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Bradley RM, editor. The Role of the Nucleus of the Solitary Tract in Gustatory Processing. Boca Raton (FL): CRC Press/Taylor & Francis; 2007.

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The Role of the Nucleus of the Solitary Tract in Gustatory Processing.

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Chapter 4Reflex Connections

and .

4.1. INTRODUCTION

The NST plays a pivotal role as a portal of entry of visceral and sensory information arising from the gut, cardiorespiratory, somatosensory, and taste systems. The role of the NST in autonomic and circulatory control has been recently reviewed [1,2] but connections from the NST to brainstem motor systems responsible for muscle activity related to feeding and salivary secretion have only recently received attention. Studies of the neurons and synaptic connections between taste afferent input and preganglionic neurons controlling the salivary glands are limited. And although there is considerable anatomical knowledge of the circuits connecting the rostral NST (rNST) to the orofacial motor neuron pools, details of the neurobiology of the synaptic connections remain to be studied. Despite this paucity of information, some functional properties of the reflex connections between the rNST and brainstem motor and preganglionic secretomotor neurons are known and are reviewed here.

Gustatory information processed by the rNST is distributed to a number of brain locations. By far the most studied is the rostral connection via the parabrachial nucleus to higher brain centers responsible for sensory and hedonic gustatory processing. However, just as important are connections to brainstem loci that are the basis of a number of reflex activities [3,4]. During feeding, several oral-motor behaviors are initiated, such as chewing, licking, and swallowing. These motor behaviors are organized at the brainstem level and can occur even after decerebration. Another reflex involves the facial expressions that occur in response to taste stimuli. Both humans and rats make stereotypical facial expressions to taste qualities and these have been extensively studied and used as a behavioral measure of taste hedonics [5]. In humans, these expressions can be elicited at birth before any experience of taste stimuli has occurred and are, therefore, considered to be innate, implying developmentally determined rNST circuits [6].

Moreover, this reflex behavior is retained in decerebrate animals, again indicating innate brainstem circuits [7]. Finally, saliva is secreted in response to taste and somatosensory oral stimulation. Because salivary secretion is solely initiated in response to activation of the autonomic nerve supply to the salivary glands [8], sensory information from the oral cavity must form the afferent limb of this reflex. The gustatory component of these essential reflexes, therefore, is processed and initiated by the rNST and reflects complex neural mechanisms that occur when sensory information arrives at the nucleus.

4.2. NEUROMUSCULAR-RELATED REFLEX ACTIVITY

As early as 1909, Ramón Y Cajal [9] described the neuromuscular reflex activity initiated by feeding. He states

“Imagine that food acts as a stimulus on lingual and glossopharyngeal nerve endings. As indicated in Figure 4.1 [see also Figure 1 in Miller [3],], impulses course along the two nerves to their respective ganglia and then along the central branches to the corresponding medullary sensory nuclei, where the two nerves give rise to abundant collaterals. Within these nuclei, impulses pass from the collaterals to cells that are contacted by the collaterals, and then to the axon of cells in the sensory nuclei. As is well known, these axons form the central (second order) pathways associated with the trigeminal and glossopharyngeal nerves. Collaterals arising from these pathways distribute impulses to hypoglossal neurons, and the tongue muscles contract. It is quite likely that this circuit mediates the various reflexes activated by inputs from the lingual nerve, including chewing, swallowing, sucking, and so on.” (Translated by Swanson and Swanson [10].)

FIGURE 4.1. Diagram by Cajal showing the direction of current flow through the trigeminal, glossopharyngeal, and vagus nerves.

FIGURE 4.1

Diagram by Cajal showing the direction of current flow through the trigeminal, glossopharyngeal, and vagus nerves. The glossopharyngeal nerve (IX) is shown forming the descending solitary tract (c) and as indicated by the arrow conducts information to (more...)

Thus, Cajal had already defined the basic reflex circuit from sensory endings in the dorsal tongue mucosa to the hypoglossal motor nucleus. Note that the sensory contribution of the facial nerve input is missing from Cajal’s diagram, because at the time he published his description, there was still some confusion regarding the contribution of the sensory part of the facial nerve to the solitary tract and nucleus (see Chapter 1). Cajal also failed to detail the contribution of gustatory and somatosensory input to the hypoglossal reflex. Functional details of the reflex circuits described by Cajal inspired a number of later investigators.

4.2.1. Physiological Investigations of Gusto-Lingual Reflexes

The physiological study of reflex orofacial activity was pioneered by Sherrington [11,12], who noted in decerebrate cat preparations that mechanical stimulation of the tongue filiform papillae resulted in tongue movements. Electrical stimulation of the combined chorda-lingual nerve, which contains the afferent fibers innervating both taste and somatosensory receptors, also resulted in reflex tongue movement. Thus, the afferent limb described in Cajal’s anatomical descriptions of reflex tongue movements was established. Electrical stimulation of the chorda-lingual nerve evokes neural discharges in the hypoglossal nerve with a latency of 7 ms as well as synaptic potentials in the hypoglossal motoneurons [13,14]. Based on this latency, only two synapses are involved in the reflex, and one of these is between the afferent fibers and either the NST or trigeminal sensory nuclei, leading to the conclusion that only one internuncial relay is involved in this reflex [15]. Synaptic potentials and reflex discharges in the hypoglossal motoneurons were also elicited by mechanical stimulation of the dorsal tongue surface [15,16]. A similar tongue reflex can be elicited by stimulation of the glossopharyngeal nerve with a slightly longer latency [17].

In most of these earlier studies, either tactile or nociceptive stimulation is assumed to be the sensory system responsible for the afferent limb of the reflex, although Porter [14] entertained the possibility that chorda tympani fibers might be activated by the lingual nerve stimulation. Kawamura [18] suggested that other sensory modalities besides tactile stimulation may also be important in feedback regulation of tongue movements. This suggestion was subsequently tested by Yamamoto [19] using mechanical, gustatory, and thermal stimuli to demonstrate that application of KCl, NaCl, HCl, and cooling stimuli to the tongue all evoked efferent neural activity in the hypoglossal nerve (Figure 4.2). However, these taste-initiated reflex activities in the hypoglossal nerve had very long latencies (mean = 6 sec) that do not compare to the behavioral latencies, throwing some doubt on the significance of the electrophysiological experiments. In behavioral experiments, Weiffenbach and Thach [20] and Nowlis [21] reported that drops of glucose solution applied to the tongue tip in infants elicited lateral tongue movements after a short latency (Weiffenbach, personal communication). Moreover, in both the animal and human studies, these tongue reflex responses could be elicited without the involvement of rostral brain centers [6].

FIGURE 4.2. Electrophysiological responses evoked in the rat hypoglossal nerve to taste and thermal stimuli applied (indicated by the arrow) to the tongue.

FIGURE 4.2

Electrophysiological responses evoked in the rat hypoglossal nerve to taste and thermal stimuli applied (indicated by the arrow) to the tongue. (Reprinted from Yamamoto, T., Brain Res., 92, 499–504, 1975, with permission from Elsevier.)

4.2.2. Physiological Investigations of Gusto-Facial Reflexes

Little information is available on the functional connections between afferent taste input and motoneurons in the facial nucleus responsible for the stereotypical responses to taste stimuli. Most of the projections to the facial motor nucleus originate from neurons in the reticular formation [22] but some derive from the trigeminal complex [23,24], and even fewer connections are reported projecting from the NST [25,26]. However, experiments with lesioned decerebrate animals demonstrate that the circuits responsible for mimetic responses to taste stimuli are at the brainstem level [7]. The results of lesions in NST and PBN indicate marked changes in the taste reactivity test elicited by taste stimuli [27]. Facial nerve responses to tongue stimulation with taste stimuli have been reported, and neural activity elicited by citric acid and NaCl occurs after a short latency [6]. However, these experiments were very preliminary and merit further analysis in additional animals.

4.3. GUSTO-SALIVARY REFLEX ACTIVITY

A key component of the oral milieu is saliva secreted by the major and minor salivary glands. Saliva, although mainly consisting of water, has numerous functions [28,29], such as providing the lubrication necessary for movements of speech, mastication, and swallowing. It provides a buffer to stabilize intraoral pH. An indication of the importance of saliva for oral health is demonstrated when it is absent or reduced, resulting in a fetid mouth due to intraoral bacterial proliferation. Beside these numerous vital functions, saliva is essential in the initial stages of taste transduction, because it acts as a solvent for taste stimuli, a transport medium for the dissolved stimuli, and a possible source of ions that pass through taste receptor apical ion channels to depolarize or hyperpolarize taste receptor cells.

4.3.1. Taste-Initiated Reflex Secretion of Saliva from the Major Salivary Glands

To provide the saliva necessary for these functions, stimulation of taste receptors reflexly initiates saliva flow [30,31]. The reflex does not merely switch the flow of saliva on and off, but is influenced by the sensory properties of the stimulus. For example, citric acid stimulation initiates high salivary flow rates rich in bicarbonate acting as a buffer, whereas sweet-tasting stimuli result in a lower flow rate of saliva containing salivary amylase [32–35]. Moreover, this modality-specific reflex activity occurs in decerebrate animals [36]. Most of these results were obtained in anesthetized animals; in experiments investigating reflex salivary secretion in awake, behaving animals, some interesting differences were reported [37]. For example, recordings of salivary flow and licking behavior reveal that salivary flow is greatest during grooming behavior (Figure 4.3A) and while eating pellet food (Figure 4.3B) and is considerably less with sweet, sour, and salty stimuli (Figure 4.3C). Interestingly, salivary flow to taste stimuli was highest after quinine infusion into the oral cavity (Figure 4.3Da and 4.3Db), presumably in an effort to remove the aversive stimulus from the mouth. However, because the animals used in these studies are awake, forebrain centers involved in the control of feeding may also contribute to the control of the salivary nucleus neurons in the brainstem.

FIGURE 4.3. Recordings of submandibular salivary secretion, jaw movement, and licking from an unanesthetized rat.

FIGURE 4.3

Recordings of submandibular salivary secretion, jaw movement, and licking from an unanesthetized rat. Each tracing consists of salivary flow rate (Salivation), electo-myographic activity of the left and right masseter muscles (L Mass, R Mass), and licking (more...)

4.3.2. Taste-Initiated Reflex Secretion of Saliva from von Ebner’s Salivary Glands

Although salivary secretion from the major salivary glands is important to provide saliva bathing the oral mucosa, taste buds in the circumvallate and foliate papillae are situated in clefts in the tongue surface. Von Ebner’s lingual salivary glands drain into the clefts of these papillae and are responsible for providing the microenvironment of the taste buds. Taste stimuli reach the circumvallate and foliate taste buds via the diffusion pathway provided by von Ebner’s gland secretions, and the glands are also responsible for flushing out taste stimuli as well as maintaining a healthy cleft environment. Thus, there is cooperative interaction between the taste buds in the circumvallate and foliate papillae and von Ebner’s gland secretions. This interaction was examined by taking advantage of the fact that the single centrally placed circumvallate papilla in the rat is bilaterally innervated. Recordings of taste stimulation of the circumvallate papilla could be made from one glossopharyngeal nerve while saliva flow to the papilla cleft was initiated by electrical stimulation of the contralateral glossopharyngeal nerve [38]. Salivary secretion from von Ebner’s glands significantly reduced taste responses to stimulation of the circumvallate papilla by taste stimuli (Figure 4.4). Because the reduction in taste responses was blocked by the parasympathetic antagonist atropine, which acts at the gland synapses, the reduction in taste response was concluded to be due to saliva flow washing the stimulus from the receptors.

FIGURE 4.4. (A) Summated whole-nerve recordings of ipsilateral glossopharyngeal nerve responses to 0.

FIGURE 4.4

(A) Summated whole-nerve recordings of ipsilateral glossopharyngeal nerve responses to 0.5 M NH4Cl, citric acid, KCl, and NaCl applied to the circumvallate papilla in a rat. During the recording of the taste response, the contralateral glossopharyngeal (more...)

4.3.3. Brainstem Salivatory Nuclei

The gustatory-salivatory reflexes involve afferent input to the rNST that then synapses with parasympathetic secretomotor neurons innervating the salivary glands. The parasympathetic preganglionic neurons controlling the salivary glands are collected in a column of brainstem neurons termed the salivatory nuclei. Efferent axons of the preganglionic neurons synapse with cells in peripheral autonomic ganglia that then send axons to synapse with the secretory cells of the salivary glands [39]. The parasympathetic neurons integrate input from both the rNST and forebrain areas and form the final common pathway to the salivary glands.

Numerous pathway tracing and electrical stimulation studies have defined the efferent connections from the brainstem to the salivary glands [40]. The salivatory nuclei are divided into a superior and inferior division based on the association of their preganglionic axons with a cranial nerve. There is no anatomical demarcation between the superior and inferior divisions of the salivatory nuclei. Cell bodies of preganglionic fibers innervating the submandibular and sublingual salivary glands form the superior salivatory nucleus (SSN) with efferent fibers that travel with the chorda tympani nerve (VII) to the glands. Cell bodies of preganglionic fibers innervating the parotid and von Ebner’s glands form the inferior salivatory nucleus (ISN) with efferent fibers that travel with the glossopharyngeal nerve (IX) to the glands (Figure 4.5).

FIGURE 4.5. Schematic of the parasympathetic innervation of the salivary glands.

FIGURE 4.5

Schematic of the parasympathetic innervation of the salivary glands. The cell bodies of the secretomotor neurons lie in the salivatory nucleus situated adjacent and medio-ventral to the solitary nucleus. Efferent axons from the salivatory neurons travel (more...)

4.3.4. Neurobiology of the Salivatory Neurons

Neurons of the ISN are situated along the medial border of the rNST (Figure 4.6A). They have been subjected to detailed morphological analysis and found to vary in the complexity of their dendritic trees [41]. Neurons of the ISN innervating the parotid and von Ebner’s glands consist of two separate cell groups; the most ventral in the nucleus supplies von Ebner’s glands, whereas the more dorsal neurons innervate the parotid gland (Figure 4.7). The parotid preganglionic neurons are also larger than the neurons innervating von Ebner’s glands (Figure 4.8). Dendrites of the salivatory neurons penetrate into the rNST, facilitating synaptic contacts, and a few ISN neurons are actually situated within the rNST (Figure 4.6B). By double-labeling the afferent input to the rNST and the neurons of the ISN, afferent fibers are seen to travel to the ISN neurons, suggesting monosynaptic connections between the afferent taste fibers and the parasympathetic efferent neuron (Figure 4.9)

FIGURE 4.6. (A) Horizontal section through the rat brainstem showing the nucleus of the solitary tract (NST) and retrogradely labeled neurons of the inferior salivatory nucleus (ISN).

FIGURE 4.6

(A) Horizontal section through the rat brainstem showing the nucleus of the solitary tract (NST) and retrogradely labeled neurons of the inferior salivatory nucleus (ISN). Rostral is towards the top of the figure. IV, fourth ventricle; ST, solitary tract. (more...)

FIGURE 4.7. Confocal images of inferior salivatory nucleus neurons (ISN).

FIGURE 4.7

Confocal images of inferior salivatory nucleus neurons (ISN). Neurons innervating the parotid gland were labeled with a green fluorescent tracer, and neurons innervating von Ebner’s glands were labeled with a red fluorescent tracer. The left column (more...)

FIGURE 4.8. Histograms comparing the morphometric characteristics of inferior salivatory neurons innervating the parotid and von Ebner’s salivary glands.

FIGURE 4.8

Histograms comparing the morphometric characteristics of inferior salivatory neurons innervating the parotid and von Ebner’s salivary glands. The parotid gland neurons were labeled via the otic ganglion (Otic) and von Ebner’s gland neurons (more...)

FIGURE 4.9. Merged confocal image of the contribution of the glossopharyngeal nerve to the solitary tract (red, ST) and ISN neurons innervating von Ebner’s gland (green).

FIGURE 4.9

Merged confocal image of the contribution of the glossopharyngeal nerve to the solitary tract (red, ST) and ISN neurons innervating von Ebner’s gland (green). The fibers of the solitary tract give off collateral branches, some of which reach the (more...)

Attempts have been made to study synaptic connections between the afferent input and the salivatory nucleus neurons. Because the parasympathetic fibers travel in the chorda tympani and glossopharyngeal nerves, salivatory neurons can be electrophysiologically identified by antidromic electrical stimulation [42–44]. It was found that electrical stimulation resulted in the generation of a few action potentials with variable latency ranging from 10 to 85 ms, suggesting that the gustatory reflex involves multiple synapses between the afferent input and the efferent output. However, it was not possible to confirm whether the recordings actually originated from salivatory neurons using this methodology. More recently, by prelabeling ISN and SSN neurons, it has become possible to identify them in brain slices and make whole-cell recordings from the neurons [45,46]. Recordings from identified neurons of the salivatory nuclei have demonstrated that the postsynaptic potentials initiated by stimulation of the solitary tract or adjacent neuropil are a mixture of excitation and inhibition (Figure 4.10) [47,48]. Applications of synaptic agonists and antagonists have revealed that the excitatory component is mediated by NMDA and AMPA glutamate receptors and that inhibition results from stimulation of GABAA receptors [47,49]. Glycinergic receptors have been demonstrated on some salivatory neurons, also [47]. Somata and dendrites of salivatory neurons receive symmetric synapses from glutamatergic, GABA, and glycine immunoreactive varicosities [50]. Salivatory nucleus neurons were shown to express NMDA, AMPA, and kainate glutamate receptor subtypes. Labeling by NMDA receptor subtypes was especially prominent. NR2B stained the nuclei strongly, whereas NR1, NR2A, and GluR1 receptor subtypes were also expressed in the dendrites, as well as the neuron cell bodies [51]. Based on the neurophysiological measures, these excitatory and inhibitory synapses either are monosynaptic connections between primary afferent fibers or involve polysynaptic connections via neurons in the rNST [49].

FIGURE 4.10. Excitatory postsynaptic currents (EPSC) recorded from neurons of the superior salivatory nucleus.

FIGURE 4.10

Excitatory postsynaptic currents (EPSC) recorded from neurons of the superior salivatory nucleus. Synaptic currents were evoked by electrical stimulation close to the neuron. (A)(a) Total current recorded at potentials between –90 and +50 mV voltage (more...)

The salivary reflex is also influenced by descending input from higher brain centers [30], and a number of neuropeptides have been hypothesized to be involved in this descending modulation of secretion as demonstrated by strong immunoreactivity for substance P, serotonin (5HT), neuropeptide Y, somatostatin, tyrosine hydroxylase, vasoactive intestinal peptide, and calcitonin gene-related peptide [52]. Of these neuropeptides, substance P and 5HT have been shown to excite salivatory neurons in a concentration-dependent manner [53,54].

4.4. FUTURE DIRECTIONS

Neurobiologists have long used reflex activity to probe the function of neural circuits, and because there are several well-defined reflexes that involve the NST, it will be possible to use these reflexes to define how the NST functions. In particular, gustosalivary reflexes seem ideal for this purpose. The afferent limb consists of input from somatosensory and gustatory receptors, and the motor output is made up of parasympathetic secretomotor neurons. Using brain slices, the afferent input can be stimulated, and by prelabeling the parasympathetic neurons, the efferent limb of the reflex arc can be visualized for recording. Indeed, this has already been utilized by the Bradley group as well as Matsuo’s group in Japan. The task ahead is to define the role of the rNST neurons in this reflex. Because various taste modalities are known to initiate different types of saliva, it will be important to determine the underlying connections responsible for these differences. For example, because acid stimuli initiate high flow rates of saliva concentrated with bicarbonate buffer, is it possible that acid-best fibers make direct monosynaptic contacts with the parasympathetic neurons? Are the afferent inputs segregated so that some connect to rostral directed taste pathways, while others are connected to salivatory nucleus neurons? What are the roles of descending connections to the salivatory nucleus neurons and how do they interact with the ascending input? Much recent experimental evidence has indicated that the rNST is not a simple relay nucleus, and study of these reflexes will contribute much new knowledge to our understanding of how complex the rNST really is.

ACKNOWLEDGMENT

The preparation of this chapter was supported in part by NIH grant DC 000288 from the National Institute on Deafness and Other Communication Disorders to R. M. Bradley.

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Copyright © 2007, Taylor & Francis Group, LLC.
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