Mechanoreceptor modulation of endogenous respiratory rhythms in vertebrates

While pulmonary mechanoreceptors appear to play little or no role in determining the eupneic breathing pattern in some species of vertebrates, they do in others as well as in all species under conditions of elevated respiratory drive. Tonic and phasic inputs from this receptor group have independent roles in determining breathing pattern. Thus withholding lung inflation produces very different results from receptor denervation. There are at least five phases to the respiratory cycle that appear to be under separate control. Tonic receptor input is involved primarily in regulating the length of the respiratory pause, which can occur at the end of inspiration or expiration, depending on the species. Phasic receptor input has different effects during different phases of the cycle as well as different effects at different times during a single phase. This activity contributes to phase switching during the ventilation cycle and thus to the regulation of breathing frequency and tidal volume. The significance of the modulatory effects of phasic input on the duration of different phases of the ventilation cycle is not totally clear, but the evidence suggests that phasic input acts to stabilize the respiratory pattern and may be instrumental in optimizing the breathing pattern in terms of ergometric costs. This appears to be the case in all vertebrate classes, despite dramatic differences in the mechanical events associated with ventilation arising from different respiratory pumps. These receptors also appear to have significant roles other than those associated with modulation of respiratory rhythm, particularly in lower vertebrates. Many of these roles, such as maintaining the integrity of the gill curtain in fish or buoyancy control and regulation of blood flow distribution in reptiles, may be as important as their role in modulating the endogenous rhythm.

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Recovery of breathing pattern after 15 min of cerebral ischemia in rabbits

Journal of Applied Physiology ◽

10.1152/jappl.1990.69.5.1676 ◽

1990 ◽

Vol 69 (5) ◽

pp. 1676-1681 ◽

Cited By ~ 6

Author(s):

R. Pluta ◽

J. R. Romaniuk

Keyword(s):

Cerebral Ischemia ◽

Neural Control ◽

Breathing Pattern ◽

Respiratory Pattern ◽

Lung Inflation ◽

Brachiocephalic Trunk ◽

Precise Analysis ◽

Neural Control Of Breathing ◽

Recurrent Laryngeal Nerves ◽

The Brain

The study was undertaken to ascertain the neural control of breathing and vagal reflexes during and after cerebral ischemia. The experiments were performed on anesthetized, paralyzed, and artificially ventilated rabbits. Cerebral ischemia was induced by reversible intrathoracic occlusion of the brachiocephalic trunk and the left subclavian and both internal thoracic arteries for 15 min. The effect of cerebral ischemia on breathing pattern was assessed by monitoring the integrated activities of phrenic and recurrent laryngeal nerves. Ischemia produced enhancement of breathing followed by apnea and gasping. During enhanced breathing as well as during gasping, the inspiratory-inhibiting effect of lung inflation (Breuer-Hering reflex) was abolished. When brain circulation was restored, respiratory activity started with gasps, which later were intermingled with eupneic type of inspirations. During the onset of a eupneic breath, lung inflation produced inspiratory facilitation but never an inhibition. However, after 30 min of recovery from cerebral ischemia, the Breuer-Hering reflex was restored. Results show that precise analysis of vagal reflexes and respiratory pattern during ischemia and resuscitation may be used as an indicator of resumption of autonomic activity in the brain stem.

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Effects on respiratory pattern of focal cooling in the medulla of the dog

Journal of Applied Physiology ◽

10.1152/jappl.1988.65.5.2004 ◽

1988 ◽

Vol 65 (5) ◽

pp. 2004-2010 ◽

Cited By ~ 4

Author(s):

M. Adams ◽

T. Chonan ◽

N. S. Cherniack ◽

C. von Euler

Keyword(s):

Respiratory Rhythm ◽

Nucleus Ambiguus ◽

Respiratory Pattern ◽

Respiratory Drive ◽

Timing Effect ◽

Diaphragm Electrical Activity ◽

Inspiratory Activity ◽

Ventral Medullary Surface ◽

Focal Cooling

Studies in cats have shown that, in addition to respiratory neuron groups in the dorsomedial (DRG) and ventrolateral (VRG) medulla, neural structures in the most ventral medullary regions are important for the maintenance of respiratory rhythm. The purpose of this study was to determine whether a similar superficially located ventral region was present in the dog and to assess the role of each of the other regions in the canine medulla important in the control of breathing, in 20 anesthetized, vagotomized, and artificially ventilated dogs, a cryoprobe was used to cool selected regions of the medulla to 15-20 degrees C. Respiratory output was determined from phrenic nerve or diaphragm electrical activity. Cooling in or near the nucleus of the solitary tract altered timing and produced little change in the amplitude or rate of rise of inspiratory activity; lengthening of inspiratory time was the most common timing effect observed. Cooling in ventrolateral regions affected the amplitude and rate of rise of respiratory activity. Depression of neural tidal volume and apnea could be produced by unilateral cooling in two ventrolateral regions: 1) near the nucleus ambiguus and nucleus para-ambiguus and 2) just beneath the ventral medullary surface. These findings indicate that in the dog dorsomedial neural structures influence respiratory timing, whereas more ventral structures are important to respiratory drive.

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The Relationship between Lung Volume, Respiratory Drive and Breathing Pattern in the Turtle, Chrysemys Picta

Journal of Experimental Biology ◽

10.1242/jeb.120.1.233 ◽

1986 ◽

Vol 120 (1) ◽

pp. 233-247 ◽

Cited By ~ 3

Author(s):

W.K. MILSOM ◽

P. CHAN

Keyword(s):

Lung Volume ◽

Breathing Pattern ◽

Minute Ventilation ◽

Gas Mixtures ◽

Chrysemys Picta ◽

Breath Holding ◽

Respiratory Drive ◽

Separate Control ◽

Induced Changes ◽

Breathing Room

Induced changes in resting lung volume (VLR) in the turtle Chrysemys picta (Schneider) had no effect on resting levels of minute ventilation in animals breathing room air but did change their breathing pattern. Increasing VLR caused an increase in the number of breaths in each episode (burst) of breathing but a reduction in the incidence of such breathing bursts and thus an increase in the length of periods of breath-holding. The data indicate that these effects were largely the consequence of changes in lung volume per se rather than changes in lung gas stores. Although both hypoxia and hypercapnia stimulated ventilation via increases in tidal volume and breathing frequency, they produced distinct changes in breathing pattern. While hypoxia (3% O2) caused an increase in the number of bursts of breathing (B/min) and reduced the number of breaths (b) in each burst (b/B), hypercapnia (5% CO2) increased both B/min and b/B. These data suggest that the size and incidence of bursts of breathing must be under separate control. One consequence of the different effects of hypoxia and hypercapnia on breaths per burst (b/B) was that hypoxic-hypercapnic gas mixtures (3% O2+5% CO2) failed to stimulate ventilation as much as hypercapnia alone. Administration of hypoxic, hypercapnic and hypoxic-hypercapnic gas mixtures to elevate respiratory drive eliminated the effects of changes in VLR on breathing pattern. Thus, although changes in VLR are important in the control of breathholding in animals breathing air, their effect decreases as respiratory drive increases.

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Respiratory and Mayer wave-related discharge patterns of raphé and pontine neurons change with vagotomy

Journal of Applied Physiology ◽

10.1152/japplphysiol.01324.2009 ◽

2010 ◽

Vol 109 (1) ◽

pp. 189-202 ◽

Cited By ~ 33

Author(s):

K. F. Morris ◽

S. C. Nuding ◽

L. S. Segers ◽

D. M. Baekey ◽

R. Shannon ◽

...

Keyword(s):

Respiratory Rhythm ◽

Respiratory Drive ◽

Lung Inflation ◽

Firing Patterns ◽

Cross Correlation Analysis ◽

Before And After ◽

Respiratory Modulation ◽

Discharge Patterns ◽

Mayer Wave ◽

Raphe Neurons

Previous models have attributed changes in respiratory modulation of pontine neurons after vagotomy to a loss of pulmonary stretch receptor “gating” of an efference copy of inspiratory drive. Recently, our group confirmed that pontine neurons change firing patterns and become more respiratory modulated after vagotomy, although average peak and mean firing rates of the sample did not increase (Dick et al., J Physiol 586: 4265–4282, 2008). Because raphé neurons are also elements of the brain stem respiratory network, we tested the hypotheses that after vagotomy raphé neurons have increased respiratory modulation and that alterations in their firing patterns are similar to those seen for pontine neurons during withheld lung inflation. Raphé and pontine neurons were recorded simultaneously before and after vagotomy in decerebrated cats. Before vagotomy, 14% of 95 raphé neurons had increased activity during single respiratory cycles prolonged by withholding lung inflation; 13% exhibited decreased activity. After vagotomy, the average index of respiratory modulation (η2) increased (0.05 ± 0.10 to 0.12 ± 0.18 SD; Student's paired t-test, P < 0.01). Time series and frequency domain analyses identified pontine and raphé neuron firing rate modulations with a 0.1-Hz rhythm coherent with blood pressure Mayer waves. These “Mayer wave-related oscillations” (MWROs) were coupled with central respiratory drive and became synchronized with the central respiratory rhythm after vagotomy (7 of 10 animals). Cross-correlation analysis identified functional connectivity in 52 of 360 pairs of neurons with MWROs. Collectively, the results suggest that a distributed network participates in the generation of MWROs and in the coordination of respiratory and vasomotor rhythms.

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Analysis of a periodic breathing pattern associated with Mayer waves

American Journal of Physiology-Legacy Content ◽

10.1152/ajplegacy.1975.228.3.768 ◽

1975 ◽

Vol 228 (3) ◽

pp. 768-774 ◽

Cited By ~ 33

Author(s):

G Preiss ◽

S Iscoe ◽

C Polosa

Keyword(s):

Arterial Pressure ◽

Breathing Pattern ◽

Neuromuscular Block ◽

Sensory Information ◽

Pressure Oscillation ◽

Periodic Breathing ◽

Systemic Arterial Pressure ◽

Artery Occlusion ◽

Respiratory Pattern ◽

Respiratory Drive

Cats subjected to common carotid artery occlusion and hemorrhage developed a waxing and waning of respiratory amplitude recurring with a period of 24 s (range 10-60). Occasionally the waning phase terminated with apnea. This respiratory pattern, reminiscent of "periodic" breathing, was usually associated with an oscillation of sympathetic neural activity, and of systemic arterial pressure, of the same period. A similar pattern of modulation of phrenic nerve activity was observed during neuromuscular block and artificial ventilation and when, at the same time, the associated systemic arterial pressure oscillation was eliminated. These findings suggest that this breathing pattern is not the result of an analogous pattern in the discharge of gas tension-sensitive and/or blood flow- and pressure-sensitive receptors that is fed back to the central nervous system (CNS). Hence the pattern must be generated within the CNS with no need of rhythmic sensory information. The pattern can be accounted for by the assumption that the central respiratory drive potentials are riding on top of a slow oscillation of phrenic motoneuron membrane potential with a 24-s period.

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Pulmonary afferent and central influences on respiratory phase-switching in the cat

Canadian Journal of Physiology and Pharmacology ◽

10.1139/y81-103 ◽

1981 ◽

Vol 59 (7) ◽

pp. 675-682 ◽

Cited By ~ 4

Author(s):

Morton I. Cohen

Keyword(s):

Respiratory Rhythm ◽

Respiratory Neuron ◽

Lung Inflation ◽

Phase Switching ◽

Neuron Populations ◽

Stretch Receptors ◽

Pulmonary Stretch Receptors ◽

Pneumotaxic Center ◽

Respiratory Phases ◽

Medullary Respiratory Neuron

A striking feature of the mammalian respiratory rhythm generator is the abruptness of the transitions between the inspiratory (I) and expiratory (E) phases ("phase-switching"). Although reciprocal inhibitory actions between I and E neurons are important for maintaining the alternation of respiratory phases, phase-switching actions are probably produced by recurrent inhibitory neuronal loops acting within each phase. The operation of such negative feedback circuits has been studied using two types of experimental input: (a) activation of pulmonary stretch receptors by lung inflation, which shortens the I phase and prolongs the E phase, and (b) electrical stimulation in the rostral pontine "pneumotaxic center" region, which can produce premature I → E or E → I switching, depending on stimulation site. These inputs produce diverse effects on discharges of various types of medullary respiratory neuron; analysis of such observations has led to hypotheses about the possible roles of different neuron populations in phase-switching.

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Temporal variations in the pattern of breathing

Journal of Applied Physiology ◽

10.1152/jappl.1996.80.4.1079 ◽

1996 ◽

Vol 80 (4) ◽

pp. 1079-1087 ◽

Cited By ~ 78

Author(s):

E. N. Bruce

Keyword(s):

White Noise ◽

Breathing Pattern ◽

Respiratory Rhythm ◽

Temporal Variations ◽

Feedback Loops ◽

Respiratory Pattern ◽

Nonlinear Interactions ◽

Time Varying ◽

Rhythm Generation ◽

Physiological Processes

Breath-to-breath variations in the pattern of breathing can occur as uncorrelated random variations (“white noise”), correlated random changes, or as one of two types of nonrandom variations: periodic oscillations or nonrandom nonperiodic fluctuations. White noise is probably present in all physiological processes. In many cases, periodic variations are due to oscillations originating in chemoreflex feedback loops. It has long been hypothesized that correlated random variations in breathing pattern are due to central neutral “memory mechanisms, but part of this behavior might be due to chemoreflex mechanisms. Recently it has been concluded that nonlinear interactions between pulmonary and airway afferent activities and integrative central respiratory mechanisms can produce nonrandom nonperiodic (and also periodic) variability of the respiratory pattern. These latter studies have provided new insights about the behavioral relevance of the integrative character of central respiratory mechanisms and the time-varying nature of pulmonary afferent activities and have emphasized the importance of identifying the physiological bases for these phenomena. These and other findings are interpreted assuming that respiratory rhythm generation/pattern formation occurs via a nonlinear oscillator, and novel inferences concerning temporal variations of the breathing pattern are proposed.

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Responses of respiratory drive and breathing pattern to inspiratory loading during nitrous oxide and isoflurane sedation

Acta Anaesthesiologica Scandinavica ◽

10.1111/j.1399-6576.1998.tb05374.x ◽

1998 ◽

Vol 42 (9) ◽

pp. 1043-1049 ◽

Cited By ~ 2

Author(s):

A. ÖStlund ◽

D. Linnarsson

Keyword(s):

Nitrous Oxide ◽

Breathing Pattern ◽

Respiratory Drive

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Tracheal occlusion-evoked respiratory load compensation and inhibitory neurotransmitter expression in rats

Journal of Applied Physiology ◽

10.1152/japplphysiol.01256.2013 ◽

2014 ◽

Vol 116 (8) ◽

pp. 1006-1016 ◽

Cited By ~ 2

Author(s):

Hsiu-Wen Tsai ◽

Paul W. Davenport

Keyword(s):

Neural Network ◽

Brain Stem ◽

Breathing Pattern ◽

Respiratory Rhythm ◽

Inhibitory Neurotransmitter ◽

Load Compensation ◽

Efferent Projections ◽

Motor Reflex ◽

Sensory Pathway ◽

The Brain

Respiratory load compensation is a sensory-motor reflex generated in the brain stem respiratory neural network. The nucleus of the solitary tract (NTS) is thought to be the primary structure to process the respiratory load-related afferent activity and contribute to the modification of the breathing pattern by sending efferent projections to other structures in the brain stem respiratory neural network. The sensory pathway and motor responses of respiratory load compensation have been studied extensively; however, the mechanism of neurogenesis of load compensation is still unknown. A variety of studies has shown that inhibitory interconnections among the brain stem respiratory groups play critical roles for the genesis of respiratory rhythm and pattern. The purpose of this study was to examine whether inhibitory glycinergic neurons in the NTS were activated by external and transient tracheal occlusions (ETTO) in anesthetized animals. The results showed that ETTO produced load compensation responses with increased inspiratory, expiratory, and total breath time, as well as elevated activation of inhibitory glycinergic neurons in the caudal NTS (cNTS) and intermediate NTS (iNTS). Vagotomized animals receiving transient respiratory loads did not exhibit these load compensation responses. In addition, vagotomy significantly reduced the activation of inhibitory glycinergic neurons in the cNTS and iNTS. The results suggest that these activated inhibitory glycinergic neurons in the NTS might be essential for the neurogenesis of load compensation responses in anesthetized animals.

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