Sensory information from the upper airway: Role in the control of breathing

doi:10.1016/0034-5687(95)00048-I

Respiration Physiology

Volume 102, Issue 1, October 1995, Pages 1-16

Respiration Physiolo...

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Abstract

The functional integrity of extrathoracic airways critically depends on the proper orchestration of the activities of a set of patency-maintaining muscles. Recruitment and control of these muscles is regulated by laryngeal and trigeminal afferents that originate from pressure sensing endings. These sensors are particularly numerous among laryngeal receptors and, indeed, they constitute the main element in the respiration-modulated activity of the superior laryngeal nerve. Considering that the most compliant region of the upper airway, and thus more vulnerable to inspiratory collapse, lies cranially to the larynx, the laryngeal pressure-sensing endings seem to be ideally located for detecting collapsing forces and initiating reflex mechanisms for the preservation of patency. This process operates by activating upper airway dilating muscles and by decreasing inspiratory drive: both actions limit the effect of the collapsing forces. Cold reception is differently represented in various mammalian species within nasal and laryngeal segments. Cooling of the upper airway has an inhibitory influence on breathing, especially in newborns, and a depressive effect on upper airway dilating muscles. The latter response is presumably mediated through the inhibitory effect of cooling on laryngeal pressure endings. These responses could be harmful during occlusive episodes. Powerful defensive responses with distinct characteristics can be elicited through the stimulation of laryngeal and nasal irritant type receptors. Sneezing is elicited through the stimulation of trigeminal afferents, cough through the stimulation of laryngeal vagal endings. Changes in osmolality and ionic composition of the mucosal surface liquid can lead to conspicuous alterations in receptor activity and related reflexes.

References (59)

AndersonJ.W. et al.
Carbon dioxide-responsive laryngeal receptors in the dog
Respir. Physiol.
(1990)
BartlettD. et al.
Influence of laryngeal CO₂ on respiratory activities of motor nerves to accessory muscles
Respir. Physiol.
(1992)
JammesY. et al.
Afferent and efferents components of the bronchial vagal branches in cats
J. Auton. Nerv. Syst.
(1982)
JammesY. et al.
Respiratory effects of cold air breathing in anesthetized cats
Respir. Physiol.
(1983)
JammesY. et al.
Laryngeal afferents activated by phenyldiguanide and their response to cold air or helium-oxygen
Respir. Physiol.
(1987)
MacronJ.-M. et al.
Influence of vagal afferents in the sneeze reflex in cats
Neurosci. Lett.
(1994)
MortolaJ.P. et al.
Sulphur dioxide block of laryngeal receptors in rabbits
Respir. Physiol.
(1985)
Sant'AmbrogioF.B. et al.
Menthol in the upper airway depresses ventilation in newborn dogs
Respir. Physiol.
(1992)
Sant'AmbrogioG. et al.
Laryngeal receptors responding to transmural pressure, airflow and local muscle activity
Respir. Physiol.
(1983)
SekizawaS. et al.
The respiratory activity of the superior laryngeal nerve in the rat
Respir. Physiol.
(1991)

SekizawaS. et al.

Nasal receptors responding to noxious chemical irritants

Respir. Physiol.

(1994)

TsuboneH.

Nasal “flow” receptors of the rat

Respir. Physiol.

(1989)

TsuboneH. et al.

Respiratory activity in the superior laryngeal nerve of the rabbit

Respir. Physiol.

(1987)

TsuboneH. et al.

Laryngeal afferent activity and reflexes in the guinea pig

Respir. Physiol.

(1991)

UkabamC.U. et al.

Phrenic and hypoglossal neural responses to cold airflow in the upper airway

Respir. Physiol.

(1992)

WalloisF. et al.

Trigeminal nasal receptors related to respiration and to various stimuli in cats

Respir. Physiol.

(1991)

WalloisF. et al.

Influence of trigeminal nasal afferents on bulbar respiratory neuronal activity

Brain. Res.

(1992)

WalloisF. et al.

Postnatal development of the anterior ethmoidal nerve in cats: unmyelinated and myelinated nerve fiber analysis

Neurosci. Lett.

(1993)

AndersonJ.W. et al.

Water-responsive laryngeal receptors in the dog are not specialized endings

Respir. Physiol.

(1990)

AndersonJ.W. et al.

Stimulation of laryngeal afferents by I-menthol alters pattern of breathing in newborn dogs

Am. J. Respir. Crit. Care Med.

(1994)

BartlettD. et al.

Responses of laryngeal receptors to intralaryngeal CO₂ in the cat

J. Physiol. (London)

(1992)

BasnerR.C. et al.

Breathing route influences upper airway muscle activity in awake normal adults

J. Appl. Physiol.

(1989)

BasnerR.C. et al.

Effect of inspired air temperature on genioglossus activity during nose breathing in awake humans

J. Appl. Physiol.

(1990)

ChungK. et al.

The fiber composition of the superior laryngeal nerve

FASEB J.

(1993)

GhoshT.K. et al.

Influence of intralaryngeal CO₂ on the response of laryngeal afferents to upper airway negative pressure

J. Appl. Physiol.

(1994)

GlebovskyV.D. et al.

Stimulation of nasal cavity mucose trigeminal receptors with respiratory airflows

Sechenov. Physiol. J. USSR

(1984)

HigenbottamT. et al.

The cough response to ultrasonically nebulized distilled water in heart-lung transplantation patients

Am. Rev. Respir. Dis.

(1989)

HolzerP.

Capsaicin: cellular target, mechanisms of action, and selectivity for thin sensory neurons

Pharmacol. Rev.

(1991)

HornerR.L. et al.

Evidence for reflex upper airway dilator muscle activation by sudden negative airway pressure in man

J. Physiol. (London)

(1991)

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Citation Excerpt :
Sneezing results from stimulation of trigeminal afferents and cough through stimulation of laryngeal vagal endings. Changes in osmolality and ionic composition of mucosal surface liquid can stimulate various receptors and related reflexes (Widdicombe, 1986a; Sant'Ambrogio et al., 1995). With recent advances in molecular biology, different agonists and antagonists have become available.
This chapter broadly reviews cardiopulmonary sympathetic and vagal sensors and their reflex functions during physiologic and pathophysiologic processes. Mechanosensory operating mechanisms, including their central projections, are described under multiple sensor theory. In addition, ways to interpret evidence surrounding several controversial issues are provided, with detailed reasoning on how conclusions are derived. Cardiopulmonary sensory roles in breathing control and the development of symptoms and signs and pathophysiologic processes in cardiopulmonary diseases (such as cough and neuroimmune interaction) also are discussed.
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The depth, rate, and regularity of breathing change following transition from wakefulness to sleep. Interactions between sleep and breathing involve direct effects of the central mechanisms that generate sleep states exerted at multiple respiratory regulatory sites, such as the central respiratory pattern generator, respiratory premotor pathways, and motoneurons that innervate the respiratory pump and upper airway muscles, as well as effects secondary to sleep-related changes in metabolism. This chapter discusses respiratory effects of sleep as they occur under physiologic conditions. Breathing and central respiratory neuronal activities during nonrapid eye movement (NREM) sleep and REM sleep are characterized in relation to activity of central wake-active and sleep-active neurons. Consideration is given to the obstructive sleep apnea syndrome because in this common disorder, state-dependent control of upper airway patency by upper airway muscles attains high significance and recurrent arousals from sleep are triggered by hypercapnic and hypoxic episodes. Selected clinical trials are discussed in which pharmacological interventions targeted transmission in noradrenergic, serotonergic, cholinergic, and other state-dependent pathways identified as mediators of ventilatory changes during sleep. Central pathways for arousals elicited by chemical stimulation of breathing are given special attention for their important role in sleep loss and fragmentation in sleep-related respiratory disorders.
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Menthol-induced facilitation of cerebrocortical excitatory propagation induced by air puff stimulation of the nasal cavity in the rat: An optical imaging study
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Temperature plays a critical role in the sensation of airflow in the nasal mucosa. Neural activities of the ethmoidal nerve, a trigeminal afferent, responding to airflow are suppressed by warm airflow, whereas cold airflow enhances the ethmoidal nerve activities, which is mimicked by application of menthol, a cold-sensitive TRPM8 receptor agonist. However, it has been an open issue how menthol modulates the spatiotemporal profiles of neural activities of somatosensory cortical neurons. In this study, we assessed neural responses to an air puff stimulation (100 ms) to the nasal cavity in the absence or presence of l-menthol using an optical imaging technique with a voltage-sensitive dye in the primary cortex (S1) of urethane-anesthetized rats. A weak air puff application (15 psi) without l-menthol induced neural excitation in a part of the contralateral S1. The air puff stimulation with l-menthol significantly increased the optical signal intensity, expanded the activated area, and shortened the latency, compared to those in the absence of l-menthol. These results suggest that activation of cold-sensitive TRPM8 receptors sharpens airflow sensation in the nasal cavity and expands the receptive field, especially toward the pharynx, which may contribute to enhanced flavor perception.
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The peak amplitude in the initial and secondary responding regions increased in a stimulation intensity-dependent manner up to 20 psi (p < 0.01, ANOVA or ANOVA on ranks) and the area of the cortical response reached plateau at 20 psi. Most odorants induce simultaneous activation of the olfactory and trigeminal systems, and recent studies have reported an interaction between the two (Sant'Ambrogio et al., 1995; Brand, 2006; Croy et al., 2014). To examine the effect of odor on S1 excitation induced by the contralateral air puff application, we compared the peak amplitude of S1 excitation between the puff application of the deodorized air and amyl acetate (Fig. 4).
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Frontiers reviewSensory information from the upper airway: Role in the control of breathing

Abstract

Respir. Physiol.

Respir. Physiol.

J. Auton. Nerv. Syst.

Respir. Physiol.

Respir. Physiol.

Neurosci. Lett.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Brain. Res.

Neurosci. Lett.

Water-responsive laryngeal receptors in the dog are not specialized endings

Respir. Physiol.

Stimulation of laryngeal afferents by I-menthol alters pattern of breathing in newborn dogs

Am. J. Respir. Crit. Care Med.

Responses of laryngeal receptors to intralaryngeal CO2 in the cat

J. Physiol. (London)

Breathing route influences upper airway muscle activity in awake normal adults

J. Appl. Physiol.

Effect of inspired air temperature on genioglossus activity during nose breathing in awake humans

J. Appl. Physiol.

The fiber composition of the superior laryngeal nerve

FASEB J.

Influence of intralaryngeal CO2 on the response of laryngeal afferents to upper airway negative pressure

J. Appl. Physiol.

Stimulation of nasal cavity mucose trigeminal receptors with respiratory airflows

Sechenov. Physiol. J. USSR

The cough response to ultrasonically nebulized distilled water in heart-lung transplantation patients

Am. Rev. Respir. Dis.

Capsaicin: cellular target, mechanisms of action, and selectivity for thin sensory neurons

Pharmacol. Rev.

Evidence for reflex upper airway dilator muscle activation by sudden negative airway pressure in man

J. Physiol. (London)

Frontiers review
Sensory information from the upper airway: Role in the control of breathing

Responses of laryngeal receptors to intralaryngeal CO₂ in the cat

Influence of intralaryngeal CO₂ on the response of laryngeal afferents to upper airway negative pressure