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Oscillation, Gating, and Memory in the Respiratory Control System

Frederic L. Eldridge, David E. Millhorn

10.1002/cphy.cp030203

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 Oscillation of Respiratory Stimuli
1.1 Chemical Stimuli
1.2 Mechanical Stimuli
2 Gating
2.1 Mechanisms
2.2 Physiological Effects
3 Memory in Respiratory Control System
3.1 Memories of Short and Medium Duration
3.2 Memories of Long Duration
Figure 1. Figure 1.

Arterial pressure (AP), change of medullary extracellular fluid (ECF) pH, and airway partial pressure of CO2 () in a paralyzed ventilated cat. A: oscillations of ECF pH (0.006 units) and arterial pressure with same period ventilation produced by respirator. Time lag between inspiration (down‐stroke of CO2 tracing) and onset of alkaline shift in medullary ECF pH is ∼4 s. B: effects of reversing arterial pressure oscillations by inflation of balloon in descending aorta (horizontal bars). Reversal has no effect on amplitude or timing of medullary ECF pH oscillations and shows that they result from CO2 oscillations derived from breathing.
Figure 2. Figure 2.

Carotid body discharge and relationship to respiratory activity. A: carotid sinus nerve (CSN) activity and integrated phrenic activity in vagotomized paralyzed cat ventilated at slow rate. One CSN is intact. Activity of CSN oscillates with frequency of ventilator; phrenic bursting frequency is almost twice as fast. Arrows mark last half of inspiration, when carotid activity should be most effective in modifying inspiration. Phrenic bursts occurring at peak of oscillating CSN discharge are greater than those occurring at its nadir. Variations of phrenic activity disappeared (not shown) after remaining intact CSN was cut. AP, arterial pressure. B: CSN activity, tidal volume, and airway partial pressure of CO2 () in spontaneously breathing cat with intact vagi and 1 intact carotid body. Peak of inspiration (arrows) occurs just before nadir of CSN oscillation.

From Eldridge 64
Figure 3. Figure 3.

Facilitatory respiratory memory after stimulation of carotid sinus nerve (CSN) in paralyzed vagotomized cat with partial pressure of CO2 () kept constant by servocontroller. Recording shows facilitatory effect of CSN stimulus and slow recovery process (after‐discharge) after its cessation. Time constant of afterdischarge is 58 s.

From Eldridge and Gill‐Kumar 66
Figure 4. Figure 4.

Experiments showing that complete suppression of inspiratory activity during carotid sinus nerve (CSN) stimulation does not prevent activation of central memory or afterdischarge in paralyzed vagotomized cat. A: control experiment showing base‐line activity at left, effect of CSN stimulation of 30 s, and afterdischarge. B: base‐line activity, effect of combined CSN and vagal stimulation, and recovery. Although inspiration is completely inhibited by vagal effects during combined stimulation, poststimulation respiratory activity is augmented, just as in control experiment, and decays with approximately the same time course.

From Eldridge and Gill‐Kumar 66
Figure 5. Figure 5.

Effects of different modes of carotid sinus nerve stimulation on respiratory (phrenic) response during stimulation and on recovery process in paralyzed vagotomized cat. A: continuous stimulation. B: expiratory‐only stimulation. C: alternate‐cycle stimulation. Stimulated breaths of alternate‐cycle experiment are similar to those of continuous stimulation, and nonstimulated breaths are similar to those of expiratory stimulation. Despite differences in direct effects of stimulus, afterdischarges are similar in all 3 experiments. Slowly rising activity during expiratory‐only stimulations represents increasing activation of mechanism producing afterdischarge. AP, arterial pressure.

From Eldridge and Gill‐Kumar 68
Figure 6. Figure 6.

Integrated phrenic activity from paralyzed ventilated newborn piglet before, during, and after electrical stimulation of superior laryngeal nerve lasting (from top down) 5, 10, 30, and 45 s. Bars, duration of stimulation. With each increase of stimulus duration, period of poststimulus apnea is progressively longer and initial respiratory activity is progressively less.

From Lawson 120
Figure 7. Figure 7.

Phrenic nerve activity and integrated phrenic activity in paralyzed ventilated vagotomized cat before, during (bars, 30‐s duration), and after stimulation of pulmonary stretch receptor afferents in cervical vagus nerve. Effect of central memory shown during poststimulus recovery of 2 experiments (A and B) performed at different end‐tidal partial pressure of CO2 () levels. The effect, which is a prolonged inspiratory duration and slowed frequency, is opposite of that expected if memory involved only persistence of vagally mediated off‐switch input.
Figure 8. Figure 8.

Poststimulus effect in spinal motoneurons. Recording shows effect in paralyzed spinal (C1) cat of physical stimulation of calf muscles on phrenic burst activity evoked by rhythmic compression of posterior lower thorax. Muscle stimulation causes marked inhibition of phrenic bursts, but at its offset there is marked overshoot of activity that returns to control only after >20 s. AP, arterial pressure.

From Eldridge, Millhorn, et al. 70
Figure 9. Figure 9.

Long‐lasting facilitatory memory induced by carotid sinus nerve (CSN) stimulation. Records are from paralyzed vagotomized glomectomized cat with end‐tidal partial pressure of CO2 () held constant at 31 Torr by servocontroller. Records show arterial pressure (AP) and integrated phrenic nerve activity. Top: control, CSN stimulation of 2 min, and recovery (afterdischarge). Phrenic activity is increased over control even after complete decay of afterdischarge at 5 min. The 2nd, 3rd, and 4th stimulations are not shown, but phrenic activity increases further both before and after 5th stimulation (middle). Phrenic activity remains elevated for at least 50 min after final stimulation (bottom).

From Millhorn, Eldridge, and Waldrop 134
Figure 10. Figure 10.

Long‐lasting poststimulation inhibition of respiration after stimulation of calf muscles. A: integrated phrenic activity and arterial pressure in paralyzed vagotomized glomectomized cat. Records show control, stimulation of muscles, and recovery. Brief poststimulus facilitatory memory (afterdischarge) occurs but is followed by decrease of phrenic activity to below prestimulation level. B: expanded record showing that poststimulus depression of phrenic activity persists for >30 min. AP, arterial pressure.

From Waldrop, Eldridge, and Millhorn 178


Figure 1.

Arterial pressure (AP), change of medullary extracellular fluid (ECF) pH, and airway partial pressure of CO2 () in a paralyzed ventilated cat. A: oscillations of ECF pH (0.006 units) and arterial pressure with same period ventilation produced by respirator. Time lag between inspiration (down‐stroke of CO2 tracing) and onset of alkaline shift in medullary ECF pH is ∼4 s. B: effects of reversing arterial pressure oscillations by inflation of balloon in descending aorta (horizontal bars). Reversal has no effect on amplitude or timing of medullary ECF pH oscillations and shows that they result from CO2 oscillations derived from breathing.



Figure 2.

Carotid body discharge and relationship to respiratory activity. A: carotid sinus nerve (CSN) activity and integrated phrenic activity in vagotomized paralyzed cat ventilated at slow rate. One CSN is intact. Activity of CSN oscillates with frequency of ventilator; phrenic bursting frequency is almost twice as fast. Arrows mark last half of inspiration, when carotid activity should be most effective in modifying inspiration. Phrenic bursts occurring at peak of oscillating CSN discharge are greater than those occurring at its nadir. Variations of phrenic activity disappeared (not shown) after remaining intact CSN was cut. AP, arterial pressure. B: CSN activity, tidal volume, and airway partial pressure of CO2 () in spontaneously breathing cat with intact vagi and 1 intact carotid body. Peak of inspiration (arrows) occurs just before nadir of CSN oscillation.

From Eldridge 64


Figure 3.

Facilitatory respiratory memory after stimulation of carotid sinus nerve (CSN) in paralyzed vagotomized cat with partial pressure of CO2 () kept constant by servocontroller. Recording shows facilitatory effect of CSN stimulus and slow recovery process (after‐discharge) after its cessation. Time constant of afterdischarge is 58 s.

From Eldridge and Gill‐Kumar 66


Figure 4.

Experiments showing that complete suppression of inspiratory activity during carotid sinus nerve (CSN) stimulation does not prevent activation of central memory or afterdischarge in paralyzed vagotomized cat. A: control experiment showing base‐line activity at left, effect of CSN stimulation of 30 s, and afterdischarge. B: base‐line activity, effect of combined CSN and vagal stimulation, and recovery. Although inspiration is completely inhibited by vagal effects during combined stimulation, poststimulation respiratory activity is augmented, just as in control experiment, and decays with approximately the same time course.

From Eldridge and Gill‐Kumar 66


Figure 5.

Effects of different modes of carotid sinus nerve stimulation on respiratory (phrenic) response during stimulation and on recovery process in paralyzed vagotomized cat. A: continuous stimulation. B: expiratory‐only stimulation. C: alternate‐cycle stimulation. Stimulated breaths of alternate‐cycle experiment are similar to those of continuous stimulation, and nonstimulated breaths are similar to those of expiratory stimulation. Despite differences in direct effects of stimulus, afterdischarges are similar in all 3 experiments. Slowly rising activity during expiratory‐only stimulations represents increasing activation of mechanism producing afterdischarge. AP, arterial pressure.

From Eldridge and Gill‐Kumar 68


Figure 6.

Integrated phrenic activity from paralyzed ventilated newborn piglet before, during, and after electrical stimulation of superior laryngeal nerve lasting (from top down) 5, 10, 30, and 45 s. Bars, duration of stimulation. With each increase of stimulus duration, period of poststimulus apnea is progressively longer and initial respiratory activity is progressively less.

From Lawson 120


Figure 7.

Phrenic nerve activity and integrated phrenic activity in paralyzed ventilated vagotomized cat before, during (bars, 30‐s duration), and after stimulation of pulmonary stretch receptor afferents in cervical vagus nerve. Effect of central memory shown during poststimulus recovery of 2 experiments (A and B) performed at different end‐tidal partial pressure of CO2 () levels. The effect, which is a prolonged inspiratory duration and slowed frequency, is opposite of that expected if memory involved only persistence of vagally mediated off‐switch input.



Figure 8.

Poststimulus effect in spinal motoneurons. Recording shows effect in paralyzed spinal (C1) cat of physical stimulation of calf muscles on phrenic burst activity evoked by rhythmic compression of posterior lower thorax. Muscle stimulation causes marked inhibition of phrenic bursts, but at its offset there is marked overshoot of activity that returns to control only after >20 s. AP, arterial pressure.

From Eldridge, Millhorn, et al. 70


Figure 9.

Long‐lasting facilitatory memory induced by carotid sinus nerve (CSN) stimulation. Records are from paralyzed vagotomized glomectomized cat with end‐tidal partial pressure of CO2 () held constant at 31 Torr by servocontroller. Records show arterial pressure (AP) and integrated phrenic nerve activity. Top: control, CSN stimulation of 2 min, and recovery (afterdischarge). Phrenic activity is increased over control even after complete decay of afterdischarge at 5 min. The 2nd, 3rd, and 4th stimulations are not shown, but phrenic activity increases further both before and after 5th stimulation (middle). Phrenic activity remains elevated for at least 50 min after final stimulation (bottom).

From Millhorn, Eldridge, and Waldrop 134


Figure 10.

Long‐lasting poststimulation inhibition of respiration after stimulation of calf muscles. A: integrated phrenic activity and arterial pressure in paralyzed vagotomized glomectomized cat. Records show control, stimulation of muscles, and recovery. Brief poststimulus facilitatory memory (afterdischarge) occurs but is followed by decrease of phrenic activity to below prestimulation level. B: expanded record showing that poststimulus depression of phrenic activity persists for >30 min. AP, arterial pressure.

From Waldrop, Eldridge, and Millhorn 178
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Article Title: Oscillation, Gating, and Memory in the Respiratory Control System
 

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Frederic L. Eldridge, David E. Millhorn. Oscillation, Gating, and Memory in the Respiratory Control System. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 93-114. First published in print 1986. doi: 10.1002/cphy.cp030203