Activation of 5-Hydroxytryptamine Type 3 Receptor-Expressing C-Fiber Vagal Afferents Inhibits Retrotrapezoid Nucleus Chemoreceptors in Rats

2007 ◽  
Vol 98 (6) ◽  
pp. 3627-3637 ◽  
Author(s):  
Thiago S. Moreira ◽  
Ana C. Takakura ◽  
Eduardo Colombari ◽  
Patrice G. Guyenet
Keyword(s):  
Inhibitory Effect ◽  
Vagal Afferents ◽  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
Lung Inflation ◽  
Retrotrapezoid Nucleus ◽  
Carotid Bodies ◽  
C Fiber ◽  
Limited Degree ◽  
Type 3

Retrotrapezoid nucleus (RTN) chemoreceptors are regulated by inputs from the carotid bodies (CB) and from pulmonary mechanoreceptors. Here we tested whether RTN neurons are influenced by 5-hydroxytryptamine type 3 receptor-expressing C-fiber vagal afferents. In urethan-anesthetized rats, selective activation of vagal C-fiber afferents by phenylbiguanide (PBG) eliminated the phrenic nerve discharge (PND) and inhibited RTN neurons ( n = 24). PBG had no inhibitory effect in vagotomized rats. Muscimol injection into the solitary tract nucleus, commissural part, reduced inhibition of PND and RTN by PBG (73%), blocked activation of PND and RTN by CB stimulation (cyanide) but had no effect on inhibition of PND and RTN by lung inflation. Bilateral injections of muscimol into interstitial solitary tract nucleus (NTS) reduced the inhibition of PND and RTN by PBG (53%), blocked the inhibitory effects of lung inflation but did not change the activation of PND and RTN neurons by CB stimulation. PBG and lung inflation activated postinspiratory neurons located within the rostral ventral respiratory group (rVRG) and inhibited inspiratory and expiratory neurons. Bilateral injections of muscimol into rVRG eliminated PND and partially decreased RTN neuron inhibition by PBG (32%). In conclusion, activation of cardiopulmonary C-fiber afferents inhibits the activity of RTN chemoreceptors. The pathway relays within a broad medial region of the NTS and involves the rVRG to a limited degree. The apnea triggered by activation of cardiopulmonary C-fiber afferents may be due in part to a reduction of the activity of RTN chemoreceptors.

GABAergic Pump Cells of Solitary Tract Nucleus Innervate Retrotrapezoid Nucleus Chemoreceptors

2007 ◽  
Vol 98 (1) ◽  
pp. 374-381 ◽  
Author(s):  
Ana C. Takakura ◽  
Thiago S. Moreira ◽  
Gavin H. West ◽  
Justin M. Gwilt ◽  
Eduardo Colombari ◽  
...  
Keyword(s):  
Area Postrema ◽  
Inhibitory Neurons ◽  
Acid Decarboxylase ◽  
Solitary Tract ◽  
Vagus Nerves ◽  
Toxin B ◽  
Lung Inflation ◽  
Retrotrapezoid Nucleus ◽  
Nucleus Of Solitary Tract ◽  
Tracheal Pressure

The retrotrapezoid nucleus (RTN) contains central respiratory chemoreceptors that are inhibited by activation of slowly adapting pulmonary stretch receptors (SARs). Here we examine whether RTN inhibition by lung inflation could be mediated by a direct projection from SAR second-order neurons (pump cells). Pump cells ( n = 56 neurons, 13 rats) were recorded in the nucleus of solitary tract (NTS) of halothane-anesthetized rats with intact vagus nerves. Pump cells had discharges that coincided with lung inflation as monitored by the tracheal pressure. Their activity increased when end-expiratory pressure was raised and stopped instantly when ventilation was interrupted in expiration. Many pump cells could be antidromically activated from RTN (12/36). Nine of those were labeled with biotinamide. Of these nine cells, eight contained glutamic acid decarboxylase 67 (GAD67) mRNA and seven were found to reside in the lower half of the interstitial subnucleus of NTS (iNTS). Using the retrograde tracer cholera toxin-B, we confirmed that neurons located in or close to iNTS innervate RTN (two rats). Many such neurons contained GAD67 mRNA and a few contained glycine transporter2 (GLYT2) mRNA. Anterograde tract tracing with biotinylated dextranamide (four rats) applied to iNTS also confirmed that this region innervates RTN by a predominantly GABAergic projection. This work confirms that many rat NTS pump cells are located in and around the interstitial subnucleus at area postrema level. We demonstrate that a GABAergic subset of these pump cells innervates the RTN region. We conclude that these inhibitory neurons probably contact RTN chemoreceptors and mediate their inhibition by lung inflation.

Role of bronchopulmonary C-fiber afferents in the apneic response to cigarette smoke

1987 ◽  
Vol 63 (4) ◽  
pp. 1366-1373 ◽  
Author(s):  
L. Y. Lee ◽  
E. R. Beck ◽  
R. F. Morton ◽  
Y. R. Kou ◽  
D. T. Frazier
Keyword(s):  
Cigarette Smoke ◽  
Control Level ◽  
Vagal Afferents ◽  
Smoke Inhalation ◽  
Coolant Temperature ◽  
Positive Pressure ◽  
Base Line ◽  
Lung Inflation ◽  
C Fiber

The role of vagal bronchopulmonary C-fiber afferents in eliciting the immediate changes in breathing pattern after acute inhalation of cigarette smoke was assessed with a selective blockade of myelinated vagal afferents (innervating both stretch and irritant receptors) utilizing the method of differential cooling. In 15 of 17 chloralose-anesthetized dogs tested, spontaneous inhalation of cigarette smoke (19.7% avg conc, 500–700 ml vol) reproducibly caused the following immediate responses: apnea, bradycardia, and hypotension. These responses occurred within 1 to 2 breaths of smoke inhalation and were followed by a delayed hyperpnea. The apneic duration reached 326 +/- 33% (SE) (n = 15) of the mean base-line expiratory duration. Differential cold block of both vagi (coolant temperature 8.4 +/- 0.3 degrees C) abolished the reflex apnea induced by a positive-pressure (7–10 cmH2O) lung inflation but did not affect the apneic response to smoke inhalation (345 +/- 35%). The smoke-induced apnea was completely abolished by lowering the coolant temperature to -1.3 +/- 0.2 degrees C (n = 10) or by bilateral vagotomy (n = 5) and returned to the control level after both vagi were rewarmed. Based on these results, we suggest that the immediate apneic response to inhaled cigarette smoke is elicited by a stimulation of vagal C-fiber afferents in the lungs and airways.

Acute effects of acrolein on breathing: role of vagal bronchopulmonary afferents

1992 ◽  
Vol 72 (3) ◽  
pp. 1050-1056 ◽  
Author(s):  
B. P. Lee ◽  
R. F. Morton ◽  
L. Y. Lee
Keyword(s):  
Inhibitory Effect ◽  
Acute Effects ◽  
Afferent Stimulation ◽  
Lung Inflation ◽  
Anesthetized Rats ◽  
C Fiber ◽  
Bilateral Vagotomy ◽  
Irritant Receptors

Spontaneous inhalation of acrolein vapor (350 ppm, 1 ml/100 g body wt) elicited an immediate and transient inhibitory effect on breathing in anesthetized rats, characterized by a prolongation of expiratory duration and accompanied by a bradycardia; ventilation was reduced by 47 +/- 6%, which returned to baseline after three to seven breaths. When both vagi were cooled to 6.6 +/- 0.1 degrees C, the reflex apneic response to lung inflation was completely abolished but the bradypneic response to acrolein was not affected. After perineural capsaicin treatment of both cervical vagi to selectively block the capsaicin-sensitive C-fiber afferents, acrolein no longer evoked an inhibitory effect on breathing; conversely, an augmented inspiration was consistently elicited with the first breath of acrolein inhalation, which was subsequently abolished by cooling both vagi to 6.5 degrees C. The inhibitory effect of inhaling acrolein at a lower concentration (200 ppm) was not detectable, whereas that of a higher concentration (600 ppm) was more intense and prolonged. All these responses were completely eliminated by bilateral vagotomy. These results suggest that inhaled acrolein activated both vagal C-fiber endings and rapidly adapting irritant receptors in the airways, but the acrolein-induced inhibitory effect on breathing was elicited primarily by the C-fiber afferent stimulation.

scholarly journals Leptin inhibits swallowing in rats

2006 ◽  
Vol 291 (3) ◽  
pp. R657-R663 ◽  
Author(s):  
Bernadette Félix ◽  
André Jean ◽  
Claude Roman
Keyword(s):  
Food Intake ◽  
Feeding Behavior ◽  
Wistar Rats ◽  
Leptin Receptor ◽  
Superior Laryngeal Nerve ◽  
Inhibitory Effect ◽  
Zucker Rats ◽  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
Leptin Receptors

Swallowing is under the control of premotoneurons located in the medullary solitary tract nucleus. Although rats with transected midbrain do not seek out food, they are able to ingest food present near the mouth, and acute food deprivation induces an increase in food intake. Leptin is a satiety signal that regulates feeding behavior. Because leptin receptors are found within the caudal brainstem, and because food intake is regulated in midbrain transected rats, this study tested the hypothesis that leptin is able to modify the activity of premotoneurons involved in swallowing. Leptin was microinjected at the subpostremal level of the medullary solitary tract nucleus in anesthetized Wistar rats. Electromyographic electrodes in sublingual muscles allowed recording of swallowing induced by stimulation of sensitive fibers of the superior laryngeal nerve. Repeated stimulation induced rhythmic swallowing. Microinjection of leptin (0.1 pg and 0.1 ng) in the swallowing center induced an inhibition of rhythmic swallowing (latency of <30 s) as shown by the reduced number and strength of electromyographic activities, which could last several minutes. The threshold of the leptin-induced inhibition was close to 0.1 pg. Interestingly, the inhibitory effect of leptin was not observed in leptin receptor-deficient Zucker rats. Here we show that, in Wistar rats, leptin already known to modulate the discharge of medullary solitary tract nucleus-sensitive neurons involved in satiety reflexes can also modify the activity of swallowing premotoneurons, thereby inhibiting an essential motor component of feeding behavior.

scholarly journals Cervical vagus nerve stimulation augments spontaneous discharge in second- and higher-order sensory neurons in the rat nucleus of the solitary tract

2017 ◽  
Vol 313 (2) ◽  
pp. H354-H367 ◽  
Author(s):  
Eric Beaumont ◽  
Regenia P. Campbell ◽  
Michael C. Andresen ◽  
Stephanie Scofield ◽  
Krishna Singh ◽  
...  
Keyword(s):  
Vagus Nerve ◽  
Nerve Stimulation ◽  
Vagus Nerve Stimulation ◽  
Higher Order ◽  
Second Order ◽  
Vagal Afferents ◽  
Visceral Afferents ◽  
Solitary Tract ◽  
C Fiber ◽  
Vagal Afferent

Vagus nerve stimulation (VNS) currently treats patients with drug-resistant epilepsy, depression, and heart failure. The mild intensities used in chronic VNS suggest that primary visceral afferents and central nervous system activation are involved. Here, we measured the activity of neurons in the nucleus of the solitary tract (NTS) in anesthetized rats using clinically styled VNS. Our chief findings indicate that VNS at threshold bradycardic intensity activated NTS neuron discharge in one-third of NTS neurons. This VNS directly activated only myelinated vagal afferents projecting to second-order NTS neurons. Most VNS-induced activity in NTS, however, was unsynchronized to vagal stimuli. Thus, VNS activated unsynchronized activity in NTS neurons that were second order to vagal afferent C-fibers as well as higher-order NTS neurons only polysynaptically activated by the vagus. Overall, cardiovascular-sensitive and -insensitive NTS neurons were similarly activated by VNS: 3/4 neurons with monosynaptic vagal A-fiber afferents, 6/42 neurons with monosynaptic vagal C-fiber afferents, and 16/21 polysynaptic NTS neurons. Provocatively, vagal A-fibers indirectly activated C-fiber neurons during VNS. Elevated spontaneous spiking was quantitatively much higher than synchronized activity and extended well into the periods of nonstimulation. Surprisingly, many polysynaptic NTS neurons responded to half the bradycardic intensity used in clinical studies, indicating that a subset of myelinated vagal afferents is sufficient to evoke VNS indirect activation. Our study uncovered a myelinated vagal afferent drive that indirectly activates NTS neurons and thus central pathways beyond NTS and support reconsideration of brain contributions of vagal afferents underpinning of therapeutic impacts. NEW & NOTEWORTHY Acute vagus nerve stimulation elevated activity in neurons located in the medial nucleus of the solitary tract. Such stimuli directly activated only myelinated vagal afferents but indirectly activated a subpopulation of second- and higher-order neurons, suggesting that afferent mechanisms and central neuron activation may be responsible for vagus nerve stimulation efficacy.

scholarly journals GABAergic pump cells of solitary tract nucleus innervate retrotrapezoid nucleus chemoreceptors

2008 ◽  
Vol 22 (S1) ◽  
Author(s):  
Ana C Takakura ◽  
Thiago S Moreira ◽  
Ruth L Stornetta ◽  
Patrice G Guyenet
Keyword(s):  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
Retrotrapezoid Nucleus

scholarly journals Hypoxia–sensitive glutamatergic neurons of solitary tract nucleus (NTS) innervate the retrotrapezoid nucleus (RTN) in rats

2006 ◽  
Vol 20 (4) ◽  
Author(s):  
Ana Carolina Thomaz Takakura ◽  
Thiago S Moreira ◽  
Gavin H West ◽  
Ruth L Stornetta ◽  
Patrice G Guyenet
Keyword(s):  
Solitary Tract Nucleus ◽  
Solitary Tract ◽  
Glutamatergic Neurons ◽  
Retrotrapezoid Nucleus
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