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Neurophysiology of Breathing in Mammals

Jack L. Feldman

10.1002/cphy.cp010409

Source: Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Respiratory Homeostasis and Control of Respiratory Movements
1.1 Effectors of Ventilation
1.2 Respiratory Muscles and Their Innervation
1.3 Summary
2 Central Location of Respiratory Controller
2.1 Historical Background
2.2 Summary
2.3 Modern View
2.4 Brain Stem Anatomy
2.5 Classification of Respiratory Neurons
2.6 Connections Between Respiratory Neurons
2.7 Location and Mechanisms for Generation of Respiratory Patterns
2.8 Production of Respiratory Pattern
2.9 Central Pattern Generation and Respiration
2.10 Hypothesis for Role of Dorsal and Ventral Respiratory Groups in Generating Respiratory Pattern
3 Sensors
3.1 Time Course of Responses to Respiratory Afferent Stimulation
3.2 Integrated Responses to Changes in Carbon Dioxide
3.3 Integrated Responses to Changes in Oxygen
3.4 Summary
4 Mechanoreceptors
4.1 Pulmonary Stretch Receptors
4.2 Summary
5 Exercise—An Example of an Integrated Response
5.1 Critique
6 State Dependence
7 Conclusion
Figure 1. Figure 1.

Schematic drawing for neural control of ventilation. Output of brain respiratory controller activates spinal and cranial motoneurons innervating thoracoabdominal and laryngeal‐pharyngeal muscles. Thoracoabdominal muscles control configuration of rib cage and diaphragm, which via mechanical coupling of lung (broken line) results in ventilation. Ease with which air enters and leaves the lungs is determined by airway caliber, partly controlled by laryngeal‐pharyngeal muscles, and via autonomic innervation of airway smooth muscle. Ventilation, along with nonventilatory factors, determines blood and brain fluid levels of O2, CO2, and pH. Levels of these regulated variables are transduced into a pattern of afferent activity at peripheral and intracranial chemoreceptors. These signals feed into respiratory controller, which makes appropriate adjustments in its output to motoneurons, thereby controlling ventilation and regulating , pH, and related variables. Respiratory controller makes adjustments in movements based on signals from mechanoreceptors in respiratory muscles and in lung and airways. , partial pressure of O2 in arterial blood.
Figure 2. Figure 2.

Neurophysiological investigation of central respiratory pattern generation seeks to explain timing and pattern of respiratory motor nerve outflow (e.g., traces 2–6) in terms of membrane, synaptic, and network properties of neurons with respiratory‐modulated discharge patterns [top trace, extracellular activity of an inspiratory‐modulated neuron in dorsal respiratory group (DRG)] and signals provided by respiratory‐related afferents, such as pulmonary mechanoreceptors. Traces from anesthetized, vagotomized adult cat. R, right; L, left; Phr, phrenic nerve; IC, intercostal nerve; T3, T7, T10: 3rd, 7th, and 10th thoracic root.
Figure 3. Figure 3.

Ramón y Cajal's model for respiratory control. Arrows indicate direction of nerve impulses. Respiratory neurons in solitary tract process information from vagal pulmonary afferents (K) [cell bodies in nodose ganglion (J)] and some blood factor present in local capillaries (A). Descending control signals go to spinal motoneurons (D) innervating intercostal muscles (F) or diaphragm (E, G).

From Ramón y Cajal 469
Figure 4. Figure 4.

A: ventral view; location in cat brain stem of ventral medullary regions possibly involved in central chemoreception. B‐E: dorsal view; dorsal (DRG), ventral (VRG), and pontine (PRG) respiratory groups, major clusters of respiratory related neurons. A, cranial nerves as indicated; C1, first cervical spinal root. Ventral surface is highly vascularized and only major blood vessels are indicated. Three areas are indicated where cooling, stimulation, and/or coagulation lead to reproducible alterations in respiratory outflow (see INTRACRANIAL CARBON DIOXIDE RECEPTION …, p. 492). B: cerebellum removed (normal position indicated by dotted lines, cerebellar peduncles indicated by flat surface just medial to V, VII, and VIII nerve roots). Populations of neurons are major concentrations of extracellularly recordable respiratory‐modulated neurons. Ventrolateral column, in regions of nucleus ambiguus and nucleus retroambigualis from C1 to retrofacial nucleus, is referred to as VRG. Population of predominantly expiratory neurons is most caudal (caudal VRG). Population of predominantly inspiratory neurons is between obex and retrofacial nucleus (rostral VRG). Another population of expiratory neurons is most rostral, just medial to retrofacial nucleus; this is referred to as the Bötzinger Complex (BötC). Dorsomedial population, spanning ∼2.0 mm rostral from obex, is in region of ventrolateral nucleus of solitary tract; it is referred to as DRG and contains predominantly inspiratory neurons. In dorsolateral rostral pons, in region of parabrachial nuclei and Kölliker‐Fuse nucleus, is another concentration of neurons seen most clearly in vagotomized preparations. It consists of a lateral inspiratory population and a medial expiratory population bridged by a phase‐spanning inspiratory‐expiratory (IE) population. This region is the PRG. C‐E: transverse sections of brain stem at levels indicated in B (see ref. 51 for detailed anatomical descriptions). Location and extent of populations are only approximate and can vary in different preparations. A, nucleus ambiguus; AP, area postrema; BC, brachium conjunctivum; BP, brachium pontis; DMV, dorsal motor nucleus of vagus; KF, Kölliker‐Fuse nucleus; mV, motor trigeminal nucleus; NPBL, nucleus parabrachialis lateralis; NPBM, nucleus parabrachialis medialis; S, solitary tract; SV, spinal trigeminal nucleus; VH, ventral horn.
Figure 5. Figure 5.

Cycle‐triggered histograms of impulse discharge patterns of respiratory‐modulated brain stem neurons in decerebrate, barbiturate‐, or chloralose‐urethan‐anesthetized cats. Ordinate marker, 50 impulses/s. Onsets and offsets of discharge are smeared due to temporal dispersion of individual cycle lengths. Onsets and offsets of discharges of many I and E neurons overlap each other.
Figure 6. Figure 6.

Effect of multiple microlesions in VRG and DRG on integrated phrenic (Phr) nerve discharge in vagotomized anesthetized cat. Traces are clustered in pairs and each pair represents integrated phrenic nerve activity before and after lesion in area specified. A: left phrenic nerve discharge; B: right phrenic nerve discharge; C: locations of lesions, reconstructed from histological sections. Lesions were not made in rostral portions of left VRG because no respiratory‐modulated activity was found at sites indicated by Xs. Microlesions were made by passing current between 2 microelectrodes positioned ∼1 mm apart in same population. All lesions were completed in <10 h. Note that predominant effect of these lesions is to reduce amplitude of Phr nerve activity, with only modest effect on timing.

From Speck and Feldman 587
Figure 7. Figure 7.

Inspiratory cycle‐triggered histograms of phrenic nerve activity representing control cycles with no stimulation (thin line) and cycles with spinal cord stimulation at the C2 level, with optimal placement for stimulating descending axons of inspiratory premotor neurons (400‐ms train, 50 Hz, 100 μA; thick line) at 2 different delays. Stimulation elicits very short latency excitation due to orthodromic excitation followed by brief period of reduced activity. Transient depression of phrenic nerve activity has no lasting influence on subsequent evolution of phrenic discharge. Bins are 20 ms.

From Feldman et al. 221
Figure 8. Figure 8.

Generation of rhythmic movements can be considered to result from interaction among 4 components. Many different rhythmic patterns of motoneuronal activity, as indicated in neurograms at bottom, underlie resulting coordinated movement.

From Feldman and Grillner 219
Figure 9. Figure 9.

Examples of experimental perturbations that have marked effects on pattern of augmenting phrenic activity with modest change in timing. A: alteration of end‐expiratory percent CO2 in vagotomized and paralyzed cats; B: successive microlesions of DRG and VRG in vagotomized cat (see Fig. 6).
Figure 10. Figure 10.

Two different schematic models for respiratory pattern generation. A: threshold model showing reciprocal relationship between amplitude of outflow and phase timing. B: timer model where amplitude of outflow and timing are separately determined; ⊝, possible pacemaker involvement in function generation.

From Feldman 210
Figure 11. Figure 11.

Cross‐correlation histogram and neuron → contralateral phrenic nerve correlations of an inspiratory augmenting neuron (I↗) and an inspiratory decrementing neuron (I), which were recorded simultaneously from separate microelectrodes in the VRG. A: cross‐correlogram of these 2 neurons exhibits a peak straddling zero lag. Underlying interaction responsible for this peak may be either mutual excitation or shared common input that may be excitatory or inhibitory. Means and SDs for indicated ranges of lag are shown on right. B: cross correlations between each of 2 neurons and contralateral phrenic and ipsilateral recurrent laryngeal nerve activities. Nerve activities were full‐wave rectified before processing. Mean and SD for each correlation is shown on left. Note peaks in neuron‐phrenic nerve correlations that suggest a projection from these neurons to phrenic motoneurons but not to recurrent laryngeal motoneurons. Recordings were obtained in paralyzed, nonvagotomized cat ventilated with cycle‐triggered pump. Bins are 0.2 ms.

From Feldman and Speck 223
Figure 12. Figure 12.

Reciprocal inhibition demonstrated by intracellular recording of membrane potentials and current injection (A, B) or Cl− injection (C). A: phrenic motoneuron (top trace) and whole phrenic nerve (bottom trace) activities before (A1) and after (A2) hyperpolarizing current injection. B: internal intercostal motoneuron (top trace) and diaphragmatic EMG (bottom trace) before (B1) and after (B2) hyperpolarizing current injection. C: DRG inspiratory neuron (MPRB) and phrenic motoneuronal activity (PN) before and during Cl− injection. EMG, electromyogram.

A from Berger 49; B from Sears 557; C from Richter et al. 515
Figure 13. Figure 13.

Effects on respiratory motor activity of stimulus trains (ST) delivered to vagus or superior laryngeal nerve. All traces are average of 21 respiratory cycles. Top trace represents control phrenic nerve activity. In middle trace, vagus nerve stimulation begins 100 ms after inspiratory onset and continues until inspiratory termination. In bottom trace, superior laryngeal nerve stimulation begins 100 ms after inspiratory onset and continues for 100 ms.

From Iscoe, Feldman, and Cohen 313
Figure 14. Figure 14.

Magnitude of perturbations necessary to produce inspiratory → expiratory phase transitions declines with time during inspiration. In all curves, ordinates represent magnitude of lung inflation (A‐C) or stimulating voltage (D, E); abscissas represent inspiratory duration [TI]. A: in spontaneously breathing anesthetized cats rebreathing from a small balloon, inspiratory duration decreases as CO2 necessarily increases. B: in paralyzed anesthetized or decerebrate cats, lung volume [produced by artificial inflation at higher (▴) or lower (▪) pressures] necessary to terminate inspiration is higher for shorter inspirations. C: after lesioning in PRG (▪), volume threshold for inspiratory phase termination greatly increases but still shows a time‐dependent decline (▴, prelesion control). D: in anesthetized cats, increased voltages of PRG stimulation are needed for earlier termination of inspiration. The voltage threshold is less when lungs are inflated (•) than when lungs are deflated (•). E: in decerebrate cats, higher current stimulation of intercostal nerve afferents is needed to terminate inspiration earlier. Increasing CO2 raises the threshold.

A from Clark and Euler 125; B and C from Feldman and Gautier 218; D from Euler and Trippenbach 204; E from Speck and Webber 588
Figure 15. Figure 15.

Effects on peak integrated phrenic nerve activity of cooling the intermediate area of the ventral medulla. A: ventral surface temperatures at different levels; B: levels at different ventral surface temperatures. Data in A and B from vagotomized cat on constant artificial ventilation.

From Cherniack et al. 121
Figure 16. Figure 16.

A: mean values of carotid body‐chemoreceptor discharge in response to changes in at 3 levels of CO2. B: ventilatory response to hypoxia in 2 human subjects, 1 with low response (•), 1 with high response (•). Ventilation is plotted against alveolar . This is traditional hyperbolic response curve

A from Vidruk and Dempsey 613; B from Rebuck and Slutsky 498
Figure 17. Figure 17.

Changes in tidal volume or peak phrenic activity with carotid sinus nerve stimuli given at various times during inspiration. Composite results of all cats studied, arranged in bins for each 5% of inspiration. All stimuli were 0.5 s in duration at 20–25 Hz. To normalize data obtained in different cats, the change from mean of unstimulated breaths has been used.

From Eldridge 192
Figure 18. Figure 18.

A‐C: effects of changes in pulmonary afferent and PRG activity on integrated phrenic nerve activity in 3 anesthetized paralyzed cats ventilated with a cycle‐triggered pump. Bars indicate inflation (A1, A2, B, C1 and C2) or vagal electrical stimulation (A3). A1: intact cat, no inflation during 4th and 9th cycle; A2: after bivagotomy; and A3: stimulation of afferent vagi. Stimulation lasted for duration of inspiration and was stopped for 4th and 9th cycles. Time scale: 1 s/small division. B: cat after bilateral lesions of PRG. When pump was stopped, there was apneustic inspiration that ceased spontaneously. C1: cat after bilateral lesions of PRG. Apneusis stopped only after inflation that commenced 10 s after onset of inspiration. Note that inspiratory cutoff produced by inflation was gradual. C2: inflation with smaller flow than C1. Note partial inhibition produced by 2 inflations during apneustic inspiration. Time scale: 1 s/small division.

From Feldman and Gautier 218
Figure 19. Figure 19.

Cycle‐triggered histograms of phrenic and recurrent laryngeal discharge in anesthetized paralyzed cat. Heavy lines indicate average discharge from 11 cycles with no lung inflation; light lines indicate cycles with lung inflation coincident with phrenic discharge. Note that lung inflation has no effect on evolution of phrenic discharge pattern but markedly inhibits laryngeal discharge.

From Feldman and Speck 223
Figure 20. Figure 20.

Types of inspiratory neuronal responses in impulse activity to withholding inflation in paralyzed anesthetized cats. Light lines, control; inflation delivered during inspiration. Heavy lines, test; inflation not delivered during inspiration. Each set of traces consists of cycle‐triggered histograms (50‐ms bins) of phrenic motoneuronal activity and neuronal impulse activity in equal numbers of control and test cycles. Number of cycles averaged: A, D, E, 20; B, 17; and C, 14. Types of neuronal responses: A, inflation (0), no change in slope of neuronal histogram; B, inflation (+), excited by inflation; C, inflation (0) recruited, no change of discharge (which stays at zero level) during time corresponding to control inspiratory duration, recruitment of firing during lengthened part of inspiration; D, inflation (−), inhibited by inflation; E, inflation (−) tonic, respiratory modulation inhibited by inflation, tonic discharge level.

From Cohen and Feldman 138
Figure 21. Figure 21.

Properties of hypothetical inhibitory process, ϕ, controlling expiratory duration, Te, as modified by stimulus inputs that shorten (left) or lengthen (right) duration of E. Phi is a function that decays exponentially (time constant = 1.5 s) from its maximum value of 1.0 at start of expiration. Control Te is 3.0 s; threshold for I onset (ϕTHR) is arbitrarily set at 0.135. Left top, vertical arrows represent pulse inputs that cause reduction in ϕ by 0.25, followed by a rebound increase of 0.125; left bottom, shortening of expiration produced by inputs at different times; right top, vertical arrows and lines represent pulse inputs that cause increase in ϕ of 0.250; right bottom, lengthening of Te produced by inputs at different times. Tec, control Te; Test, stimulus cycle Te.

From Cohen and Feldman 138
Figure 22. Figure 22.

Ventilatory response (Va) and arterial acid‐base status during steady‐state rhythmic exercise in healthy young adults. Abscissa indicates exercise intensity as a function of CO2 production (). Insert shows time course of ventilatory response.

From Dempsey et al. 166
Figure 23. Figure 23.

Polygraph traces of phrenic responses and responses of an I(−) tonic neuron located in PRG, preventing inflation in a paralyzed decerebrate cat for 1 test cycle. Phr, integrated phrenic discharge; unit spikes, standard pulses derived from neuronal impulses. Inflation was applied during inspiration except during 3rd cycle when inflation was withheld (see also Fig. 20E).

From Feldman et al. 216


Figure 1.

Schematic drawing for neural control of ventilation. Output of brain respiratory controller activates spinal and cranial motoneurons innervating thoracoabdominal and laryngeal‐pharyngeal muscles. Thoracoabdominal muscles control configuration of rib cage and diaphragm, which via mechanical coupling of lung (broken line) results in ventilation. Ease with which air enters and leaves the lungs is determined by airway caliber, partly controlled by laryngeal‐pharyngeal muscles, and via autonomic innervation of airway smooth muscle. Ventilation, along with nonventilatory factors, determines blood and brain fluid levels of O2, CO2, and pH. Levels of these regulated variables are transduced into a pattern of afferent activity at peripheral and intracranial chemoreceptors. These signals feed into respiratory controller, which makes appropriate adjustments in its output to motoneurons, thereby controlling ventilation and regulating , pH, and related variables. Respiratory controller makes adjustments in movements based on signals from mechanoreceptors in respiratory muscles and in lung and airways. , partial pressure of O2 in arterial blood.



Figure 2.

Neurophysiological investigation of central respiratory pattern generation seeks to explain timing and pattern of respiratory motor nerve outflow (e.g., traces 2–6) in terms of membrane, synaptic, and network properties of neurons with respiratory‐modulated discharge patterns [top trace, extracellular activity of an inspiratory‐modulated neuron in dorsal respiratory group (DRG)] and signals provided by respiratory‐related afferents, such as pulmonary mechanoreceptors. Traces from anesthetized, vagotomized adult cat. R, right; L, left; Phr, phrenic nerve; IC, intercostal nerve; T3, T7, T10: 3rd, 7th, and 10th thoracic root.



Figure 3.

Ramón y Cajal's model for respiratory control. Arrows indicate direction of nerve impulses. Respiratory neurons in solitary tract process information from vagal pulmonary afferents (K) [cell bodies in nodose ganglion (J)] and some blood factor present in local capillaries (A). Descending control signals go to spinal motoneurons (D) innervating intercostal muscles (F) or diaphragm (E, G).

From Ramón y Cajal 469


Figure 4.

A: ventral view; location in cat brain stem of ventral medullary regions possibly involved in central chemoreception. B‐E: dorsal view; dorsal (DRG), ventral (VRG), and pontine (PRG) respiratory groups, major clusters of respiratory related neurons. A, cranial nerves as indicated; C1, first cervical spinal root. Ventral surface is highly vascularized and only major blood vessels are indicated. Three areas are indicated where cooling, stimulation, and/or coagulation lead to reproducible alterations in respiratory outflow (see INTRACRANIAL CARBON DIOXIDE RECEPTION …, p. 492). B: cerebellum removed (normal position indicated by dotted lines, cerebellar peduncles indicated by flat surface just medial to V, VII, and VIII nerve roots). Populations of neurons are major concentrations of extracellularly recordable respiratory‐modulated neurons. Ventrolateral column, in regions of nucleus ambiguus and nucleus retroambigualis from C1 to retrofacial nucleus, is referred to as VRG. Population of predominantly expiratory neurons is most caudal (caudal VRG). Population of predominantly inspiratory neurons is between obex and retrofacial nucleus (rostral VRG). Another population of expiratory neurons is most rostral, just medial to retrofacial nucleus; this is referred to as the Bötzinger Complex (BötC). Dorsomedial population, spanning ∼2.0 mm rostral from obex, is in region of ventrolateral nucleus of solitary tract; it is referred to as DRG and contains predominantly inspiratory neurons. In dorsolateral rostral pons, in region of parabrachial nuclei and Kölliker‐Fuse nucleus, is another concentration of neurons seen most clearly in vagotomized preparations. It consists of a lateral inspiratory population and a medial expiratory population bridged by a phase‐spanning inspiratory‐expiratory (IE) population. This region is the PRG. C‐E: transverse sections of brain stem at levels indicated in B (see ref. 51 for detailed anatomical descriptions). Location and extent of populations are only approximate and can vary in different preparations. A, nucleus ambiguus; AP, area postrema; BC, brachium conjunctivum; BP, brachium pontis; DMV, dorsal motor nucleus of vagus; KF, Kölliker‐Fuse nucleus; mV, motor trigeminal nucleus; NPBL, nucleus parabrachialis lateralis; NPBM, nucleus parabrachialis medialis; S, solitary tract; SV, spinal trigeminal nucleus; VH, ventral horn.



Figure 5.

Cycle‐triggered histograms of impulse discharge patterns of respiratory‐modulated brain stem neurons in decerebrate, barbiturate‐, or chloralose‐urethan‐anesthetized cats. Ordinate marker, 50 impulses/s. Onsets and offsets of discharge are smeared due to temporal dispersion of individual cycle lengths. Onsets and offsets of discharges of many I and E neurons overlap each other.



Figure 6.

Effect of multiple microlesions in VRG and DRG on integrated phrenic (Phr) nerve discharge in vagotomized anesthetized cat. Traces are clustered in pairs and each pair represents integrated phrenic nerve activity before and after lesion in area specified. A: left phrenic nerve discharge; B: right phrenic nerve discharge; C: locations of lesions, reconstructed from histological sections. Lesions were not made in rostral portions of left VRG because no respiratory‐modulated activity was found at sites indicated by Xs. Microlesions were made by passing current between 2 microelectrodes positioned ∼1 mm apart in same population. All lesions were completed in <10 h. Note that predominant effect of these lesions is to reduce amplitude of Phr nerve activity, with only modest effect on timing.

From Speck and Feldman 587


Figure 7.

Inspiratory cycle‐triggered histograms of phrenic nerve activity representing control cycles with no stimulation (thin line) and cycles with spinal cord stimulation at the C2 level, with optimal placement for stimulating descending axons of inspiratory premotor neurons (400‐ms train, 50 Hz, 100 μA; thick line) at 2 different delays. Stimulation elicits very short latency excitation due to orthodromic excitation followed by brief period of reduced activity. Transient depression of phrenic nerve activity has no lasting influence on subsequent evolution of phrenic discharge. Bins are 20 ms.

From Feldman et al. 221


Figure 8.

Generation of rhythmic movements can be considered to result from interaction among 4 components. Many different rhythmic patterns of motoneuronal activity, as indicated in neurograms at bottom, underlie resulting coordinated movement.

From Feldman and Grillner 219


Figure 9.

Examples of experimental perturbations that have marked effects on pattern of augmenting phrenic activity with modest change in timing. A: alteration of end‐expiratory percent CO2 in vagotomized and paralyzed cats; B: successive microlesions of DRG and VRG in vagotomized cat (see Fig. 6).



Figure 10.

Two different schematic models for respiratory pattern generation. A: threshold model showing reciprocal relationship between amplitude of outflow and phase timing. B: timer model where amplitude of outflow and timing are separately determined; ⊝, possible pacemaker involvement in function generation.

From Feldman 210


Figure 11.

Cross‐correlation histogram and neuron → contralateral phrenic nerve correlations of an inspiratory augmenting neuron (I↗) and an inspiratory decrementing neuron (I), which were recorded simultaneously from separate microelectrodes in the VRG. A: cross‐correlogram of these 2 neurons exhibits a peak straddling zero lag. Underlying interaction responsible for this peak may be either mutual excitation or shared common input that may be excitatory or inhibitory. Means and SDs for indicated ranges of lag are shown on right. B: cross correlations between each of 2 neurons and contralateral phrenic and ipsilateral recurrent laryngeal nerve activities. Nerve activities were full‐wave rectified before processing. Mean and SD for each correlation is shown on left. Note peaks in neuron‐phrenic nerve correlations that suggest a projection from these neurons to phrenic motoneurons but not to recurrent laryngeal motoneurons. Recordings were obtained in paralyzed, nonvagotomized cat ventilated with cycle‐triggered pump. Bins are 0.2 ms.

From Feldman and Speck 223


Figure 12.

Reciprocal inhibition demonstrated by intracellular recording of membrane potentials and current injection (A, B) or Cl− injection (C). A: phrenic motoneuron (top trace) and whole phrenic nerve (bottom trace) activities before (A1) and after (A2) hyperpolarizing current injection. B: internal intercostal motoneuron (top trace) and diaphragmatic EMG (bottom trace) before (B1) and after (B2) hyperpolarizing current injection. C: DRG inspiratory neuron (MPRB) and phrenic motoneuronal activity (PN) before and during Cl− injection. EMG, electromyogram.

A from Berger 49; B from Sears 557; C from Richter et al. 515


Figure 13.

Effects on respiratory motor activity of stimulus trains (ST) delivered to vagus or superior laryngeal nerve. All traces are average of 21 respiratory cycles. Top trace represents control phrenic nerve activity. In middle trace, vagus nerve stimulation begins 100 ms after inspiratory onset and continues until inspiratory termination. In bottom trace, superior laryngeal nerve stimulation begins 100 ms after inspiratory onset and continues for 100 ms.

From Iscoe, Feldman, and Cohen 313


Figure 14.

Magnitude of perturbations necessary to produce inspiratory → expiratory phase transitions declines with time during inspiration. In all curves, ordinates represent magnitude of lung inflation (A‐C) or stimulating voltage (D, E); abscissas represent inspiratory duration [TI]. A: in spontaneously breathing anesthetized cats rebreathing from a small balloon, inspiratory duration decreases as CO2 necessarily increases. B: in paralyzed anesthetized or decerebrate cats, lung volume [produced by artificial inflation at higher (▴) or lower (▪) pressures] necessary to terminate inspiration is higher for shorter inspirations. C: after lesioning in PRG (▪), volume threshold for inspiratory phase termination greatly increases but still shows a time‐dependent decline (▴, prelesion control). D: in anesthetized cats, increased voltages of PRG stimulation are needed for earlier termination of inspiration. The voltage threshold is less when lungs are inflated (•) than when lungs are deflated (•). E: in decerebrate cats, higher current stimulation of intercostal nerve afferents is needed to terminate inspiration earlier. Increasing CO2 raises the threshold.

A from Clark and Euler 125; B and C from Feldman and Gautier 218; D from Euler and Trippenbach 204; E from Speck and Webber 588


Figure 15.

Effects on peak integrated phrenic nerve activity of cooling the intermediate area of the ventral medulla. A: ventral surface temperatures at different levels; B: levels at different ventral surface temperatures. Data in A and B from vagotomized cat on constant artificial ventilation.

From Cherniack et al. 121


Figure 16.

A: mean values of carotid body‐chemoreceptor discharge in response to changes in at 3 levels of CO2. B: ventilatory response to hypoxia in 2 human subjects, 1 with low response (•), 1 with high response (•). Ventilation is plotted against alveolar . This is traditional hyperbolic response curve

A from Vidruk and Dempsey 613; B from Rebuck and Slutsky 498


Figure 17.

Changes in tidal volume or peak phrenic activity with carotid sinus nerve stimuli given at various times during inspiration. Composite results of all cats studied, arranged in bins for each 5% of inspiration. All stimuli were 0.5 s in duration at 20–25 Hz. To normalize data obtained in different cats, the change from mean of unstimulated breaths has been used.

From Eldridge 192


Figure 18.

A‐C: effects of changes in pulmonary afferent and PRG activity on integrated phrenic nerve activity in 3 anesthetized paralyzed cats ventilated with a cycle‐triggered pump. Bars indicate inflation (A1, A2, B, C1 and C2) or vagal electrical stimulation (A3). A1: intact cat, no inflation during 4th and 9th cycle; A2: after bivagotomy; and A3: stimulation of afferent vagi. Stimulation lasted for duration of inspiration and was stopped for 4th and 9th cycles. Time scale: 1 s/small division. B: cat after bilateral lesions of PRG. When pump was stopped, there was apneustic inspiration that ceased spontaneously. C1: cat after bilateral lesions of PRG. Apneusis stopped only after inflation that commenced 10 s after onset of inspiration. Note that inspiratory cutoff produced by inflation was gradual. C2: inflation with smaller flow than C1. Note partial inhibition produced by 2 inflations during apneustic inspiration. Time scale: 1 s/small division.

From Feldman and Gautier 218


Figure 19.

Cycle‐triggered histograms of phrenic and recurrent laryngeal discharge in anesthetized paralyzed cat. Heavy lines indicate average discharge from 11 cycles with no lung inflation; light lines indicate cycles with lung inflation coincident with phrenic discharge. Note that lung inflation has no effect on evolution of phrenic discharge pattern but markedly inhibits laryngeal discharge.

From Feldman and Speck 223


Figure 20.

Types of inspiratory neuronal responses in impulse activity to withholding inflation in paralyzed anesthetized cats. Light lines, control; inflation delivered during inspiration. Heavy lines, test; inflation not delivered during inspiration. Each set of traces consists of cycle‐triggered histograms (50‐ms bins) of phrenic motoneuronal activity and neuronal impulse activity in equal numbers of control and test cycles. Number of cycles averaged: A, D, E, 20; B, 17; and C, 14. Types of neuronal responses: A, inflation (0), no change in slope of neuronal histogram; B, inflation (+), excited by inflation; C, inflation (0) recruited, no change of discharge (which stays at zero level) during time corresponding to control inspiratory duration, recruitment of firing during lengthened part of inspiration; D, inflation (−), inhibited by inflation; E, inflation (−) tonic, respiratory modulation inhibited by inflation, tonic discharge level.

From Cohen and Feldman 138


Figure 21.

Properties of hypothetical inhibitory process, ϕ, controlling expiratory duration, Te, as modified by stimulus inputs that shorten (left) or lengthen (right) duration of E. Phi is a function that decays exponentially (time constant = 1.5 s) from its maximum value of 1.0 at start of expiration. Control Te is 3.0 s; threshold for I onset (ϕTHR) is arbitrarily set at 0.135. Left top, vertical arrows represent pulse inputs that cause reduction in ϕ by 0.25, followed by a rebound increase of 0.125; left bottom, shortening of expiration produced by inputs at different times; right top, vertical arrows and lines represent pulse inputs that cause increase in ϕ of 0.250; right bottom, lengthening of Te produced by inputs at different times. Tec, control Te; Test, stimulus cycle Te.

From Cohen and Feldman 138


Figure 22.

Ventilatory response (Va) and arterial acid‐base status during steady‐state rhythmic exercise in healthy young adults. Abscissa indicates exercise intensity as a function of CO2 production (). Insert shows time course of ventilatory response.

From Dempsey et al. 166


Figure 23.

Polygraph traces of phrenic responses and responses of an I(−) tonic neuron located in PRG, preventing inflation in a paralyzed decerebrate cat for 1 test cycle. Phr, integrated phrenic discharge; unit spikes, standard pulses derived from neuronal impulses. Inflation was applied during inspiration except during 3rd cycle when inflation was withheld (see also Fig. 20E).

From Feldman et al. 216
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Article Title: Neurophysiology of Breathing in Mammals
 

How to Cite

Jack L. Feldman. Neurophysiology of Breathing in Mammals. Compr Physiol 2011, Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain: 463-524. First published in print 1986. doi: 10.1002/cphy.cp010409