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Reflexes from the Upper Respiratory Tract

John G. Widdicombe

10.1002/cphy.cp030211

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Reflexes from the Nose
1.1 Receptors and Afferent Nerves
1.2 Apnea and the Diving Response
1.3 The Sneeze
1.4 Sniffing
1.5 Other Reflexes From the Nose
2 Reflexes from the Pharynx
2.1 Aspiration Reflex
2.2 Swallowing
2.3 Other Pharyngeal Reflexes
3 Reflexes from the Larynx
3.1 Nervous End Organs in the Larynx
3.2 Recordings From Afferent Fibers
3.3 Respiratory Reflexes
3.4 Cardiovascular Reflexes
3.5 Other Laryngeal Reflexes
4 General Upper Airway Reflex Responses
4.1 Responses to Pressure
4.2 Responses to Flow
4.3 Responses to Temperature Changes
4.4 Sensation
Figure 1. Figure 1.

Two intraepithelial nerve endings (arrows) from respiratory mucosa of nasal septum. Axon terminals are enwrapped by cell membranes of epithelial cells. Axoplasm of endings contains accumulations of typical small mitochondria and some microvesicles. Int, intercellular space; BL, epithelial basal lamina; M, part of basal or Bowman's membrane. Male, 11 yr old; × ∼16,700.

From Cauna 53
Figure 2. Figure 2.

Diagram of innervation of human nose. N, nerve; GG, geniculate ganglion; SG, sphenopalatine ganglion; SCG, superior cervical ganglion; MN, maxillary nerve; GSPN, greater superficial petrosal nerve.

From Eccles 80
Figure 3. Figure 3.

Development of bradycardia in response to forcible submersion of head of domestic duck Anas platyrhynchos (A) and muskrat Ondatra zibethica (B). Downward deflection of event marker indicates point of submersion in each case; ecg, electrocardiogram.

From Bamford and Jones 17
Figure 4. Figure 4.

Effect of nasal stimulation in 19‐day‐old rabbit. Nasal balloon inflated at marker by top trace and deflated 10 s later. Note prolonged apnea and bradycardia. and , partial pressures of O2 and CO2, respectively.

From Wealthall 289
Figure 5. Figure 5.

Effect of insufflation of ammonia vapor into nose. Each trace shows from top to bottom: signal, blood pressure (BP), transpulmonary pressure (Ptp), lower tracheal flow (), and tracheal pressure (translaryngeal pressure) (Ptr), with saturation of pressure recorder. A: insufflation of 3 ml of 1:100 ammonia vapor into nose, with superior laryngeal nerves intact. Note sneezing, positive deflections of Ptp, and increase in laryngeal resistance in expiratory phase. B: insufflation of 3 ml of 1:1,000 ammonia vapor into nose, with superior laryngeal nerves intact. Note no sneezing and increase in breathing frequency and laryngeal resistance. C: insufflation of 3 ml 1:1,000 ammonia vapor into nose, with superior laryngeal nerves cut. Note slowing of breathing and increase in laryngeal resistance.

From Szereda‐Przestaszewska and Widdicombe 265
Figure 6. Figure 6.

Schematic illustration of nasal autonomic innervation. Preganglionic sympathetic (S) neurons contain acetylcholine (ACh) and originate from thoracic region of spinal cord. These neurons relay in superior cervical ganglion (SCG). Most postganglionic noradrenergic (NA) fibers run together (not shown) with preganglionic parasympathetic (PS) nerve to form so‐called vidian nerve (*), which enters sphenopalatine ganglion (SPG). Sympathetic nerves predominantly innervate blood vessels (A, arterioles; V, venous sinusoids and venules), whereas adrenergic innervation of glands is sparse. Neuropeptide Y (NPY) occurs in noradrenergic periarterial nerves. Postganglionic cholinergic fibers innervate both blood vessels and exocrine glands. Vasoactive intestinal peptide (VIP) and peptide histidine isoleucine (PHI) are present in sphenopalatine ganglion cells, presumably together with ACh. Sensory supply from trigeminal ganglion (TG) travels in maxillary portion (**) and joins posterior nasal nerves. Substance P (SP) neurons constitute population of trigeminal efferents with peripheral branches within respiratory epithelium as well as around arterioles, venules, and sphenopalatine ganglion cells.

From Lundblad 161
Figure 7. Figure 7.

Frozen section, with Schofield's silver stain, of cat epipharyngeal region showing nerve fibers ramifying among epithelial cells. Photograph by A. M. S. White.

From Fillenz and Widdicombe 85
Figure 8. Figure 8.

Blood pressure (BP) and action potentials in strand of pharyngeal branch of glossopharyngeal nerve during stimulation of epipharynx. A: 3 ml of ammonia vapor at signal; no response. B: mechanical stimulation with nylon fiber during signal; transient discharges with each movement of thread. C and D: airflow at 6 liters/min through catheter in left nostril; rapidly adapting discharges at start of airflow only. Long horizontal bars mark duration of each stimulus.

From Nail et al. 192
Figure 9. Figure 9.

Illustration of innervation of upper airway mucous membrane. Note that lower laryngopharyngeal compartment formed by pharyngeal airway closure is supplied primarily by superior laryngeal branch of vagus nerve.

From Mathew et al. 169
Figure 10. Figure 10.

Response of phrenic motoneuron discharge to epipharyngeal stimulation. A: control ventilation. B: mechanical stimulation of epipharyngeal mucosa. C: electrical stimulation of glossopharyngeal nerve at 20 shocks/s. Each trace shows from top to bottom: systemic arterial blood pressure (BP), multifiber discharge, and single‐motoneuron discharge. Horizontal bars below B and C represent duration of stimulus. Note repeated brief inspiratory efforts in B and C and entrainment in C.

From Nail et al. 193
Figure 11. Figure 11.

Laryngeal mechanoreceptor responding to negative transmural pressure. Recording from left superior laryngeal nerve. A: upper airway breathing changed to tracheostomy breathing at arrow. B: upper airway breathing and upper airway occlusion. C: tracheostomy breathing and tracheal occlusion. Note that maximal activity is seen during upper airway occlusion, in which larynx is subjected to increased negative pressure. AP, action potentials; Pes, esophageal pressure.

From Sant'Ambrogio et al. 221
Figure 12. Figure 12.

Laryngeal mechanoreceptor responding to distortion caused by action of upper airway muscles (drive). Recordings are from left superior laryngeal nerve. A and D: upper airway breathing changed to tracheostomy breathing (arrow). B and E: upper airway breathing and upper airway occlusion. C and F: tracheostomy breathing and tracheal occlusion. Comparison of receptor discharge during efforts in B and C indicates inhibitory influence of negative pressure. Note in A‐C that inspiratory activity is present and is not influenced by flow. Inspiratory activity increases when inspiratory drive increases (occluded efforts). D‐F represent same receptor after cold block of recurrent laryngeal nerves. Note that in D‐F activity is substantially reduced. AP, action potentials; Ptr, pressure in tracheal lumen.

From Sant'Ambrogio et al. 221
Figure 13. Figure 13.

Behavior of laryngeal flow (cold) receptor during inhalation of warm air. Dog is spontaneously breathing through upper airway. Note that inspiratory modulation of receptor disappears when laryngeal temperature during inspiration is raised to expiratory level by inhalation of warm air (between arrows). AP, action potentials; Pes, esophageal pressure; , airflow; Lar. Temp, laryngeal temperature.

From Sant'Ambrogio et al. 224
Figure 14. Figure 14.

Recordings from single water‐sensitive fiber in superior laryngeal nerve of adult dog. Onset of discharge coincided with arrival of fluids in larynx with negligible latency. Time marks denote 1‐s intervals. Four solutions applied in lower traces were isotonic (300 mM). Only saline did not stimulate receptor.

From Boggs and Bartlett 27
Figure 15. Figure 15.

Coughing caused by insufflation of 20 ml of 1:200 ammonia vapor in air into larynx of cat. Note positive deflection of transpulmonary pressure (TPP) coinciding with activity in abdominal electromyogram. Each trace shows from top to bottom: blood pressure (BP), TPP, tidal volume, phrenic integral, phrenic activity, abdominal electromyogram, and signal; recording is continuous.

From Boushey et al. 32
Figure 16. Figure 16.

Simultaneous recording of afferent, efferent, and effector (ventilatory) component of expiration reflex in anesthetized cat. Note firing of afferent action potentials and expiratory effort. Each trace shows from top to bottom: pleural pressure (Ppl), tracheal airflow (), tidal volume (Vt), lumbar nerve electroneurogram (n. lumb.), action potentials from receptors recorded in superior laryngeal nerve (N. laryng. cran.), and brief contact of cotton wool pledget with dorsal part of both vocal folds (Stim). Time marker, 1 s.

From Tomori and Stransky 271
Figure 17. Figure 17.

Effect of insufflation of 1:105 ammonia vapor into larynx of cat before (top) and after (bottom) cutting superior laryngeal nerves. Note slight slowing of breathing, absence of expiratory efforts, and increase in laryngeal resistance before denervation. Each trace shows from top to bottom: signal, blood pressure (BP), transpulmonary pressure (Ptp), lower tracheal flow (), and translaryngeal pressure (Ptr), with saturation of pressure recorder.

From Szereda‐Przestaszewska and Widdicombe 265
Figure 18. Figure 18.

Airflow resistance of upper (•) and lower (▴) zones during sleep in normal humans. Resistance of larynx and lungs (▴) does not change, whereas resistance above retroepiglottic space increases during sleep. REM, rapid‐eye‐movement sleep. n = 5.

From Hudgel et al. 112
Figure 19. Figure 19.

Changes in respiratory frequency associated with changes in transmural airway pressure in rabbit isolated upper airway. Data from 1 animal. Frequency change was determined from first 3 breaths after change in pressure compared with last 3 breaths prior to change.

From Mathew et al. 167
Figure 20. Figure 20.

Responses of moving averages of diaphragm (Dia) and upper airway muscles to upper airway negative pressure. A: electromyogram before and for first 3 breaths during application of −5 cmH2O to larynx in representative animal. All upper airway muscles show increases in phasic activity; inspiratory time is minimally increased. B: −10 cmH2O applied to nasopharynx of same animal produced greater effects on inspiratory time and peak amplitude of upper airway muscles. GG, genioglossus; PCA, posterior cricoarytenoid; AN, alae nasi.

From van Lunteren et al. 283
Figure 21. Figure 21.

Effect of negative upper airway pressure (UA press) on nasal electromyogram (EMG). UA pressure changes (top trace), direct nasal EMG (middle trace), and integrated nasal EMG (bottom trace) are shown. Phasic inspiratory activity present during control period increases markedly during negative pressure application, with increase in inspiratory and expiratory times.

From Mathew 166


Figure 1.

Two intraepithelial nerve endings (arrows) from respiratory mucosa of nasal septum. Axon terminals are enwrapped by cell membranes of epithelial cells. Axoplasm of endings contains accumulations of typical small mitochondria and some microvesicles. Int, intercellular space; BL, epithelial basal lamina; M, part of basal or Bowman's membrane. Male, 11 yr old; × ∼16,700.

From Cauna 53


Figure 2.

Diagram of innervation of human nose. N, nerve; GG, geniculate ganglion; SG, sphenopalatine ganglion; SCG, superior cervical ganglion; MN, maxillary nerve; GSPN, greater superficial petrosal nerve.

From Eccles 80


Figure 3.

Development of bradycardia in response to forcible submersion of head of domestic duck Anas platyrhynchos (A) and muskrat Ondatra zibethica (B). Downward deflection of event marker indicates point of submersion in each case; ecg, electrocardiogram.

From Bamford and Jones 17


Figure 4.

Effect of nasal stimulation in 19‐day‐old rabbit. Nasal balloon inflated at marker by top trace and deflated 10 s later. Note prolonged apnea and bradycardia. and , partial pressures of O2 and CO2, respectively.

From Wealthall 289


Figure 5.

Effect of insufflation of ammonia vapor into nose. Each trace shows from top to bottom: signal, blood pressure (BP), transpulmonary pressure (Ptp), lower tracheal flow (), and tracheal pressure (translaryngeal pressure) (Ptr), with saturation of pressure recorder. A: insufflation of 3 ml of 1:100 ammonia vapor into nose, with superior laryngeal nerves intact. Note sneezing, positive deflections of Ptp, and increase in laryngeal resistance in expiratory phase. B: insufflation of 3 ml of 1:1,000 ammonia vapor into nose, with superior laryngeal nerves intact. Note no sneezing and increase in breathing frequency and laryngeal resistance. C: insufflation of 3 ml 1:1,000 ammonia vapor into nose, with superior laryngeal nerves cut. Note slowing of breathing and increase in laryngeal resistance.

From Szereda‐Przestaszewska and Widdicombe 265


Figure 6.

Schematic illustration of nasal autonomic innervation. Preganglionic sympathetic (S) neurons contain acetylcholine (ACh) and originate from thoracic region of spinal cord. These neurons relay in superior cervical ganglion (SCG). Most postganglionic noradrenergic (NA) fibers run together (not shown) with preganglionic parasympathetic (PS) nerve to form so‐called vidian nerve (*), which enters sphenopalatine ganglion (SPG). Sympathetic nerves predominantly innervate blood vessels (A, arterioles; V, venous sinusoids and venules), whereas adrenergic innervation of glands is sparse. Neuropeptide Y (NPY) occurs in noradrenergic periarterial nerves. Postganglionic cholinergic fibers innervate both blood vessels and exocrine glands. Vasoactive intestinal peptide (VIP) and peptide histidine isoleucine (PHI) are present in sphenopalatine ganglion cells, presumably together with ACh. Sensory supply from trigeminal ganglion (TG) travels in maxillary portion (**) and joins posterior nasal nerves. Substance P (SP) neurons constitute population of trigeminal efferents with peripheral branches within respiratory epithelium as well as around arterioles, venules, and sphenopalatine ganglion cells.

From Lundblad 161


Figure 7.

Frozen section, with Schofield's silver stain, of cat epipharyngeal region showing nerve fibers ramifying among epithelial cells. Photograph by A. M. S. White.

From Fillenz and Widdicombe 85


Figure 8.

Blood pressure (BP) and action potentials in strand of pharyngeal branch of glossopharyngeal nerve during stimulation of epipharynx. A: 3 ml of ammonia vapor at signal; no response. B: mechanical stimulation with nylon fiber during signal; transient discharges with each movement of thread. C and D: airflow at 6 liters/min through catheter in left nostril; rapidly adapting discharges at start of airflow only. Long horizontal bars mark duration of each stimulus.

From Nail et al. 192


Figure 9.

Illustration of innervation of upper airway mucous membrane. Note that lower laryngopharyngeal compartment formed by pharyngeal airway closure is supplied primarily by superior laryngeal branch of vagus nerve.

From Mathew et al. 169


Figure 10.

Response of phrenic motoneuron discharge to epipharyngeal stimulation. A: control ventilation. B: mechanical stimulation of epipharyngeal mucosa. C: electrical stimulation of glossopharyngeal nerve at 20 shocks/s. Each trace shows from top to bottom: systemic arterial blood pressure (BP), multifiber discharge, and single‐motoneuron discharge. Horizontal bars below B and C represent duration of stimulus. Note repeated brief inspiratory efforts in B and C and entrainment in C.

From Nail et al. 193


Figure 11.

Laryngeal mechanoreceptor responding to negative transmural pressure. Recording from left superior laryngeal nerve. A: upper airway breathing changed to tracheostomy breathing at arrow. B: upper airway breathing and upper airway occlusion. C: tracheostomy breathing and tracheal occlusion. Note that maximal activity is seen during upper airway occlusion, in which larynx is subjected to increased negative pressure. AP, action potentials; Pes, esophageal pressure.

From Sant'Ambrogio et al. 221


Figure 12.

Laryngeal mechanoreceptor responding to distortion caused by action of upper airway muscles (drive). Recordings are from left superior laryngeal nerve. A and D: upper airway breathing changed to tracheostomy breathing (arrow). B and E: upper airway breathing and upper airway occlusion. C and F: tracheostomy breathing and tracheal occlusion. Comparison of receptor discharge during efforts in B and C indicates inhibitory influence of negative pressure. Note in A‐C that inspiratory activity is present and is not influenced by flow. Inspiratory activity increases when inspiratory drive increases (occluded efforts). D‐F represent same receptor after cold block of recurrent laryngeal nerves. Note that in D‐F activity is substantially reduced. AP, action potentials; Ptr, pressure in tracheal lumen.

From Sant'Ambrogio et al. 221


Figure 13.

Behavior of laryngeal flow (cold) receptor during inhalation of warm air. Dog is spontaneously breathing through upper airway. Note that inspiratory modulation of receptor disappears when laryngeal temperature during inspiration is raised to expiratory level by inhalation of warm air (between arrows). AP, action potentials; Pes, esophageal pressure; , airflow; Lar. Temp, laryngeal temperature.

From Sant'Ambrogio et al. 224


Figure 14.

Recordings from single water‐sensitive fiber in superior laryngeal nerve of adult dog. Onset of discharge coincided with arrival of fluids in larynx with negligible latency. Time marks denote 1‐s intervals. Four solutions applied in lower traces were isotonic (300 mM). Only saline did not stimulate receptor.

From Boggs and Bartlett 27


Figure 15.

Coughing caused by insufflation of 20 ml of 1:200 ammonia vapor in air into larynx of cat. Note positive deflection of transpulmonary pressure (TPP) coinciding with activity in abdominal electromyogram. Each trace shows from top to bottom: blood pressure (BP), TPP, tidal volume, phrenic integral, phrenic activity, abdominal electromyogram, and signal; recording is continuous.

From Boushey et al. 32


Figure 16.

Simultaneous recording of afferent, efferent, and effector (ventilatory) component of expiration reflex in anesthetized cat. Note firing of afferent action potentials and expiratory effort. Each trace shows from top to bottom: pleural pressure (Ppl), tracheal airflow (), tidal volume (Vt), lumbar nerve electroneurogram (n. lumb.), action potentials from receptors recorded in superior laryngeal nerve (N. laryng. cran.), and brief contact of cotton wool pledget with dorsal part of both vocal folds (Stim). Time marker, 1 s.

From Tomori and Stransky 271


Figure 17.

Effect of insufflation of 1:105 ammonia vapor into larynx of cat before (top) and after (bottom) cutting superior laryngeal nerves. Note slight slowing of breathing, absence of expiratory efforts, and increase in laryngeal resistance before denervation. Each trace shows from top to bottom: signal, blood pressure (BP), transpulmonary pressure (Ptp), lower tracheal flow (), and translaryngeal pressure (Ptr), with saturation of pressure recorder.

From Szereda‐Przestaszewska and Widdicombe 265


Figure 18.

Airflow resistance of upper (•) and lower (▴) zones during sleep in normal humans. Resistance of larynx and lungs (▴) does not change, whereas resistance above retroepiglottic space increases during sleep. REM, rapid‐eye‐movement sleep. n = 5.

From Hudgel et al. 112


Figure 19.

Changes in respiratory frequency associated with changes in transmural airway pressure in rabbit isolated upper airway. Data from 1 animal. Frequency change was determined from first 3 breaths after change in pressure compared with last 3 breaths prior to change.

From Mathew et al. 167


Figure 20.

Responses of moving averages of diaphragm (Dia) and upper airway muscles to upper airway negative pressure. A: electromyogram before and for first 3 breaths during application of −5 cmH2O to larynx in representative animal. All upper airway muscles show increases in phasic activity; inspiratory time is minimally increased. B: −10 cmH2O applied to nasopharynx of same animal produced greater effects on inspiratory time and peak amplitude of upper airway muscles. GG, genioglossus; PCA, posterior cricoarytenoid; AN, alae nasi.

From van Lunteren et al. 283


Figure 21.

Effect of negative upper airway pressure (UA press) on nasal electromyogram (EMG). UA pressure changes (top trace), direct nasal EMG (middle trace), and integrated nasal EMG (bottom trace) are shown. Phasic inspiratory activity present during control period increases markedly during negative pressure application, with increase in inspiratory and expiratory times.

From Mathew 166
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Article Title: Reflexes from the Upper Respiratory Tract
 

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John G. Widdicombe. Reflexes from the Upper Respiratory Tract. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 363-394. First published in print 1986. doi: 10.1002/cphy.cp030211