 15 tested phenylephrine (100 mg/kg) caused a small, repeatable response from the parotid gland; these glands also secreted when isoprenaline was given. DIsCuSSION The auriculo-temporal nerve is no doubt the principal secretory nerve of the parotid gland of the cat, as witness the lively salivary flow on its electrical stimulation; the marked effects of its section; the appearance of degeneration secretion [Emmelin and Str6mblad, 1958b]; the development of a high degree of supersensitivity in the secretory cells [Str6mblad, 1955; Ekstrom and Emmelin, 1973]; the great reduction of the secretory responses to stimulation of oral receptors or afferent nerves, or inhibition of cholinesterase in the gland; and the great fall in the glandular choline acetyltransferase activity. Secretory effects still obtainable reflexly indicate, however, that secretory nerves reach the gland by other routes also, and the main additional pathway seems to be along the internal maxillary artery, as is the case in dogs [Holmberg, 1971]. The proportion of fibres outside the auriculo-temporal nerve seems smaller in cats than in dogs, judging from the more marked effects of section of the nerve in cats. In dogs 20-70% of the reflexly induced secretory response remained [Garrett and Holmberg, 1970]; in cats the response to afferent glossopharyngeal stimulation was probably not more than about 10% in most cases, and even in the eserine test, where supersensitivity undoubtedly magnified the effects, there was only about 15% of the response left after degeneration ofthe auriculotemporal nerve. The corresponding figure for dogs is about 30% [Holmberg, 1972]. In dogs section of the nerve reduced the choline acetyltransferase activity only to 30% after a week [Ekstr6m and Holmberg, 1972] but in cats to 11%. As in dogs, secretion could sometimes be elicited reflexly even when the fibres round the artery had been eliminated, but because of the minuteness of the response no attempt was made to trace the fibres still carrying secretory impulses to the gland. Apparently the fibres were cholinergic, for atropine in low dosage abolished the response. Electrical stimulation of the cervical sympathetic trunk caused parotid secretion in most cats, and the response resembled that obtained in the submaxillary gland of this species except that it was much smaller and seemed to be mediated mainly via fl-receptors. It is remarkable that even in cats in which the parotid response to sympathetic stimulation was fairly pronounced, there was no indication that sympathetic secretory fibres contributed to the volume of saliva produced reflexly from the mouth or by electrical stimulation of oral nerves. In the submaxillary gland of the cat secretion can be elicited by afferent stimulation of the sciatic nerve, and here not only parasympathetic but also sympathetic secretory nerves are at work [Velo and Hoff, 1961]. There may be a difference in this respect between the glands or, perhaps more likely, the reflex elicited from the oral region may engage only parasympathetic fibres whereas stimuli of the nociceptive type activate sympathetic fibres also. As is well known the secretory responses of the dog's submaxillary and parotid glands to feeding are abolished by atropine [see Babkin, 1950]. The possibility
7 Parotid Secretion in Cats that sympathetic fibres normally take part in the reflexes from the mouth but add other constituents than water to the saliva may have to be kept in mind. ACKNOWLEDGMENT This work was supported by a grant to N. E. from the Swedish Medical Research Council (B 72-14X-539). REFERENCES BABKiN, B. P. (1950). Secretory Mechanism of the Digestive Glands, 2nd ed., Hoeber, New York. BRADFORD, J. R. (1887). The electrical phenomena accompanying the excitation of socalled secretory and trophic nerve fibres, in the salivary glands of the dog and cat. Journal of Physiology, 8, CRAGG, B. G. (1965). Failure of conduction and of synaptic transmission in degenerating mammalian C fibres. Journal of Physiology, 179, EKsTR6M, J. and EMMELIN, N. (1974). Reinnervation of the denervated parotid gland of the cat. Quarterly Journal of Experimental Physiology, 59, 1-9. EKSTROM, J. and HOLMBERG, J. (1972). Choline acetyltransferase in the normal and parasympathetically denervated parotid gland of the dog. Acta Physiologica Scandinavica, 86, EmmEiaN, N. and STROMBLAD, B. C. R. (1958a). The effect of anticholinesterases on the parotid gland after parasympathetic decentralization or denervation. British Journal of Pharmacology amd Chemotherapy, 13, EMMELIN, N. and STROMBLAD, B. C. R. (1958b). A 'paroxysmal' secretion of saliva following parasympathetic denervation of the parotid gland. Journal of Physiology, 134, FRITZ, E. M. and BOTELHO, S. Y. (1969). Role of autonomic nerve impulses in secretion by the parotid gland of the cat. American Journal of Physiology, 216, GARRTT, J. R. (1966). The innervation of salivary glands. III. The effects of certain experimental procedures on cholinesterase-positive nerves in glands of the cat. Journal of the Royal Microscopical Society, 86, GARRETT, J. R. and HOLMBERG, J. (1970). The secretory parasympathetic innervation of the parotid gland of the dog. Journal of Physiology, 209, 19-20P. HOLMBERG, J. (1971). The secretory nerves of the parotid gland of the dog. Journal of Physiology, 219, HOLMBERG, J. (1972). Secretion from the dog's parotid at different time intervals after denervation. Acta Physiologica Scandinavica, 85, MIma R, F. R. (1913). On the reactions of the salivary centres. Quarterly Journal of Experimental Physiology, 6, NAvROcKi, F. (1868). Die Innervation der Parotis. Studien des Physiologischen Instituts zu Breslau, 4, NORDENFELT, I. (1963). Choline acetylase in normal and denervated salivary glands. Quarterly Journal of Experimental Physiology, 48, NORDENFELT, I. (1965). On the sympathetic innervation of the parotid gland of the cat. Quarterly Journal of Experimental Physiology, 50, OHLIN, P. and STROMBLAD, B. C. R. (1958). Supersensitivity of the vessels of the parotid gland after denervation. British Journal of Pharmacology and Chemotherapy, 13, RIcHINs, C. A. and KUNTZ, A. (1953). Role of sympathetic nerves in the regulation of salivary secretion. American Journal of Physiology, 173, STROMBLAD, R. (1955). Sensitivity of the normal and denervated parotid gland to chemical agents. Acta Physiologica Scandinavica, 33, VELO, A. G. and HOFF, E. C. (1961). Salivary responses to cortical and sciatic stimulation. American Journal of Physiology, 200, von WITTcIca (1867). Parotis und Sympathicus. VirchowsArchivfiirpathologische Anatomie und Physiologie, XXXIX, VOL. Lix, NO
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