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The Journal of Neurophysiology Vol. 80 No. 1 July 1998, pp. 48-58
Copyright ©1998 by the American Physiological Society
Second Department of Orthodontics and Department of Physiology, Faculty of Dentistry, Tokyo Medical and Dental University, Tokyo 113-8549, Japan
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Ono, Takashi, Yasuo Ishiwata, Noritaka Inaba, Takayuki Kuroda, and Yoshio Nakamura. Modulation of the inspiratory-related activity of hypoglossal premotor neurons during ingestion and rejection in the decerebrate cat. J. Neurophysiol. 80: 48-58, 1998. Single-unit activities of the bulbar reticular inspiratory neurons directly projecting to hypoglossal motoneurons were studied during fictive ingestion (e.g., swallowing) and rejection elicited by repetitive stimulation of the superior laryngeal nerve and by application of water to the pharynx in immobilized decerebrated cats. The single-unit activity was recorded during 113 episodes of fictive ingestion from 25 inspiratory neurons directly projecting to hypoglossal motoneurons (single projection neurons) and 7 inspiratory neurons directly projecting to both hypoglossal and phrenic motoneurons (dual projection neurons) in the regions ventrolateral to the nucleus tractus solitarii and dorsomedial to the nucleus ambiguus. All of single projection neurons ceased inspiratory-related rhythmical discharges coincidentally with the onset of repetitive stimulation of the superior laryngeal nerve. The majority of them (19/25, 76%, type A) showed a spike burst during ingestion, whereas the minority (6/25, 24%, type B) kept silent until the end of repetitive stimulation of the superior laryngeal nerve. During fictive ingestion elicited by application of water to the pharynx, the type-A neurons showed a spike burst activity, whereas the type-B neurons kept silent. All dual projection neurons (7/7, 100%, type C) ceased inspiratory-related rhythmical discharges at the onset of repetitive stimulation of the superior laryngeal nerve and showed no activity during fictive ingestion. Likewise, the type-C neurons kept silent during fictive ingestion elicited by application of water to the pharynx. A spike burst was induced during 33 episodes of fictive rejection in all of 5 tested type-A, 3 tested type-B, and 6 tested type-C neurons. It is concluded that the premotor neurons involved in the respiratory-related rhythmical activity of hypoglossal motoneurons is responsible for switching from respiration to ingestion and rejection.
The tongue is a multifunctional organ participating in a variety of functions, such as sucking, licking, mastication, vocalization, respiration, and swallowing (Lowe 1981) Experiments were performed in 12 adult cats of either sex weighing 2.7-4.7 kg. The animal use protocol was reviewed and approved by the Screening Committee for Animal Research of Tokyo Medical and Dental University. From two days before the surgical procedures, animals were given a prophylactic dose of antibiotics. Chlorpromazine hydrochloride (2.0 mg/kg im) and atropine sulfate (0.1 mg/kg im) were initially administered; 30 min later, ketamine hydrochloride was given (40 mg/kg im). After the trachea and right superficial radial vein were canulated, halothane (1.5-2.0%) insufflation was started and continued throughout the surgical procedures.
EMG activity of the tongue muscles and the diaphragm during ingestion and rejection
A typical record of EMG activity of the extrinsic tongue muscles (i.e., the hyoglossus, the styloglossus, the geniohyoid, and the GG muscles) and the diaphragm during ingestion and rejection before immobilization is illustrated in Fig. 1. Repetitive SLN stimulation was applied to elicit swallowing (Fig. 1, downward arrows). Shortly after the cessation of repetitive SLN stimulation (Fig. 1, upward arrows), occurrence of swallowing was observed (Fig. 1, i). During swallowing, a burst activity was coincidentally observed in the styloglossus, the geniohyoid, and the GG muscles during expiration. No change was observed in the EMG activity of the diaphragm. When a volume of water was applied into the pharynx (Fig. 1, arrowhead), expulsive behavior was elicited. The most visible component of this rejection response was a large jaw opening (gape). During rejection (Fig. 1, r), a burst activity was coincidentally found in the hyoglossus, the styloglossus, the geniohyoid, and the GG muscles as well as the diaphragm. The amplitude of EMG activities of these muscles during rejection was significantly larger than those recorded during ingestion (swallowing). In addition, the duration of EMG activities of these muscles during rejection was significantly longer than that recorded during ingestion. The second episode of rejection was followed by swallowing characterized by simultaneous activation of the styloglossus, the geniohyoid, and the GG muscles.
Activity of bulbar inspiratory neurons during fictive ingestion
Single-unit activity was recorded from 25 respiratory neurons directly projecting to XII Mns (single projection neurons) and 7 neurons directly projecting to both XII and PH Mns via bifurcating axons (dual projection neurons) during fictive ingestion elicited by both SLN stimulation and water application to the pharynx after the animal was immobilized. All these neurons were inspiratory neurons.
Activity of bulbar inspiratory neurons during fictive rejection
Single-unit activities recorded from a type-A neuron and a type-B neuron during fictive rejection are illustrated in Fig. 4. Shortly after application of water (Fig. 4, A and B, arrows), a sporadic burst activity occurred in the XII and PH nerve discharges (Fig. 4, A and B, r). These episodes were regarded as fictive rejection and were distinguished from other behaviors, because 1) the same pattern of discharge in both the XII and PH nerves were demonstrated in association with a large mouth opening, or gape before the animal was immobilized (DiNardo and Travers 1994
Activity of bulbar inspiratory neurons during fictive swallow-breath
Weak activation in the PH nerve discharge occurs in association with swallowing, which is called swallow-breath (Dick et al. 1993
Classification of XII premotor neurons with inspiratory-related activity
In this study the behavior of 32 respiratory neurons in the regions vl-NTS and dm-AMB, which monosynaptically project either to XII Mns or to both the XII and PH Mns, was investigated during fictive ingestion and rejection. These respiratory neurons showed rhythmical burst activities in coincidence with the rhythmical discharge of the PH nerve. They antidromically responded to microstimulation of their respective motor nucleus. In addition, averaging of the rectified XII and PH nerve discharges with respect to spontaneous spikes of these respiratory neurons revealed an increase in the activity of either the XII nerve or both the XII and PH nerves. In the present study, we did not attempt to investigate modulation of respiratory neurons that projected to neither XII or PH Mns, nor those that projected only to PH Mns. Therefore it should be taken into account that the sampling of respiratory neurons was biased.
Patterns of activity of subpopulations of XII premotor neurons during fictive ingestion and rejection
Identification of motor activity elicited by repetitive SLN stimulation and water application to the pharynx before the animal was immobilized was somewhat difficult to interpret. Nevertheless, it is highly likely that the ingestive response with coactivation of the GG, the geniohyoid, and the styloglossus muscles represents buccopharyngeal phase of swallowing (Doty and Bosma 1956) Relationship between subpopulations of XII premotor neurons and XII Mns
Among extrinsic tongue muscles innervated by XII Mns, the GG, the styloglossus, and the geniohyoid muscles exhibit rhythmical discharges coincident with the inspiratory phase, whereas the hyoglossus muscle is more or less active during expiration in the cat (Horner 1996 Functional significance of XII premotor neurons with inspiratory-related activity
The type-A neurons ceased their inspiratory-related rhythmical activities at the onset of SLN stimulation, and kept silent during repetitive SLN stimulation until the advent of fictive ingestion. It can therefore be assumed that the type-A neurons are inactivated oligosynaptically by SLN stimulation, by their postsynaptic inhibition (Ballantyne and Richter 1991)
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
. Although some of these motor activities can occur simultaneously by utilizing the same motoneurons (Mns) as the output device (Bramble and Carrier 1983; Carter and Smith 1986a,b), others are mutually exclusive and cannot be simultaneously performed (Kaplan and Grill 1989; McFarland and Lund 1993; Weijnen et al. 1984). For instance, respiratory movements cease during swallowing, and the tongue activity coincidentally switches from the respiratory-related pattern to the swallowing-related one. It was proposed that this was probably because the central pattern generator (CPG) responsible for one motor act suppresses the activity of CPGs involved in the others (McFarland and Lund 1993; Smith and Denny 1990).
. It was suggested that the CPG for swallowing had effects on a subset of XII Mns involved in swallowing and delayed the generation of a lick cycle. DiNardo and Travers (1994) investigated the XII neural activity during ingestion (licking and swallowing) and rejection (gape) elicited by gustatory stimuli in the awake rat. They demonstrated that subsets of XII Mns were involved in switching of the motor activity from ingestion to rejection by changing their firing patterns, suggesting the overlapping between the XII premotor neurons that produce ingestion and rejection. However, the behavior of premotor neurons projecting to XII Mns (Amri et al. 1990; Manaker et al. 1992; Ono et al. 1994; Sumino and Nakamura 1974) has not been examined to date in relation to interaction of CPGs.
. Some of these inspiratory neurons had bifurcating axons projecting to both XII and phrenic (PH) Mns. We proposed that the heterogeneity of subpopulations of premotor neurons that project to XII and PH Mns may be involved not only in coordination of the activity of the tongue muscle and the diaphragm during spontaneous breathing but also in their differential responses to various stimuli.
; Gestreau et al. 1996; Grélot et al. 1992; Hooper and Moulins 1989; Huang and Satterlie 1990; Larson et al. 1994; McFarland and Lund 1993; Travers and Jackson 1992). In this study, single-unit activities of subpopulations of these XII premotor neurons with inspiratory-related activity were recorded during fictive ingestion and rejection as well as during spontaneous breathing. This was done to elucidate their roles in switching from one function to another within neuronal networks controlling the multiple functions of the tongue.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
1·h1) and artificially ventilated throughout the recording sessions. A bilateral pneumothorax was made to improve recording stability.
1.0 mm).
at 1 kHz) in the lower brain stem on the right side (from 3.0 mm rostral to 3.0 mm caudal to the obex in the rostrocaudal direction; from 1.5 mm to 4.5 mm lateral to the midline). Respiratory neurons projecting to the XII nucleus or both the XII and PH nuclei were identified by 1) a rhythmical firing activity corresponding with the respiratory cycle and 2) spike responses after a fixed short latency to microstimulation of the XII nucleus (<50 µA; duration, 0.1 ms) or both the XII and the PH (<100 µA; duration, 0.1 ms) nuclei, which showed collision with spontaneous spikes. During recording, the tracheal pressure and discharges in both the XII and PH nerves were simultaneously displayed on oscilloscopes after amplification and recorded on a tape recorder. Instantaneous firing frequency was obtained by inverting the duration between a spontaneous spike discharge and a succeeding one recorded from the respiratory neuron (i.e., 1,000 ms divided by an interspike interval in ms). To detect monosynaptic connection between the respiratory neuron and either the XII Mns or the XII Mns and PH Mns, spike-triggered averaging method was employed (Fedorko et al. 1989; Kirkwood and Sears 1973; Lipski et al. 1983). Spontaneous spike discharges of a respiratory neuron were fed to a window discriminator; the discriminated pulses were used to trigger the averager (Signal processor 7T07, San-ei, Tokyo, Japan) of simultaneously recorded XII and PH nerve discharges, which were full-wave rectified and integrated (time constant: 10 ms). Usually >2,000 sweeps were averaged with respect to trigger pulses.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 1.
Electromyographic activity of the hyoglossus, the styloglossus, the geniohyoid, the genioglossus muscles, and the diaphragm during ingestion (swallowing) and rejection (gape). Downward and upward arrows show the onset and offset of repetitive superior laryngeal nerve (SLN) stimulation, respectively. Arrowhead indicates the onset of water application. Three episodes labeled i and 2 episodes labeled r denote ingestion and rejection, respectively. HG, hyoglossus muscle; SG, styloglossus muscle; GH, geniohyoid muscle; GG, genioglossus muscle; DIA, diaphragm.
. In an early inspiratory phase, repetitive SLN stimulation was applied to elicit ingestion (Fig. 2, A and B, downward arrows). The respiratory-related rhythmical activity in the PH nerve disappeared half way to the peak (Fig. 2, A and B). Coincidentally the inspiratory neuron completely ceased firing, while the XII nerve discharge frequency exceeded its preceding inspiratory-related level. Shortly after the cessation of repetitive SLN stimulation (Fig. 2, A and B, upward arrows), a transient burst activity was observed in this inspiratory neuron. The burst consisted of spikes firing at a higher rate than the normal inspiratory discharge and was accompanied by a similar burst in the XII nerve discharge but not in the PH nerve discharge (Fig. 2, A and B, i). Because this pattern of discharge in the XII and PH nerves was the same as that seen in association with actual swallowing (ingestion) before paralysis (Fig. 1), the bursts were considered to represent a fictive ingestion (DiNardo and Travers 1994; Gestreau et al. 1996; Grélot et al. 1992; Jiang et al. 1991; Withington-Wray et al. 1988). The moment when the transient burst activity was present in the XII nerve, no activity was seen in the PH nerve discharge. In a total of 25 single projection neurons, 19 neurons showed this type of activity (type-A neurons), whereas the remaining 6 neurons showed no activity during fictive ingestion (type-B neurons).
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FIG. 2.
A-D: activity of a respiratory neuron directly projecting to hypoglossal (XII) motoneurons (Mns) during fictive ingestion. A: simultaneous record of extracellular spikes of a respiratory neuron, number of spike potentials per second (200 ms/bin), instantaneous firing frequency of spike potentials, rectified phrenic (PH) nerve discharge, rectified XII nerve discharge, and tracheal pressure (from top to bottom). Downward and upward arrows show the onset and offset of repetitive SLN stimulation, respectively. The episode labeled i denotes ingestion. B: record of the part underlined in A on an expanded time base. The episode labeled i denotes ingestion. Ca: fixed short-latency response of the respiratory neuron shown in A to stimulation of the contralateral XII nucleus (0.1 ms; 45 mA). Cb: collision of spikes with spontaneous spikes. Three sweeps (1 sweep with a fixed short-latency response and 2 sweeps with collision with spontaneous spikes) are superimposed in Ca and Cb. Spontaneous spike discharges within 0.5 ms before the onset of stimulation of the XII nucleus were collided with the antidromic spike discharge. The polarity of stimulus artifact was positive, whereas the polarity of spike discharge was negative-positive. D: averaging of rectified XII and PH nerve discharges by spontaneous spikes of the neuron shown in A-C. One thousand sweeps were averaged. Note a facilitation in the XII nerve discharge after a short latency, but not in the PH nerve discharge. IFF, instantaneous firing frequency; PH, rectified PH nerve discharge; XII, rectified XII nerve discharge; TP, tracheal pressure.
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FIG. 3.
A-E: activity of a respiratory neuron directly projecting to both the XII and PH Mns during fictive ingestion. A: simultaneous record of extracellular spikes of a respiratory neuron, number of spike potentials per second (200 ms/bin), instantaneous firing frequency of spike potentials, rectified PH nerve discharge, rectified XII nerve discharge, and tracheal pressure (from top to bottom). The episode labeled i denotes ingestion. B: record of the part underlined in A on an expanded time base. The episode labeled i denotes ingestion. Ca: fixed short-latency response of the respiratory neuron shown in A to stimulation of the contralateral XII nucleus (0.1 ms; 30 mA). Cb: fixed short-latency response of the same respiratory neuron to stimulation of the contralateral PH nucleus (0.1 ms; 12 mA). Three sweeps are superimposed in Ca and Cb. D: collision of spikes shown in Cb evoked by stimulation of the PH nucleus with spikes evoked by stimulation of the XII nucleus. Antidromic spike potentials evoked by stimulation of the PH nucleus persisted when stimulation of the XII nucleus preceded 3 ms (Da) and 2 ms (Db). When the interval was shortened to 1 ms (Dc), the antidromic spike potential evoked by stimulation of the PH nucleus was collided with that evoked by stimulation of the XII nucleus. The polarity of stimulus artifact was negative-positive, whereas the polarity of spike discharge was negative-positive. Three sweeps are superimposed. E: averaging of the rectified XII and PH nerve discharges by spontaneous spikes of the neuron shown in A-D. One thousand two hundred sweeps were averaged. Note the facilitation in both the XII and PH nerve discharges after short latencies.
; Grill and Norgren 1978; Travers and Norgren 1986) and 2) the magnitude of the XII nerve activity was larger than foregoing inspiratory-related activity. Although the magnitude of rejection seen in both the XII and PH nerve discharges was relatively less in Fig. 4A than that in Fig. 4B, these responses were qualitatively similar. In Fig. 4A, the type-A neuron showed an augmented burst activity during rejection. Likewise, a transient burst activity was observed in the type-B neuron coincidentally with the burst activity in both the XII and PH nerve discharges (Fig. 4B).
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FIG. 4.
A and B: activity of respiratory neurons directly projecting to XII Mns during fictive rejection. A: type-A neuron. B: type-B neuron. Simultaneous record of extracellular spikes of a respiratory neuron, XII nerve discharge, PH nerve discharge, and tracheal pressure are shown (from top to bottom). Downward arrows indicate the onset of water application. Two episodes labeled r denote rejection.
. Coincidentally with the characteristic activities in XII and PH nerve discharges, this inspiratory neuron fired at a higher frequency than its normal rhythmical bursting frequency. Slightly after the fictive rejection, smaller bursts were seen twice in the XII nerve discharge, but not in the PH nerve discharge (Fig. 5, i). These two episodes were considered to be fictive ingestion, because 1) the same patterns were observed in EMG activities of both the tongue muscles and the diaphragm during actual ingestion (swallowing) elicited by repetitive SLN stimulation before the animal was immobilized (Fig. 1), 2) the magnitude of the XII nerve activity was smaller than that recorded during rejection, and 3) it was reported that swallowing usually coincided with the expiratory phase of the breathing cycle in decerebrated cats (Dick et al. 1993). During fictive ingestion, this inspiratory neuron showed no activity.
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FIG. 5.
Simultaneous record of extracellular spikes of the respiratory neuron shown in Fig. 3, number of spike potentials per second (200 ms/bin), instantaneous firing frequency of spike potentials, rectified PH nerve discharge, rectified XII nerve discharge, and tracheal pressure during fictive rejection and ingestion. Arrow indicates onset of water application. Two episodes labeled i and an episode labeled r denote ingestion and rejection, respectively.
; Menon et al. 1984; Wilson et al. 1981). Figure 6 shows the pattern of activity of a type-B neuron shown in Fig. 4A during fictive swallow-breath. Shortly after application of water to the pharynx during inspiration (Fig. 6, arrow), a fictive rejection characterized by a transient burst activity in the XII and PH nerve discharges occurred (Fig. 6, r). In the following expiratory phase, a transient burst activity in the XII nerve associated with weak activity in the PH nerve discharge (Fig. 6, asterisk) was observed. This episode was regarded as a fictive swallow-breath. During fictive swallow-breath, two spike discharges were observed in the type-B neuron. The type-B neuron resumed phasic inspiratory-related activity thereafter.
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FIG. 6.
Activity of respiratory neurons directly projecting to XII Mns during fictive swallow-breath. Simultaneous record of extracellular spikes of a type-A neuron, XII nerve discharge, PH nerve discharge, and tracheal pressure are shown (from top to bottom). Downward arrow and an episode labeled r indicate the onset of water application and swallow-breath, respectively. Asterisk denotes swallow-breath.
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FIG. 7.
Activity of a respiratory neuron directly projecting to both the XII and PH Mns during swallow-breath and ingestion. Simultaneous record of extracellular spikes of a type-C neuron, XII nerve discharge, PH nerve discharge, and tracheal pressure are shown (from top to bottom). Downward arrow indicates the onset of water application. Asterisk denotes swallow-breath. Two episodes labeled i denote ingestion.
View this table:
TABLE 1.
Patterns of activity of the inspiratory neurons during fictive ingestion and rejection
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TABLE 2.
Numbers of analyzed episodes of fictive ingestion and rejection for three types of inspiratory neurons
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FIG. 8.
Schematic drawings of coronal sections of the brain stem, showing locations of neurons recorded in the present study. 
, type-A neurons (single projection neurons that showed a burst activity during fictive ingestion); 
, type-B neurons (single projection neurons that showed no activity during fictive ingestion); 
, type-C neurons (dual projection neurons that kept silent during fictive ingestion). AMB, nucleus ambiguus; DM, dorsal motor nucleus of the vagus; S, solitary tract; 5SP, spinal trigeminal nucleus; 5ST, spinal trigeminal tract; 12, hypoglossal nucleus.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
. The inspiratory neuron shown in Fig. 2 responded with antidromic spike potentials after a constant latency of 0.5 ms to stimulation of the contralateral XII nucleus. The conduction time between the soma of the inspiratory neuron and the stimulating electrode in the contralateral XII nucleus was estimated to be 0.3 ms, after 0.2 ms was subtracted as the utilization time (Jankowska and Roberts 1972a). The conduction time from the somata of XII Mns to the recording electrode on the XII nerve was estimated to be 1.0 ms, on the basis of the latency of the negative deflection of the antidromic field potential in the XII nucleus evoked by stimulation of the XII nerve minus 0.2 ms as the utilization time. If we assume a synaptic delay to be 0.3-0.4 ms (Jankowska and Roberts 1972b), the sum of conduction times in the inspiratory neuron (0.3 ms), the XII nerve (1.0 ms), and one synaptic delay (0.3-0.4 ms) amounts to 1.6-1.7 ms. Indeed, facilitation was observed in the XII nerve discharge 1.6 ms after the onset of the negative deflection of triggering spikes of the inspiratory neuron. Therefore the calculated latency corresponds well with the observed latency, within a difference too small for another neuron to be intercalated between the recorded inspiratory neuron and XII Mns. In contrast, no monosynaptic projection was found from this inspiratory neuron to PH Mns: neither antidromic spike response to stimulation in the PH nucleus nor facilitation in the PH nerve discharge was present. With respect to the remaining 24 inspiratory neurons that demonstrated facilitation in the XII nerve discharge, the latency of facilitation corresponded with the calculated monosynaptic latency within a difference of 0.2 ms. Thus we are led to conclude that there are monosynaptic excitatory projections from the recorded inspiratory neurons to XII Mns. A similar example of an inspiratory neuron that projected to XII Mns was shown in Fig. 4 in our previous study (Ono et al. 1994).
0.2 ms. Accordingly, it is concluded that these inspiratory neurons make monosynaptic excitatory projections to both XII and PH Mns. A similar example of an inspiratory neuron that projected to both XII and PH Mns was demonstrated in Fig. 5 in our previous study (Ono et al. 1994).
; Kirkwood and Sears 1973; Lipski et al. 1983) and cross-correlation (Cohen et al. 1974; Davies et al. 1985; Mateika and Duffin 1989). These studies revealed monosynaptic connections by demonstrating the peak with short latency (1.5-2.4 ms in Cohen et al. 1974; 2.5-4.5 ms in Mateika and Duffin 1989), short rise time (0.4-1.4 ms in Cohen et al. 1974; 0.5 ± 0.2 ms in Lipski et al. 1983), and short half-width (2.0 ± 0.7 ms in Lipski et al. 1983) in the nerve discharge. In Fig. 2, the rise time was 1.1 ms and the half-width was 3.1 ms. In Fig. 3, the rise time and half-width for the XII nerve discharge were 1.4 and 1.2 ms, respectively, whereas the rise time and half-width for the PH nerve discharge were 1.2 ms and 1.4 ms, respectively. These short rise time and half-width as well as the short latency comparable with those in previous studies are suggestive of presense of monosynaptic connection between inspiratory neurons and XII and PH Mns.
. However, it may not show the real proportion of neurons with bifurcating axons, because it is possible that single projection neurons and dual projection neurons may project to cranial and spinal Mns other than XII and PH Mns. In our previous study, 93% (25/27) and 7% (2/27) of the single projection neurons were antidromically activated by stimulation of contralateral and ipsilateral XII nucleus, respectively (Ono et al. 1994). Likewise, 86% (6/7) and 14% (1/7) of the dual projection neurons were antidromically activated by stimulation of contralateral and ipsilateral XII and PH nuclei, respectively. This is in accord with the previous study that showed contralateral dominance of monosynaptic projection of medullary inspiratory neurons to the PH Mns (Cohen et al. 1974). The above findings led us to investigate the contralateral projection of the inspiratory neurons in the present study. Nevertheless, the possibility could not be ruled out that the single projection neuron projects to the ipsilateral PH Mns because the projection to the contralateral spinal cord was only examined in the present study.
. What kind of motor act that accompanied spasmodic EMG activity in the tongue muscles as well as the diaphragm by applying a volume of water to the pharynx represent? We believe that it represents rejection (gape), because the animal shows a large mouth opening with a retrusive movement of the tongue with the tip pointing downward (DiNardo and Travers 1994; Travers and Norgren 1986). After the animal was immobilized, a volume of water applied to the pharynx elicited a rejection response followed by two episodes of ingestive response (Fig. 5). We believe that the rejection response indicates a fictive gape, because the PH nerve activity maintained a ramp-shaped discharge characteristic of respiration as opposed to other expulsive oropharyngeal movements such as coughing, vomiting, and sneezing (DiNardo and Travers 1994; Widdicombe 1986; Widdicombe et al. 1988).
studied intracellular activity of XII Mns during fictive swallowing in the cat. They found excitatory postsynaptic potentials that were followed by inhibitory postsynaptic potentials in some GG Mns and excitatory postsynaptic potentials in some styloglossus Mns. The type-A neurons may participate in eliciting these excitatory postsynaptic potentials. None of type-C neurons showed activity during fictive ingestion, suggesting that they do not appear to be involved in ingestion.
; Monges et al. 1978). In contrast, among the eight tested single projection neurons, all of five type-A neurons and all of three type-B neurons showed a burst activity during fictive rejection. This suggests that as a population both the type-A and the type-B neurons may participate in rejection. If this is the case, the type-A neurons may project to the XII Mns that are involved in producing the inverse behavioral functions, ingestive and rejection responses. Alternatively, the type-B neurons may project to the XII Mns that are involved in rejection but not in ingestion. This assumption is in accord with the existence of multifunctional neuronal network serving distinct functions such as breathing, coughing, and swallowing (DiNardo and Travers 1994; Gestreau et al. 1996).
; Ono et al. 1990). On the other hand, during swallowing the styloglossus and the geniohyoid muscles are active, whereas the hyoglossus muscle is inactive (Fig. 1). Several EMG investigations in humans have demonstrated that the GG muscle participates in swallowing (Cunningham and Basmajian 1969; Lowe et al. 1977; Vitti et al. 1975). However, it is still controversial whether the GG muscle is obligatory for swallowing in animals. It was reported that the GG muscle was generally inactive during swallowing in the sheep (Amri et al. 1989). Miller and Bowman (1974) suggested that GG motor units were recruited by the respiratory CPG, and intermittently by the swallowing CPG. Because the GG muscle contains muscle fibers that run spokewise in the tongue, different parts of the GG muscle that are innervated by different subsets of the GG Mns (Sauerland and Harper 1976) may serve differently in several respiratory-related activities. The EMG activity may not always represent the activity of a single muscle because the activity recorded from a given electrode site is indicative of the electrical activity of muscle fibers in the region of the electrode (English and Weeks 1989). Variations in experimental technique such as the difference in locations of electrode placement in the GG muscle may account for some of the different findings with respect to involvement of the GG muscle in swallowing. Although the present study has not been able to determine to which XII Mns the recorded inspiratory neurons project, the type-A neurons may be assumed to project to those XII Mns that innervate tongue muscles involved in both ingestion and rejection as well as inspiration, i.e., tongue muscles such as the GG, the geniohyoid, and the styloglossus muscles. In contrast, both the type-B and type-C neurons may project to the XII Mns innervating tongue muscles participating in rejection and inspiration, i.e., a part of the GG muscle that does not participate in ingestion. However, because the size of our sample is small, the patterns of projection and the possible functional differences between the type-C neurons and previously reported bulbospinal inspiratory neurons as well as between the type-A and type-B neurons require further investigation.
and/or by their disfacilitation due to abolition or decrease in excitatory inputs from the respiratory CPG, which is polysynaptically inactivated. This inactivation may be more or less sustained during repetitive SLN stimulation. In addition, afferent impulses evoked by SLN stimulation would activate the swallowing CPG that is postulated to be located in the hindbrain (Jean 1972a,b; Jean and Car 1979; Kessler and Jean 1985; Miller 1982; Roman 1986). When the activity of the CPG for ingestion reaches a certain level, patterned excitatory commands for ingestion may be issued to the type-A neurons, resulting in a transient burst activity in XII Mns unaccompanied by the PH Mn activity. This assumption is in accord with the respiratory-related intracellular activity of XII Mns during repetitive SLN stimulation in the cat (Withington-Wray et al. 1988). They reported depolarization of the XII Mn in the absence of the PH nerve activity. It is also in agreement with the simultaneous record of jaw movements and muscle activities, in which the interaction between respiratory and ingestion CPGs has been shown (McFarland and Lund 1993). Larson et al. (1994) demonstrated that some of the respiratory neurons in the ventral medulla were involved in coordination between swallowing and vocalization. They classified respiratory neurons by patterns of discharge; however, whether these neurons were interneurons or motoneurons was not studied. Recently, Gestreau et al. (1996) recorded intracellular potentials from inspiratory neurons in the NTS region during fictive coughing and swallowing. Although some of them were bulbospinal premotor neurons, their possible projection to medullary motoneurons including XII Mns were not studied. With regard to the activity of XII Mns during ingestion and rejection, DiNardo and Travers (1994) have shown functional overlap between subsets of XII Mns producing ingestion and rejection, and consequently, they have emphasized the involvement of premotor substrates in the medullary reticular formation in the production of ingestion and rejection.
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ACKNOWLEDGEMENTS |
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We are grateful to Dr. Kathleen A. Ferguson for valuable discussion and editorial suggestion in the initial preparation of the manuscript.
This work was supported by Grants-in-Aid for Scientific Research Projects and 02954164 and 01480427 from the Japanese Ministry of Education, Science and Culture. T. Ono was a recipient of a Japan Society for the Promotion of Science Fellowship for Junior Scientists.
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FOOTNOTES |
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Address for reprint requests: T. Ono, Second Dept. of Orthodontics, Faculty of Dentistry, Tokyo Medical and Dental University, 5-45 Yushima 1-chome, Bunkyo-ku, Tokyo 113-8549, Japan.
Received 24 September 1997; accepted in final form 3 April 1998.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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neurons on phrenic motoneurons studied with spike-triggered averaging.
Brain Res.
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 A. Jean Brain Stem Control of Swallowing: Neuronal Network and Cellular Mechanisms Physiol Rev, April 1, 2001; 81(2): 929 - 969. [Abstract] [Full Text] [PDF]
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 A. Sawczuk and K.M. Mosier Neural Control of Tongue Movement With Respect To Respiration and Swallowing Critical Reviews in Oral Biology & Medicine, January 1, 2001; 12(1): 18 - 37. [Abstract] [Full Text] [PDF]
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 Y. Ishiwata, T. Ono, T. Kuroda, and Y. Nakamura Jaw-Tongue Reflex: Afferents, Central Pathways, and Synaptic Potentials in Hypoglossal Motoneurons in the Cat Journal of Dental Research, August 1, 2000; 79(8): 1626 - 1634. [Abstract] [PDF]
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T. Ono, Y. Ishiwata, T. Kuroda, and Y. Nakamura Suppression of Jaw-opening and Trigemino-hypoglossal Reflexes during Swallowing in the Cat Journal of Dental Research, November 1, 1999; 78(11): 1720 - 1726. [Abstract] [PDF]
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 K. Shiba, I. Satoh, N. Kobayashi, and F. Hayashi Multifunctional Laryngeal Motoneurons: an Intracellular Study in the Cat J. Neurosci., April 1, 1999; 19(7): 2717 - 2727. [Abstract] [Full Text] [PDF]
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