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1Department of Biologic and Materials Sciences, School of Dentistry and 2Department of Molecular and Integrative Physiology, Medical School, University of Michigan, Ann Arbor, Michigan
Submitted 14 August 2006; accepted in final form 26 January 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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). Saliva also plays a role in protection of the oral mucosa and teeth. In most mammals, secretion of saliva is under the reflex control of the autonomic nervous system and is initiated by food mastication, which stimulates oral receptors. Despite the importance of this reflex the neural circuitry responsible for initiation of salivary secretion has received relatively little attention.
The cell bodies of the preganglionic parasympathetic neurons supplying the salivary glands are located in the brain stem salivatory nuclei, which are divided into inferior and superior subdivisions based on the cranial nerve distribution of the axons supplying the salivatory glands. Neurons of the inferior salivatory nucleus (ISN) innervate parotid and lingual (von Ebner) glands via the glossopharyngeal nerve, whereas the superior salivatory nucleus (SSN) innervates the submandibular, and sublingual glands via the chorda tympani branch of the facial nerve (Loewy 1990).
Neurons of the salivatory nuclei form the final common pathway of the salivatory reflex (Hector and Linden 1999). Input derived from stimulating oral taste and mechanoreceptors is one of the major afferent limbs of this reflex system. The source of other central input to the salivatory nuclei is located in a large number of rostral brain areas including the parabrachial complex, Edinger-Westphal nucleus, mesencephalic nucleus, hypothalamus, substantia innominata, bed nucleus of the stria terminalis, and amygdala (Hosoya et al. 1983, 1990; Jansen et al. 1992; Takeuchi et al. 1991). Thus both afferent sensory information as well as descending synaptic input interact at the salivatory neurons to reflexively initiate salivary secretion (Hector and Linden 1999; Kawamura and Yamamoto 1978; Matsuo 1999).
Some details of the brain stem reflex circuitry underlying the salivatory reflex have recently received attention. Neurophysiological and morphological characteristics of the salivatory neurons have been investigated (Fukami and Bradley 2005; Kim et al. 2004; Matsuo and Kang 1998), and more recently investigators have studied the excitatory and inhibitory responses to glutamate and GABA in these neurons (Bradley et al. 2005; Mitoh et al. 2004). However, in addition to glutamate and GABA, these salivatory neurons have been shown to be surrounded by fibers immunostaining for a number of neuropeptides including serotonin (5-HT) and substance P (SP), (Nemoto et al. 1995). In our current work, we have shown that neurons of the ISN respond to application of 5-HT and SP.
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METHODS |
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Sprague-Dawley rats (10–24 day old) were anesthetized with a 6% solution of halothane mixed with air (400–600 ml/min). Anesthetic level was assessed by lack of a reflex response to mild tail pinching. All surgical procedures were carried out under National Institutes of Health and University of Michigan Animal Care and Use Committee approved protocols.
A fluorescent tracer, Alexa Fluor 568 dextran (Molecular Probes) was used to retrogradely label ISN neurons innervating von Ebner'slingual salivary glands situated in the posterior tongue that secrete saliva into the clefts surrounding the circumvallate and foliate papillae. The lingual-tonsillar branch of glossopharyngeal nerve was exposed by ventral approach and cut. Crystals of the fluorescent tracer were applied to the cut central end and isolated from surrounding tissue with silicone sealer (Kwik-Cast, World Precision Instruments). The skin wound was closed with cyanoacrylate glue. Animals recovered in an isolated cage on a heating pad and when ambulatory were returned to the dam's home cage.
Preparation of brain stem slices
After 2–4 days the rats were killed with halothane and decapitated, and the brain rapidly removed and cooled for 6 min in an oxygenated, physiological saline solution in which NaCl was replaced with iso-osmotic sucrose at 4°C (Aghajanian and Rasmussen 1989). The brain stem was transected at the level of the pons and just below the obex and cemented to a Vibratome (Technical Products International) stage with cyanoacrylate glue and sectioned horizontally into 200- or 300-µm-thick slices. The slices were incubated for 
1 h in oxygenated physiological saline solution at 35°C. The physiological saline contained (in mM) 124 NaCl, 5 KCl, 2.5 CaCl2, 1.3 MgSO4, 26 NaHCO3, 1.25 NaH2PO4, and 25 dextrose and was gassed with a 95% O2-5% CO2 mixture to achieve a solution pH of 7.4.
Recording
A brain slice was transferred to a recording chamber attached to the stage of a Nikon ECLIPSE E600-FN microscope and anchored with a nylon mesh. During recording, the slice was perfused at 2–2.5 ml/min with oxygenated physiological saline solution at 35°C. All drugs were dissolved in physiological saline and applied by perfusion over the brain slices. Drug concentrations were based on those used by others in similar investigations (Browning and Travagli 1999; King et al. 1993; Lewis and Travagli 2001).
Retrogradely labeled ISN neurons were identified using brief epifluorescence illumination and then observed using infrared-differential interface contrast optics (IR-DIC) via a CCD camera (IR-1000, DAGE-MTI). A 40x water-immersion objective lens was used to identify and observe the neurons. Whole cell recordings were obtained from the labeled neurons using a patch-clamp amplifier (Axoclamp-2B, Axon Instruments). Signals were recorded through 2-kHz low-pass filter, digitized at 20 kHz (DigiData 1200, Axon Instruments), and stored on the hard disk of a computer. Data acquisition was performed using pCLAMP 8 (Axon Instruments). Patch pipettes were pulled from borosilicate glass capillaries (TW150F-4, World Precision Instruments) using a two-stage puller (PP-83, Narishige) and filled with a pipette solution containing (in mM) 130 potassium gluconate, 10 HEPES, 10 ethylene glycol-bis(
-aminoethyl ether) N,N,N',N'–tetraacetic acid (EGTA), 1 MgCl2, 1 CaCl2, and 2 ATP, buffered to pH 7.2 with KOH. Tip resistance of the filled pipettes was 6–8 M
. The junction potential due to potassium gluconate (10 mV) was subtracted from the membrane potential values (Standen and Stanfield 1992).
Neurons selected for analysis had a resting membrane potential that was stable and more negative than –40 mV, an action potential overshoot >10 mV, and an input resistance >200 M.
Data analysis
All analysis was conducted using the SPSS statistics program. Statistical analysis was performed with a Student's t-test for comparisons between pairs of groups and by one-way ANOVA with Dunnett post hoc test for comparisons between control and experimental groups. Values in the text and figures are presented as means ± SE. Statistical significance was reached at P < 0.05. Curves were fitted using the Hill equation.
Drugs
Alexa Fluor 568 dextran was purchased from Molecular Probes (Eugene, OR). SP, 5-hydroxytryptamine, 1-[2-methoxyphenyl /id]-4-[4-(2-phthalimido)-butyl] piperazine (NAN-190), 3-[2-(4- [4-fluorobenzoyl]-1-piperidinyl]-2,4[1H.3H]-quinazolinedione (ketanserine), 3-tropanyl-indole-3-carboxylate (ICS-205,930), 
-methyl-5-hydroxytryptamine (-Me-5-HT), [Sar9, Met(O2)11]-SP (SM-SP), -neurokinin (NK), and tetrodotoxin (TTX) were all purchased from Sigma (St. Louis, MO).
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RESULTS |
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The 5-HT results are based on recordings from 106 ISN neurons. Resting membrane potential ranged from –42 to –72 mV with a mean of –55 ± 1 mV. Input resistance ranged from 229 to 965 M with a mean of 497 ± 28 M, and action potential amplitude ranged from 71 to 105 mV with a mean of 89 ± 3 mV.
All 106 neurons responded to 5-HT or a 5-HT2A receptor agonist (-Me-5-HT) application. Most of the neurons (n = 100; Fig. 1, A and B) responded with a concentration-dependent membrane depolarization, whereas a very few (n = 6) responded by membrane hyperpolarization. Responses to increasing concentrations of 5-HT were tested in 27 neurons, and all were depolarized by 5-HT with a maximum depolarization of 7 ± 2 mV at 30 µM and a half-maximal response (EC50) at 3.0 µM (Fig. 1C). The depolarization was sufficient to evoke action potentials in 77% of the neurons. Neurons could be separated in two groups based on input resistance changes induced by 5-HT. Some neurons (n = 47) responded with increased input resistance (EC50 = 2.7 µM, Fig. 1D), whereas others (n = 53) responded with a decrease (EC50 = 2.6 µM, Fig. 1E) even though all were depolarized by 5-HT application.
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-Me-5-HT (50 µM in 2 neurons) resulted in membrane hyperpolarization. The hyperpolarization by 5-HT averaged 3 ± 1 mV accompanied by a decrease in both input resistance and number of action potentials elicited by a depolarizing current injection (60 pA, 100 ms, data not shown). Action potentials were evoked by a long depolarizing current injection (50 pA, 1,200 ms duration). To eliminate the influence of depolarization induced by 5-HT on voltage-gated channels, neurons were maintained at –50 mV by current injection. Compared with current injections in control buffer, application of 100 µM 5-HT increased the number of evoked spikes from 11 ± 1 to 17 ± 1 spikes (n = 8; P < 0.05) independent of any change in input resistance (an increase in 2 and a decrease in 6 neurons). In addition, the increased spike frequency was accompanied by a decrease in the time to initiate the first spike from 21 ± 3 to 17 ± 2 ms (n = 7; t-test: P < 0.05) and a decrease in the interval between the first and second spike from 66 ± 4 to 47 ± 5 ms (n = 9; t-test: P < 0.05; Fig. 2). 5-HT therefore increased the excitability of the ISN neurons.
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5-HT receptors are composed of a number of subtypes (Barnett and Sharp 1999; Hoyer et al. 2002), and we used several 5-HT receptor subtype antagonists to determine which subtypes are involved in the effects of 5-HT on the ISN neurons. Based on experiments on preganglionic parasympathetic neurons of the dorsal motor nucleus of vagus (Browning and Travagli 1999), which is a caudal extension of the ISN, we investigated the involvement of 5-HT1A, 5-HT2, 5-HT3, and 5-HT4 receptors. 5-HT (50 µM) was applied in the presence of one of these antagonists. As shown in Fig. 3, a 5-HT2A receptor antagonist, ketanserin (10 µM) blocked or largely suppressed the depolarizing effect of 5-HT (n = 13; ANOVA: P < 0.05). A 5-HT1A receptor antagonist, NAN-190 (10 µM; n = 8), and a 5-HT3/4 receptor antagonist, ICS-205,930 (10 µM; n = 9), had no significant effect on membrane depolarization by 5-HT. To confirm involvement of 5-HT2A receptors in the 5-HT response, a specific 5-HT2 receptor agonist, -Me-5-HT (50 µM) was applied which mimicked the depolarizing effect of 5-HT (n = 6). Thus 5-HT acting via 5-HT2A receptors depolarizes the ISN neurons. In two additional neurons, application of -Me-5-HT resulted in membrane hyperpolarization with a decreased input resistance similar to the group of four neurons already described that responded to 5-HT by membrane hyperpolarization. This result suggests that hyperpolarization induced by 5-HT may be mediated by 5-HT2 receptors. Because we encountered so few ISN neurons that were hyperpolarized by 5-HT, we were not able to investigate this effect further.
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The results of the responses to SP were derived from 32 ISN neurons. All of the neurons tested responded to SP by membrane depolarization, and the magnitude of the depolarization increased with concentration (Fig. 4). The maximum depolarization and input resistance increase induced by 1 µM SP was 9 ± 1 mV and 33 ± 10 M (n = 10), respectively. The half-maximal response occurred at 0.01 µM SP (Fig. 4C). Depolarization was accompanied by an increase in input resistance in 27 of the neurons (42 ± 7 M at 1 µM). In the remaining neurons (n = 5), input resistance did not apparently change. SP at concentrations of 1 µM and higher resulted in the generation of spontaneous action potentials in most of the neurons (19/21; Fig. 4A). To determine if SP acts directly on the ISN neurons, 1 µM SP was applied in the presence of 2 µM TTX. In three neurons tested, the magnitude of depolarization induced by SP was 8 ± 1 mV in control and 6 ± 1 mV in the presence of TTX, and the increase in input resistance was 120 ± 41 M in control and 77 ± 9 M in the presence of TTX (data not shown). These results indicate that SP has direct postsynaptic action on the ISN neurons.
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NK were used. In six neurons, 1 µM SP induced 8 ± 1 mV depolarization and a 13% increase in input resistance. After washout of SP, application of 3 µM SM-SP induced a similar depolarization of 7 ± 1 mV and an 11% increase of input resistance (Fig. 6, A and Ba). In a further group of six neurons, application of 3 µM NK induced a 9 ± 3 mV depolarization and an 8% increase of input resistance (Fig. 6, A and Bb). There was no significance difference between the value of the membrane potential change due to SP and the agonists applications (ANOVA: P > 0.05), and there was no significance difference in the percentage-change of input resistance between application of SP, SM-SP and NK (t-test: P > 0.05). These results indicate that both neurokinin-1 and -2 receptors are involved in the effect of SP on ISN neurons.
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DISCUSSION |
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; Lewis and Travagli 2001), which is extends caudally from the salivatory nuclei.
Although 5-HT depolarized all ISN neurons, membrane conductance changes were divergent. Parasymapathetic neurons of the salivatory and dorsal motor nucleus of the vagus are of heterogeneous morphology (Fox and Powley 1992; Kim et al. 2004) and biophysical properties (Matsuo and Kang 1998; Fukami and Bradley 2005; Tell and Bradley 1994; Travagli and Gillis 1994; Yarom et al. 1985), some neurons having predominant IA, whereas others have IKIR currents. Other ion channels have also been identified in these parasympathetic neurons involved in the excitatory effect of 5-HT (Hopwood and Trapp 2005). Depolarization of these neurons by 5-HT would potentially activate these and other voltage-dependent channels, resulting in the divergent conductance changes. Functionally, different populations of ISN neurons would potentially modulate excitatory and inhibitory input in different ways.
The source of the immunostained neuropeptides surrounding the ISN neurons is assumed to be from either brain stem or more rostral brain areas (Nemoto et al. 1995). However, both 5-HT and SP immunoreactive neurons are described in the petrosal ganglion, which contains the cell bodies of the gustatory input from the posterior tongue (Helke and Hill 1988; Okada and Miura 1992; Zhong et al. 1999). Although some of these petrosal ganglion neurons may be associated with the afferent innervation of the carotid body not all the SP-positive neurons are carotid body neurons (Finley et al. 1992). It is conceivable therefore that some of the immunohistochemical 5-HT or SP staining associated with the salivatory neurons may originate from the afferent input to the NST as has been suggested for neurons involved in the baroreceptor reflex (Raul 2003). The NST also immunostains for 5-HT receptors (Manaker and Verderame 1990; Thor et al. 1988, 1992) and neurons of the rNST respond to SP (King et al. 1993). Thus superfusion of the brain slice with 5-HT and SP would stimulate neurons in the NST that synapse with the ISN neuron, and this may be reflected in the increased synaptic activity evoked by SP in Fig. 4Bb.
Action of 5-HT and SP on other brain stem parasympathetic reflexes
The role of 5-HT and SP in the baroreceptor reflex arc has been extensively studied (Jordan 2004; Raul 2003). Microinjections of 5-HT into the caudal NST elicit the typical responses of baroreceptor activation mediated by activation of 5-HT2 postsynaptic receptors. As in the present study, 5-HT application results in both excitatory and inhibitory effects on baroreceptor reflex neurons (Sevoz-Couche et al. 2000); the excitatory effect is mediated by 5-HT2A receptors and 5-HT2C receptors are responsible for inhibition. We were not able to record from sufficient inhibitory (hyperpolarizing) ISN neurons to determine which 5-HT receptor was expressed in these neurons but all excitatory (depolarizing) neurons expressed 5-HT2A receptors. Thus there are similarities between the neurobiology of the baroreceptor and gustatory-salivatory reflex arcs. Both involve afferent input to the NST and efferent parasympathetic motor output neurons. It is possible then to conclude that as in the baroreceptor reflex, the role of 5-HT in the gustatory-salivatory reflex is as a facilitator.
SP also excites other brain stem nuclei including neurons of the caudal and rostral nucleus of the solitary tract (Champagnat et al. 1986; King et al. 1993) that receive input from sensory afferents as the major input component of reflex activity of the oral cavity and gut. The output cells of this reflex are also sensitive to SP. According to Lewis and Travagli (2001), the SP containing pathways from both the peripheral and CNS are involved in the vagal neurons controlling gastric motility.
Role of the ISN neurons in control of the von Ebner glands
The basic function of the ISN neurons examined in the current study is to integrate information from oral receptors and a number of brain areas to control the secretion of the von Ebner salivary glands. In contrast to major salivary glands that secrete directly into the oral cavity, von Ebner glands secretions empty into the clefts of the posterior tongue gustatory papillae. Because the epithelium of the clefts contains hundreds of taste receptors (Miller 1977; Miller and Smith 1984), it has always been assumed that these glands have an important role in taste function. Due to the position of the taste receptors in the cleft epithelium, taste stimuli have to somehow access the taste receptors from the oral cavity. Secretions of the von Ebner's glands provide a diffusion path facilitating the transport of taste stimuli. In addition, the von Ebner secretions flowing from the gland ducts into the clefts also function to flush out the clefts to remove taste stimuli as well as food debri and thus maintain a healthy environment. These potential roles of the secretions of von Ebner's glands in taste function have been tested experimentally (Gurkan and Bradley 1988). Stimulation of von Ebner gland secretion reduced taste responses evoked from the posterior tongue taste buds presumably via a mono- or polysynaptic reflex connecting the afferent sensory input to the ISN neurons.
The afferent limb of this reflex involves glutamate receptors (Bradley et al. 2005). However, reflex secretion of saliva also results from other sensory inputs such as olfaction (Hector and Linden 1999), vision, and "psychic" factors are also thought to act as initiators of salivary secretion (Holland and Matthews 1970). Thus there are many potential pathways involved in salivary secretion, and these may use different neurotransmitters and neuromodulators. It is therefore reasonable to suggest that 5-HT and SP have a role in either maintaining the resting flow rate or are synaptic mediators of one of the descending pathways originating from other sensory systems.
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GRANTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: R. M. Bradley, Dept. of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, MI 48109-1078 (E-mail rmbrad{at}umich.edu)
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REFERENCES |
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, onset time of a 1-min 5-HT application. Numbers above the upper trace are the membrane potential values before and after application of 5-HT. Hyperpolarizing (–100 pA, 800 ms) and depolarizing (20–100 pA in 20-pA increments, 800 ms) current pulses were injected before (a) and after (b) application of 5-HT to measure membrane resistance. B: faster time base recordings from A. Responses to the hyperpolarizing (–100 pA) and depolarizing (40 pA) pulses before (a) and after (b) application of 5-HT (spikes truncated). 5-HT dose-response relationship between 5-HT concentration and membrane potential (C) and input resistance (D and E). D shows an increase and E shows a decrease in input resistance induced by increasing concentrations of 5-HT, respectively. Numbers of measurements are shown above each data point.
