Location of parotid preganglionic neurons in the inferior salivatory nucleus and their relation to the superior salivatory nucleus of rat

doi:10.1016/j.neulet.2008.05.099

Neuroscience Letters

Volume 440, Issue 3, 8 August 2008, Pages 265-269

https://doi.org/10.1016/j.neulet.2008.05.099 Get rights and content

Abstract

In major brain maps the location of the salivatory nuclei of the rat is depicted from the level of the root of the facial nerve to the level of the rostral tip of the nucleus of the solitary tract. Most published data deal with the superior salivatory nucleus (SSN). In the present study the topography of the parasympathetic preganglionic neurons of the inferior salivatory nucleus (ISN) that innervate the parotid gland through the otic ganglion was determined by means of a retrograde transneuronal labeling technique. Parasympathetic, sympathetic and sensory neurons were labeled following injection of the virus into the parotid gland. The majority of the ISN neurons were found dorsal to the facial motor nucleus, embedded in the parvocellular reticular formation. In addition to the ISN neurons, virus-labelled cells were present in the intermediolateral (IML) cell column of the thoracic spinal cord, in the brainstem catecholamine groups, and in medullary raphe neurons. The removal of the ipsilateral superior cervical ganglion prior to the virus injection into the parotid gland did not influence the labeling of the ISN neurons but labeled neurons were not observed in the IML and A5 catecholamine cell group. In our previous study we had defined the relationship between the lacrimal and submandibular subdivison of the SSN, while in the present study we defined the relationship between the ISN and the lacrimal subdivision of SSN: the later located ventrolaterally to the caudal portion of the ISN. On the basis of these data a three-dimensional topography is given suggesting the relationship between the ISN and SSN.

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Acknowledgements

The authors thank Dr. Arnold Szabó for helping with confocal microscopy. This work was supported by grants T-046624 to IG and No. 49862 to MP, from the Hungarian National Science Foundation (OTKA), and also from the Ministry of Health, ETT 448/2006 to IG. Contract grant sponsor: Hungarian Academy of Sciences.

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The anatomical location of the superior salivatory nucleus (SSN), the site of origin of the parasympathetic preganglionic cell bodies that innervate the submandibular-sublingual salivary glands, is well established in rats. However, as of yet there is no functional data that convincingly shows the secretory nature of this region. Previous studies have not been able to differentiate between interventions on efferent or afferent fibers connected to the SSN versus interventions on the salivatory nucleus itself. Taking advantage of the fact that salivatory neurons express NMDA-receptors on their somas, in the present study SSN cell bodies were activated and lesioned sequentially by means of intracerebral application of NMDA-neurotoxin. In exp. 1 two effects, a short- and a long-term effect, were observed following NMDA administration. The first effect was high submandibular-sublingual saliva secretion during the hour following administration of the neurotoxin and the second was a profound change in drinking behavior once the animals recovered from the lesion. Thus, on post-surgery days 16, 17 and 18, the rats exhibited hyperdipsia in the presence of dry food but not in the presence of wet food. In expt. 2 results showed that saliva hypersecretion observed after NMDA-microinjection was completely blocked by the administration of atropine (a cholinergic blocker) but not after the administration of dihydroergotamine plus propranolol (α and β-adrenergic blockers, respectively). From a functional perspective, these data suggest that the somata of the parvocellular reticular formation control the secretory activity of the submandibular-sublingual salivary glands and thus constitute the SSN.
An origin of carotid vasodilation extends along the full extent of the parasympathetic parvicellular reticular region in the rat brainstem
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Tracer studies in rats using a variety of techniques, including recent transneuronal virus tracing methods, have provided anatomical evidence showing cranial parasympathetic neuronal pathways innervating several tissues. The superior and inferior salivatory nuclei and the limited part of the PcRt that was previously examined in the pons and medulla have been identified as central origins of parasympathetic neurons based on observations following injection of a viral tracer into the submandibular glands (Hübschle et al., 1998; Jansen et al., 1992), lacrimal glands (Toth et al., 1999), eye choroid (Cuthbertson et al., 2003), parotid glands (Rezek et al., 2008), gingiva and lip (Szabo et al., 2015), and pterygopalatine ganglion (Spencer et al., 1990). The functionally identified vascular area examined in the present study encompasses these structures.
During grooming in rats, cranial parasympathetic activation leads to increased carotid artery blood flow, but the brainstem origin of this vasodilation signal is poorly understood. The aim of this study was to map brainstem sites wherein chemical stimulation with l-cysteine, an ionotropic excitatory amino acid receptor activator, can trigger carotid vasodilation in anesthetized intact and superior cervical sympathectomized (SCD) rats. The right side of the brainstem was accessed ventrally; arterial blood pressure and right carotid artery flow resistance were monitored. Employing microinjections of l-cysteine into the ipsilateral brainstem, vasodilation triggering sites were identified dorsal and rostral to the rostral ventrolateral medulla (RVLM) presympathetic pressor area, forming a parasagittal plate-like response zone that varied from rat to rat. In SCD rats (N = 6), we observed a vasodilation zone in a region that included the RVLM pressor area, suggesting a parasympathetic origin. A similar zone was identified in intact rats (N = 8), except that it did not include part of the RVLM pressor area. Dye injected into vasodilator sites labelled the rostral part of the parvicellular reticular formation (PcRt), consistent with a cranial parasympathetic origin. Employing mapping with L-cysteine, a putative neuromodulator, this study provides the first functional demonstration of a carotid vasodilation area that extends along the full extent of the parasympathetic rostral PcRt region in rats.
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Citation Excerpt :
Only a few data are available in the literature about the detailed autonomic innervation of the structures of the oral cavity and associated salivary glands. Rezek and his co-workers (2008) mapped the neurons of the inferior salivatory nucleus (ISN) which supply the parasympathetic preganglionic innervation of rat parotid gland. Wojtkiewicz and his co-workers (2011) identified the chemical coding of the SCG which gives the postganglionic sympathetic innervation of the porcine parotid gland.
The major goals of this present study were 1) to further clarify which parasympathetic ganglion sends postganglionic fibers to the lower gingiva and lip that may be involved in the inflammatory processes besides the local factors; 2) to separately examine the central pathways regulating sympathetic and parasympathetic innervation; and 3) to examine the distribution of central premotor neurons on both sides. A retrogradely transported green fluorescent protein conjugated pseudorabies virus was injected into the lower gingiva and lip of intact and sympathectomized adult female rats. Some animals received virus in the adrenal medulla which receive only preganglionic sympathetic fibers to separately clarify the sympathetic nature of premotor neurons. After 72–120 h of survival and perfusion, the corresponding thoracic part of the spinal cord, brainstem, hypothalamus, cervical, otic, submandibular and trigeminal ganglia were harvested. Frozen sections were investigated under a confocal microscope. Green fluorescence indicated the presence of the virus. The postganglionic sympathetic neurons related to both organs are located in the three cervical ganglia, the preganglionic neurons in the lateral horn of the spinal cord on ipsilateral side; premotor neurons were found in the ventrolateral medulla, locus ceruleus, gigantocellular and paraventricular nucleus and perifornical region in nearly the same number on both sides. The parasympathetic postganglionic neurons related to the gingiva are present in the otic and related to the lip are present in the otic and submandibular ganglia and the preganglionic neurons are in the salivatory nuclei. Third order neurons were found in the gigantocellular reticular and hypothalamic paraventricular nuclei and perifornical area.
Role of medullary GABA signal transduction on parasympathetic reflex vasodilatation in the lower lip
2012, Brain Research
Citation Excerpt :
Rezek et al. (2008) also demonstrated that the submandibular subnucleus of the SSN joins rostrally the ISN, whereas the lacrimal subnucleus of the SSN is located ventrally and laterally to the caudal portion of the ISN. For this reason, it is not possible to selectively stimulate the ISN without stimulating the SSN, although the injection cannula and electrode was implanted in the area corresponding to the ISN (Fig. 1) (Paxinos and Watson, 2005; Rezek et al., 2008). Despite the overlapping of the ISN and the SSN, we showed that electrical stimulation of the area corresponding to the ISN evoked vasodilatation in the lower lip (Fig. 1).
In the orofacial area, noxious stimulation of the orofacial structure in the trigeminal region evokes parasympathetic reflex vasodilatation, which occurs via the trigeminal spinal nucleus (Vsp) and the inferior/superior salivatory nucleus (ISN/SSN). However, the neurotransmitter involved in the inhibitory synaptic inputs within these nuclei has never been described. This parasympathetic reflex vasodilatation is suppressed by GABAergic action of volatile anesthetics, such as isoflurane, sevoflurane, and halothane, suggesting that medullary GABAergic mechanism exerts its inhibitory effect on the parasympathetic reflex via an activation of GABA receptors. The aim of the present study was to determine the role of GABA_A and GABA_B receptors in the Vsp and the ISN in regulating the lingual nerve (LN)-evoked parasympathetic reflex vasodilatation in the lower lip. Under urethane anesthesia (1 g/kg), change in lower lip blood flow elicited by electrical stimulation of the LN was recorded in cervically vago-sympathectomized rats. Microinjection of GABA (10 μM; 0.3 μl/site) into the Vsp or the ISN significantly and reversibly attenuated the LN-evoked parasympathetic reflex vasodilatation. Microinjection of the GABA_A receptor-selective agonist muscimol (100 μM; 0.3 μl/site) or the GABA_B receptor-selective agonist baclofen (100 μM; 0.3 μl/site) into the Vsp or the ISN significantly and irreversibly reduced this reflex vasodilatation, and these effects were attenuated by pretreatment with microinjection of each receptor-selective antagonists [GABA_A receptor selective antagonist bicuculline methiodide (1 mM; 0.3 μl/site) or GABA_B receptor selective antagonist CGP-35348 (1 mM; 0.3 μl/site)] into the Vsp or the ISN. Microinjection of these antagonists alone into the Vsp or the ISN had no significant effect on this reflex vasodilatation. In addition, microinjection (0.3 μl/site) of the mixture of muscimol (100 μM) and baclofen (100 μM) into the Vsp or the ISN also significantly reduced this reflex vasodilatation. These results suggest that medullary GABA signal transduction inhibits the parasympathetic reflex vasodilatation in the rat lower lip via GABA_A and GABA_B receptors in the Vsp and the ISN.
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2012, The Mouse Nervous System
Precise motor control of visceral effector tissues, including exocrine and endocrine glands, vascular and visceral smooth muscle, adipose tissue, and cardiac muscle is essential for survival of the individual and for successful reproduction. These diverse tissue types are controlled by separate anatomical and functional pathways. These “autonomic pathways” can be activated independently or co-activated depending on the specific reflex or environmental challenge encountered. Overarching drives for activation of autonomic pathways are varied but include: adjusting vascular perfusion to tissues according to their specific requirements, maintenance of chemical gradients, energy balance, thermoregulation, and reproductive behaviors. This omits many other autonomic responses such as tear formation and regulation of pupil diameter. Above drives apply to all vertebrates, and to some extent the general anatomical and functional operation of visceromotor pathways are conserved across species. The parasympathetic, sympathetic and enteric divisions of the autonomic nervous system are best understood in the context of their anatomical projections. Peripheral autonomic motor pathways consist of a final central nervous system (CNS) neuron that sends an axon via either cranial or spinal nerves to synapse with a neuron in a peripheral ganglion which innervates the final target. The available data on peripheral autonomic pathways in mice indicates that neurotransmitter phenotype and neuroeffector transmission is broadly similar to that observed in rats and other experimental animals. There are, however, aspects of neuroanatomy, in particular the expression of some chemical markers, which differ, not only between rat and mouse, but between strains of mice. Clearly there is scope for further immunohistochemical and retrograde tracing studies to ascertain which of these differences has any functional significance. Postganglionic autonomic neurons show the same target-related morphological trends as homologous neurons in larger mammals.
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The pontine parabrachial nucleus (PBN) and medullary reticular formation (RF) are hindbrain regions that, respectively, process sensory input and coordinate motor output related to ingestive behavior. Neural processing in each hindbrain site is subject to modulation originating from several forebrain structures including the insular gustatory cortex (IC), bed nucleus of the stria terminalis (BNST), central nucleus of the amygdala (CeA), and lateral hypothalamus (LH). The present study combined electrophysiology and retrograde tracing techniques to determine the extent of overlap between neurons within the IC, BNST, CeA and LH that target both the PBN and RF. One fluorescent retrograde tracer, red (RFB) or green (GFB) latex microbeads, was injected into the gustatory PBN under electrophysiological guidance and a different retrograde tracer, GFB or fluorogold (FG), into the ipsilateral RF using the location of gustatory NST as a point of reference. Brain tissue containing each forebrain region was sectioned, scanned using a confocal microscope, and scored for the number of single and double labeled neurons. Neurons innervating the RF only, the PBN only, or both the medullary RF and PBN were observed, largely intermingled, in each forebrain region. The CeA contained the largest number of cells retrogradely labeled after tracer injection into either hindbrain region. For each forebrain area except the IC, the origin of descending input to the RF and PBN was almost entirely ipsilateral. Axons from a small percentage of hindbrain projecting forebrain neurons targeted both the PBN and RF. Target specific and non-specific inputs from a variety of forebrain nuclei to the hindbrain likely reflect functional specialization in the control of ingestive behaviors.

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Location of parotid preganglionic neurons in the inferior salivatory nucleus and their relation to the superior salivatory nucleus of rat

Abstract

Section snippets

Acknowledgements

Brain Res. Mol. Brain Res.

Brain Res.

Brain Res.

Brain Res.

Auton. Neurosci.

Neurosci. Lett.

Neuroscience

Brain Res.

Brain Res.

J. Auton. Nerv. Syst.