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Brain Stem Mechanisms for Generation and Control of Breathing Pattern

Curt Von Euler

10.1002/cphy.cp030201

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 Homeostatic and Behavioral Regulation of Breathing—Aims and Compromises
2 Some General Features of Rhythm‐Generating Mechanisms for Automatic Breathing
2.1 Is There More Than One CPG for Automatic Breathing?
2.2 Spinal Pattern Generator
2.3 Bilaterally Symmetric CPG
3 Localization of Basic Rhythm Generator for Automatic Breathing
3.1 Brain Stem Transections
3.2 Localization by Electrical Stimulation
3.3 Localization by Recording RR Neural Activity
4 Distribution of RR Neurons and Their Functional Properties
4.1 General Outline of Medullary RR Neurons
4.2 Ventral Respiratory Group
4.3 Dorsal Respiratory Group
4.4 Problem of Reciprocal Interaction Between Inspiratory and Expiratory Bulbospinal Neurons
4.5 Why Are There Two Separate Pools of Inspiratory Premotor Neurons?
4.6 Summary
5 Functional Organization of Respiratory CPG—Systems Behavior
5.1 Methods
5.2 General Organizational Features of CPG and Its Main Afferent Feedback Systems
5.3 Mechanisms Controlling Inspiratory Parameters
5.4 Control of Expiratory Parameters
5.5 Concept of Breathing Pattern for Ergometric Minimization
6 Conclusions
Figure 1. Figure 1.

Pulse rate (upper trace) and respiration (lower trace) in human listening to dissonant atonal electronic music by Stockhausen (left) and melodic music by Chopin (right).

From Harrer 540
Figure 2. Figure 2.

Cyclic (A) and tonic (B) neuronal discharge patterns from different sites in medulla oblongata in neurally isolated and completely de‐nervated rhombencephalon in unanesthetized cat (delimited by intracollicular transection and transection at 1st cervical segment). A: 1, ventilation with 6.5% CO2 in O2; 2, ventilation with pure O2. B: 1, ventilation with 6.5% CO2 in O2; 2, ventilation with pure O2; 3, ventilation with 3% CO2 in O2; 4, ventilation with 15% CO2 in O2. Time, 20 cycles/s.

Adapted from Euler and Söderberg 177
Figure 3. Figure 3.

Effects of midsagittal section through rabbit medulla on respiratory motor outputs from left (A, B) and right (C, E) phrenic nerves. “Integrated” (A, C) and direct (B, E) records of efferent phrenic activity. D: reference line for end‐tidal CO2 trace in F; G: blood pressure. Note that different rhythms and patterns are obtained from the 2 sides. Bisection of medulla extended from 4 mm rostral to obex to 1 mm caudal to obex.

From Gromysz and Karczewski 222
Figure 4. Figure 4.

Discharge patterns of various respiration‐related neurons of the ventral respiratory group plotted for a single respiratory cycle. A‐D: late‐peak inspiration‐related neurons; E‐H: expiration‐related neurons; I‐K: early‐burst inspiration‐related cells. Bottom trace: chest circumference, inspiratory deflection upward.

From Merrill 362
Figure 5. Figure 5.

Medulla (and part of spinal cord) with the 2 main aggregates of respiration‐related neurons in medulla: longitudinal column constituting ventral respiratory group (VRG) with its 3 subdivisions (marked on right) and dorsal respiratory group (DRG). Diagram further shows the group of inspiration‐related relay neurons in 1st and 2nd segments of cervical spinal cord (C1‐C2 group of Aoki). Diagram shows locations of main groups of expiratory (circles) and inspiratory (triangles) bulbospinal and relay neurons (open symbols) and their descending axons projecting to spinal motoneurons (filled symbols). In nucleus ambiguus (NA), laryngeal motoneurons are indicated. For simplicity neurons and axons are only represented on 1 side. Böt. C, Bötzinger complex; NPA, nucleus para‐ambigualis; NRA, nucleus retroambigualis; NTS, nucleus tractus solitarius; X, 10th cranial nerve.
Figure 6. Figure 6.

Major aggregates (shaded areas) of respiration‐related neurons and their afferent (left) and efferent (right) connections, as revealed by anatomical and electrophysiological mapping techniques. A, B: medial parabrachial‐Kölliker‐Fuse complex; C, D: dorsal respiratory group; E, F: ventral respiratory group. Filled triangles, cell bodies; solid lines, axons and axon collaterals; Y‐shaped endings, axonal terminations. BC, brachium conjunctivum; Böt. C, Bötzinger complex; NPA, nucleus para‐ambigualis; NPBM, nucleus parabrachialis medialis; NRA, nucleus retroambigualis; NTS, nucleus tractus solitarius.

From Kalia 275. Reproduced with permission from Annu. Rev. Physiol, vol. 43. © 1981 by Annual Reviews, Inc
Figure 7. Figure 7.

Projections of different groups of medullary respiration‐related neurons. A: inspiratory bulbospinal neurons of nucleus para‐ambigualis (NPA) of the ventral respiratory group. B: early‐burst inspiration‐related neurons of NPA. (Main axonal branches probably cross midline at level rostral to obex, not as indicated here.) C: inspiratory bulbospinal neurons of nucleus tractus solitarius (NTS) of dorsal respiratory group. D: expiratory bulbospinal premotor neurons of nucleus retroambigualis (NRA) of ventral respiratory group, insp, Inspiratory; exp, expiratory. Large filled circles, cell bodies; small filled circles, axonal terminations.

Adapted from Merrill 364
Figure 8. Figure 8.

Locations of transverse lesions used to interrupt inputs to nucleus retroambigualis expiration‐related neurons in experiments described in text.

From Merrill 364
Figure 9. Figure 9.

Medullary projections of expiration‐related neurons of the Bötzinger complex (Böt). Projections to contralateral ventrolateral nucleus tractus solitarius (NST) and ipsilateral caudal nucleus retroambigualis (NRA) have been established with electrophysiological techniques. Projections to ipsilateral inspiratory (insp) nucleus para‐ambigualis regions appear likely. Projections to phrenic motoneuron pool have subsequently been established and reported to be inhibitory, exp, Expiratory.

From Merrill 365
Figure 10. Figure 10.

Inspiratory Rα neuron. Traces A and B (top to bottom): neuron discharge, phrenic neurogram, “integrated” phrenic activity, and intratracheal pressure. A: respirator driven by “integrated” phrenic activity and switched off during middle of 3 inspirations with no change in initial rate of increase of activity. Prolongation of inspiration due to lack of volume feedback. B: respirator driven by sine wave generator; no influence by inflations and deflations on discharge rate. Neuron could not be driven by electrical stimulation of vagus nerves. C: driven spike in response to single shocks to contralateral ventrolateral funiculus of cervical cord at the 4th cervical segment. Latency, 1.1‐1.4 ms at conduction distance of 42 mm; time, 2,000 cycles/s.

From Euler et al. 173
Figure 11. Figure 11.

Discharge patterns of 2 Rβ neurons in cat under pentobarbital anesthesia paralyzed and artificially ventilated by respirator governed by efferent phrenic activity. Trace A (top to bottom): instantaneous frequency record, neuron discharge, “integrated” phrenic activity, and intratracheal pressure. During first 2 inspiratory discharges, respirator was inflating lungs (with some time lag). During last inspiration, respirator was switched off so that neuron received central inspiratory activity input, giving a slower rate of increase of inspiratory activity, which reaches roughly the same value as in first 2 breaths, but after a longer time. Inspiration terminates when discharge rate reaches approximately the same level with or without volume feedback. Traces B and C (top to bottom): neuron discharge, efferent phrenic neurogram, intratracheal pressure (with some delay), and “integrated” phrenic activity. This Rβ neuron has somewhat higher threshold than that in A. B: respirator driven by “integrated” phrenic activity (after slight time lag). C: respirator driven by sine wave generator. Neuron discharge modulated by both inspiratory activity (central inspiratory activity input) and lung volume variations. Note that deflation coinciding with peak phrenic activity reduces neuron discharge and prolongs inspiratory phase. Neuron is responsive during postinspiration inspiratory activity.

Adapted from Euler et al. 173
Figure 12. Figure 12.

Representation of Rβ neurons and their function as a summarizer of central inspiratory activity (CIA) corollary activity and pulmonary stretch‐receptor (PSR) afferent activity. The CIA corollary activity is probably not mediated by the Rα inspiratory premotor neurons; Rα and Rβ neurons probably share a common CIA input. IBS, inspiratory bulbospinal neuron.
Figure 13. Figure 13.

Discharge patterns (cycle‐triggered histograms) of early expiration‐related neurons in response to 2 kinds of reflex modulations of expiratory duration (TE). A: withholding inflation in inspiration (I) causes lengthening of inspiratory duration and proportional prolongation of TE. B: inflation during expiratory phase elicits a TE‐prolonging reflex. TE(C), average control TE; TE (T), average test TE. Test inflation (ITP) indicated in inset; duration, 80 ms; averages of 8 cycles.

From Feldman and Cohen 185
Figure 14. Figure 14.

Excitatory and synaptic inhibitory activity patterns of medullary respiration‐related neurons during inspiratory (I) and expiratory (E) phases (E1 and E2 denote subdivisions of expiratory phase). Note that there is some uncertainty about whether early expiration‐related (ER) neurons are different from postinspiration inspiratory activity (PIIA)‐related early expiratory neurons or whether they are the same neurons obtained under different experimental conditions with prolonged and normal PIIA, respectively. Vertical hatching, pattern of excitatory synaptic discharge; horizontal hatching, pattern of active synaptic inhibition. Note that during inspiratory phase the late‐onset inspiration‐related (IR) neurons receive augmenting excitation but are kept silent by dominating inhibition. During the first part of the expiratory phase, inspiratory bulbospinal (BS) neurons receive some synaptic inhibition with the synaptic excitation giving rise to their PIIA. PB, propriobulbar; Böt. C, Bötzinger complex.

Data based on Richter and Ballantyne 427 and K. Budzińska, C. von Euler, T. Pantaleo, and Y. Yamamoto, unpublished observations
Figure 15. Figure 15.

Superimposed records of moving averages of vagal afferent (Vagal aff) activity mainly from pulmonary stretch‐receptor afferents and phrenic efferent (Phr eff) activity during inflation (1) and withholding inflation in inspiration (2). This illustrates the threshold character of the Hering‐Breuer inspiration‐terminating reflex. No sign of inhibition of inspiratory activity before the inspiratory off‐switch effect close to the peak of phrenic activity in the presence of inflation and afferent feedback of pulmonary stretch‐receptor activity. (From C. von Euler and T. Trippenbach, unpublished observations.)
Figure 16. Figure 16.

Moving averages of inspiratory phrenic activity in the absence of cyclic, vagal, volume‐related feedback. A: 6 records of inspiratory trajectories at different alveolar partial pressures of CO2 () show that the rate of rise of inspiratory activity increases with increasing . B: upper trace, computer average of 30 phrenic trajectories at a partial pressure of CO2 () of 46 mmHg; lower trace, corresponding standard deviations magnified 10 times. Note that broad and rounded peak of averaged phrenic trajectories does not correspond to any such shape in any of the individual traces but is due to variations in the inspiratory off‐switch events and thus in durations of the inspiratory ramps. These variations are reflected by high values of the standard deviations.

From Bruce et al. 79
Figure 17. Figure 17.

Initial rate of rise of inspiratory activity, i.e., “integrated” phrenic activity (Int Phr ampl), in cat under light pentobarbital anesthesia made apneustic by bilateral lesions of the inspiratory off‐switch promoting sites in medial parabrachial structures and bilateral vagotomy. Effects of changes in alveolar (A) and body temperature (B). Open circles and dashed lines, half times for “integrated” phrenic activity (in relative units) to reach its apneustic plateaus. Note that the half time stays almost constant in A but is markedly shortened with increased temperature (B). insp, Inspiration.

Adapted from Euler et al. 176
Figure 18. Figure 18.

Effects on respiratory activity of unilateral moderate focal cooling (20°C) in the region of the nucleus paragigantocellularis lateralis. Moving average of phrenic efferent activity contralaterally (Phr contra) and of abdominal muscle activity ipsilaterally (Abd ipsi). (From K. Budzińska, C. von Euler, T. Pantaleo, and Y. Yamamoto, unpublished observations.)
Figure 19. Figure 19.

Lung volume of dog under pentobarbital anesthesia after bilateral vagotomy during resting condition (R), breathing CO2‐enriched gas (C), and exercise while inhaling CO2‐enriched gas (C + X).

Adapted from Kao et al. 279
Figure 20. Figure 20.

Inspiratory trajectories of moving average of efferent phrenic activity with and without brief tetanic stimulation of the right vagus nerve. A: stimulus intensity 2 dB higher than threshold for the coarsest vagal afferents (coarsest pulmonary stretch‐receptor afferents) causes transient graded stage 1 inhibition of inspiratory activity, resulting in resetting of the trajectory. Note that peak amplitude of reset trajectory reaches roughly the same height as that of unstimulated one. B: stimulus intensity 6 dB higher than threshold for the coarsest pulmonary stretch‐receptor afferents elicits inspiration‐facilitating response that in turn causes complete inspiratory off‐switching. This is probably the result of combined action of transient coactivation of pulmonary stretch‐receptor afferents and reflex increase of central inspiratory activity input. Solid bar, time and duration of stimulus (St). (From E. N. Bruce, C. von Euler, and J. R. Romaniuk, unpublished observations.)
Figure 21. Figure 21.

Moving average of phrenic (Phr) and inspiration‐related inferior laryngeal nerve (Lar inf) activity in presence (1) and absence (2) of cyclic volume feedback from lungs.
Figure 22. Figure 22.

Curvilinear (approximately hyperbolic) time dependence of Hering‐Breuer inspiration‐inhibiting reflex in cat (A) and human (B). Volume levels (a‐d) at which off‐switch threshold is attained versus corresponding inspiratory durations (TI). A: in absence of vagal feedback (broken lines), e.g., after vagotomy, TI may be relatively constant (TI,vgt). If tidal volume (VT) is altered by changing chemical drive, TI,vgt may exhibit drive dependence, an index of some mismatch between drive influence on the rate of rise of inspiratory activity and on inspiratory off‐switch threshold (see Match or mismatch between drive dependence of inspiratory off‐switch threshold and rate of CIA augmentation, p. 35). With higher volumes, inspiration‐facilitating reflexes may be elicited, providing range 3 VT‐inspiration duration relationship. B: Hering‐Breuer reflex in humans not apparent at low and moderate VT levels (range 1) but at higher volumes (range 2) is similar to that in cat. C: scatter of TI and VT in cats under light pentobarbital anesthesia at 2 different steady states of alveolar CO2 concentrations (). Volume‐time courses were not recorded, only the break points at inspiratory off‐switch. Triangles: 43 breaths, = 5.4%, TI = 1.48 s ± 0.08 (SD), VT = 31.7 ml ± 1.3 (SD). Squares: 37 breaths, = 6.5%, TI = 1.13 s ± 0.04 (SD), VT = 46.4 ml ± 1.7 (SD). Note that scatter of TI is considerably greater in states of low than with higher chemical drive. This may be because inspiratory off‐switching is more susceptible to noise variations in conditions when its threshold is approached and attained at a relatively slow rate compared to higher rate of rise of excitatory input to off‐switch mechanisms at higher . This results from both increased augmentation rate of postulated central inspiratory activity input and increased contribution from pulmonary stretch receptors. [From Bradley et al. 66.]

Data from Clark and Euler 105
Figure 23. Figure 23.

Tidal volume (VT)‐inspiration duration (TI) and TI‐expiration duration (TE) relationships in adult male without (open circles, solid line) and with (filled circles, dashed line) vibration stimulus. Note that with vibration stimulus, Hering‐Breuer threshold curve is shifted downward and range 1 of VT‐TI relationship (left) is almost abolished. Expiration duration is almost unaffected by vibration. Change in the TI‐TE relationship (right) is almost solely due to change in TI.

Adapted from Homma 252
Figure 24. Figure 24.

A: time course of fall in thresholds of inspiratory off‐switch mechanism to stimulation at optimal site in medial parabrachial nucleus (ordinate) at different times during inspiratory phase (TI, abscissa) with (filled circles) and without (open circles) phasic vagal feedback. Difference between the 2 threshold curves (hatched area) is vagal contribution to excitability of inspiratory off‐switch mechanism; its time course is represented by thick line. Stimulus strength (Stim strength) in volts above lowest threshold obtained that was equal with and without vagal feedback (0.22 V). B: corresponding curves for “integrated” phrenic activity (thick lines) with (I) and without (II) phasic vagal feedback with amplitude scale (Phr ampl) in relative units at right. Superimposed is mirror image of all threshold points from A (increasing stimulus strength downward) showing similarity in time courses between “integrated” phrenic activity and off‐switch excitability in absence of phasic vagal feedback (open circles).

From Euler and Trippenbach 179
Figure 25. Figure 25.

“Integrated” phrenic activity (Phr ampl) in cat without phasic vagal feedback. Circles, excitability (thresholds) for inspiratory off‐switch mechanism to medial parabrachial nucleus stimulation at of 32 mmHg (A) and 53 mmHg (B). Scales of phrenic activity in relative units at right. Stimulus strength (Stim strength) with increasing values downward in volts above lowest threshold obtained that was equal at both levels (0.24 V). TI, inspiration duration.

From Euler and Trippenbach 179
Figure 26. Figure 26.

“Integrated” phrenic activity (Phr ampl) in cat without phasic vagal feedback at 2 different body temperatures. Thresholds plotted for inspiratory off‐switch mechanism to medial parabrachial nucleus stimulation at 36.1 °C (circles) and 40.2°C (squares). Scale of phrenic activity in relative units at right. Stimulus strength (Stim strength) with increasing values downward in volts above lowest threshold obtained (0.18 V at 40.2°C; 0.19 V at 36.1 °C).

From Euler and Trippenbach 179
Figure 27. Figure 27.

Tidal volume (VT)‐inspiration duration (TI) relationship (A, C, D) and expiration duration (TE)‐TI relationship (B). Transient effects in cat under light pentobarbital anesthesia showing typical hysteresis loop in response to step changes in inhaled CO2 concentration (A) and corresponding TE‐TI relationship (B). Crosses, response to rapid increase in from 3.8% (breathing air) to 8.0%; triangles, response back to breathing air with of 3.8%. Effects in decerebrate cat after bilateral vagotomy with no anesthesia (C) and after administration (15 mg/kg) of pentobarbital (D). Response shown to step increase (crosses) and decrease (squares) in inhaled CO2 concentration as changed from 3.5% to 6.2% and back to 3.4%. Note that slight prolongation of TI with increased in unanesthetized condition changed to shortening of TI after pentobarbital.

From Bradley et al. 65
Figure 28. Figure 28.

Projections of cat pulmonary stretch‐receptor (PSR) afferent in nucleus tractus solitarius (NTS) region as a result of microstimulation, and antidromic responses from single PSR afferent ganglion cell in nodose ganglion. Map represents extent of NTS in relation to view of medullary dorsal surface. Penetrations of microstimulation electrodes from which response contours of point (filled circles) or field (filled diamonds) type were produced or from which no antidromic responses were evoked (open circles) are shown and a likely course of the axon and its branches indicated. Main axon within tractus solitarius (TS) seems to branch both to lateral and medial subnuclei of NTS complex. Latencies of antidromic response from each site in milliseconds in parentheses. Note that latencies increase at terminal sites compared to stimulation of main axon. Scales give distances in millimeters rostral (R), caudal (C), and lateral to obex. N Comm, nucleus commisuralis; IV, 4th ventricle.

From Donoghue et al. 145
Figure 29. Figure 29.

Two hypotheses for functional organization of inspiratory off‐switch mechanism (I O‐S) of respiratory central pattern generator (CPG). Both diagrams include inputs to inspiratory off‐switch mechanism from pulmonary stretch receptors (PSR) and parabrachial‐Kölliker‐Fuse nuclear complex (NPB‐KF) in rostral pons. A: I O‐S receives its non‐PSR increase in excitability from recurrent feedback from central inspiratory activity (CIA) integrator itself, suggested by Bradley et al. 67 and Euler and Trippenbach 179. B: alternative and more complex hypothesis of separate inspiratory ramp (I ramp) integrator and timer for I O‐S mechanism, suggested by Younes et al. 529 and d'Angelo 130. Chemoreceptive inputs excite CIA integrator (and timing integrator) and inhibit I O‐S mechanism. A depicts possibility that PSR and CIA‐related inputs to I O‐S are mediated by Rβ neurons (Σ CIA, PSR). However, this hypothesis is not essential for the model; convergence of these 2 inputs could just as well take place in I O‐S itself (as shown in B). Pools probably have many other different inputs, both excitatory and inhibitory. Different pools do not represent any anatomically defined structures. I, inspiration‐inhibiting areas; E, expiration‐inhibiting areas of NPBM‐KF; IBS, inspiratory bulbospinal neuron; synch, synchronizing connections.
Figure 30. Figure 30.

Discharge patterns (cycle‐triggered histograms) and corresponding phrenic (Phr) activity in presence and absence of cyclic pulmonary stretch‐receptor feedback, i.e., during inflation (thin lines) and during withholding of inflation (thick lines). Discharge pattern of late‐onset inspiration‐related (putative off‐switch) neuron (A) is enhanced and that of early‐burst inspiration‐related neuron (B) is decreased by lung inflation. Richter 425 suggested that inhibition of late‐onset neurons during early part of inspiratory phase is mediated by early‐burst neurons. Time scale same for A and B.

Adapted from Cohen and Feldman 119
Figure 31. Figure 31.

Initial rising and early plateau parts of apneustic activity at different values in cat with bilateral parabrachial lesions (at sites where low‐intensity stimulation yielded pure inspiration‐inhibiting effects) and bilateral vagotomy. After levels had been constant for a while, apneusis was broken by a reflex elicited by pressing on lower part of chest. (From C. von Euler, I. Marttila, J. E. Remmers, and T. Trippenbach, unpublished observations.)
Figure 32. Figure 32.

Effects of changes in body temperature on duration of apneusis in “integrated” phrenic nerve activity. Values from cat with critical apneusis‐promoting lesions bilaterally in medial parabrachial nucleus, paralyzed and artificially ventilated with phrenic‐governed respirator that permits withholding lung inflations in the inspiratory phases. Note that gain of phrenic signal in F is half those of A‐E. Bars, absence of vagal volume feedback (servorespirator switched off). At right of each record is temperature, end‐tidal CO2 concentration, and in A and F, duration of 1st apneustic breath.

From Euler et al. 176
Figure 33. Figure 33.

Oscillatory apneustic activity, possibly reflecting negative‐feedback regulation of inspiratory activity around the inspiratory off‐switch threshold. Values from cat under light pentobarbital anesthesia, paralyzed and ventilated with phrenic (Phr)‐governed servorespirator. Apneustic activity caused by superficial unilateral cooling in dorsomedial part of medulla caudal to obex in region of nucleus gracilis, combined with withholding inflation (infl) during inspiratory phase by stopping respirator (as indicated by flow record). Insp, inspiration; Exp, expiration. (From K. Budzińska, C. von Euler, I. Homma, T. Pantaleo, and Y. Yamamoto, unpublished observations.)
Figure 34. Figure 34.

Schematic representation of volume (V), flow (V), and muscle pressure (Pmus) during inspiratory (Insp) and expiratory (Exp) phases in a normal spontaneous breath. E1 and E2 denote subdivisions of expiratory phase. Dashed lines, patterns that would occur if expiration were not broken by activity of inspiratory and laryngeal muscles.

Adapted from Mead and Agostoni 357
Figure 35. Figure 35.

A: inspiratory phrenic nerve activity. Records 1‐3 at 3 different time scales. B: efferent inspiratory phrenic activity (upper tracings in each pair) and corresponding expiratory internal intercostal nerve activity (lower tracings in each pair) at increasing levels from records 1 to 3.

From Richter 425
Figure 36. Figure 36.

Pattern of membrane potential (MP) and “integrated” efferent phrenic activity (‘Int’ Phr) of an inspiration‐related, augmenting propriobulbar neuron of thoracotomized cat under pentobarbital anesthesia. Intratracheal pressure (PTr) indicates pattern of artificial respiration. Membrane potential of this neuron shows progressively increasing excitation during inspiratory phase and abrupt inhibition that is strongest initially in the first part of the expiratory phase but lasts the whole expiratory phase.

Adapted from Richter and Ballantyne 427
Figure 37. Figure 37.

Pattern of membrane potential (MP) and “integrated” phrenic nerve activity (‘Int’ Phr) of an early expiration‐related, postinspiration inspiratory activity propriobulbar neuron of thoracotomized cat under pentobarbital anesthesia. Intratracheal pressure (PTr) indicates pattern of artificial respirator.

Adapted from Richter and Ballantyne 427
Figure 38. Figure 38.

Hypothetical variations in central inspiratory inhibition (CII) elicited by inflations (A‐C) and deflations (D‐F) during expiratory phase. A: inflation pulse (1) and small inflation step (2) applied during expiration. B, C: corresponding afferent pulse and step inputs integrated centrally to change CII and thereby expiratory duration (TE). D: subthreshold (3) and suprathreshold (4) deflation steps applied during expiration. E, F: resulting reductions in CII leading to shortening of TE. Response to subthreshold deflation gives graded decrease in TE seen in E, whereas suprathreshold deflation elicits almost immediate cessation of expiration and onset of new inspiration (F). As size and timing of volume maneuvers are varied, time course of the decay rate of CII changes and effect on TE is altered correspondingly. TEC, expiratory duration of control breaths.

Adapted from Knox 294
Figure 39. Figure 39.

Hypothetical changes in process (Φ) controlling expiration duration (TE), i.e., central inspiratory inhibition (CII), in response to rostral pontine stimuli that shorten TE (left) and prolong TE (right). The Φ, or CII, is considered to decay exponentially (time constant, 1.5 s) from its maximum value (1.0) at onset of expiratory phase. Control TE is 3.0 s, which with the time constant sets threshold value for onset of inspiration (ΦTHR) at 0.135. Left top, arrowed lines: pulse inputs that cause 0.250 reduction in Φ, followed by rebound increase of 0.125. Left bottom: shortening of TE produced by stimuli delivered at different times after onset of expiration (tE→ST). Right top, arrowed lines: pulse inputs that cause 0.250 increase in Φ. Right bottom: lengthening of TE produced by rostral pontine stimuli at different times. E, expiratory; I, inspiratory; TEC, expiratory duration of control breath; TEST, expiratory duration of stimulated breath.

From Cohen and Feldman 119
Figure 40. Figure 40.

Functional control of central inspiratory inhibition (CII) and expiratory duration emphasizing roles of magnocellular (FTM) and gigantocellular (FTG) tegmental fields. I O‐S, inspiratory off‐switch mechanisms; CIA, generator of control inspiratory activity; IBS, inspiratory bulbospinal premotor neurons; NPB‐KF, parabrachial‐Kölliker‐Fuse nuclear complex; open triangles, excitation; filled circles, inhibition. Note that CII‐related neurons are normally inhibited during inspiration and have peak discharge rate very early in expiration; thereafter discharge declines slowly. These characteristics correspond to those of early expiration‐related pro‐priobulbar neurons [185; see Fig. 14]. Diagram takes into account the possibility that I O‐S receives its pulmonary stretch‐receptor (PSR) input, combined with CIA‐related input, from Rβ neurons, whereas CII probably receives its PSR input from other nucleus tractus solitarius P‐cell interneurons (P). It cannot be excluded that effects of FTM and FTG lesions and stimulations are due to passing fibers coming from the lateral tegmental fields and projecting to respiratory interneurons. I, inspiratory phase; E, expiratory phase; Temp, temperature‐related inputs from anterior hypothalamus.

Adapted from Knox 295
Figure 41. Figure 41.

“Integrated” expiratory muscle activity of internal intercostal muscle (‘Int’ exp EMG) as function of expiratory duration (TE). During constant drive conditions, peak expiratory muscle activity increases with increasing TE. Changes in TE are produced by changes in lung volume. Inset: simultaneous records of “integrated” phrenic activity (‘Int’ Phr) and “integrated” internal intercostal muscle activity (‘Int’ IIC.) at 3 different TE values. (From A. F. DiMarco, C. von Euler, J. R. Romaniuk, and Y. Yamamoto, unpublished observations.)


Figure 1.

Pulse rate (upper trace) and respiration (lower trace) in human listening to dissonant atonal electronic music by Stockhausen (left) and melodic music by Chopin (right).

From Harrer 540


Figure 2.

Cyclic (A) and tonic (B) neuronal discharge patterns from different sites in medulla oblongata in neurally isolated and completely de‐nervated rhombencephalon in unanesthetized cat (delimited by intracollicular transection and transection at 1st cervical segment). A: 1, ventilation with 6.5% CO2 in O2; 2, ventilation with pure O2. B: 1, ventilation with 6.5% CO2 in O2; 2, ventilation with pure O2; 3, ventilation with 3% CO2 in O2; 4, ventilation with 15% CO2 in O2. Time, 20 cycles/s.

Adapted from Euler and Söderberg 177


Figure 3.

Effects of midsagittal section through rabbit medulla on respiratory motor outputs from left (A, B) and right (C, E) phrenic nerves. “Integrated” (A, C) and direct (B, E) records of efferent phrenic activity. D: reference line for end‐tidal CO2 trace in F; G: blood pressure. Note that different rhythms and patterns are obtained from the 2 sides. Bisection of medulla extended from 4 mm rostral to obex to 1 mm caudal to obex.

From Gromysz and Karczewski 222


Figure 4.

Discharge patterns of various respiration‐related neurons of the ventral respiratory group plotted for a single respiratory cycle. A‐D: late‐peak inspiration‐related neurons; E‐H: expiration‐related neurons; I‐K: early‐burst inspiration‐related cells. Bottom trace: chest circumference, inspiratory deflection upward.

From Merrill 362


Figure 5.

Medulla (and part of spinal cord) with the 2 main aggregates of respiration‐related neurons in medulla: longitudinal column constituting ventral respiratory group (VRG) with its 3 subdivisions (marked on right) and dorsal respiratory group (DRG). Diagram further shows the group of inspiration‐related relay neurons in 1st and 2nd segments of cervical spinal cord (C1‐C2 group of Aoki). Diagram shows locations of main groups of expiratory (circles) and inspiratory (triangles) bulbospinal and relay neurons (open symbols) and their descending axons projecting to spinal motoneurons (filled symbols). In nucleus ambiguus (NA), laryngeal motoneurons are indicated. For simplicity neurons and axons are only represented on 1 side. Böt. C, Bötzinger complex; NPA, nucleus para‐ambigualis; NRA, nucleus retroambigualis; NTS, nucleus tractus solitarius; X, 10th cranial nerve.



Figure 6.

Major aggregates (shaded areas) of respiration‐related neurons and their afferent (left) and efferent (right) connections, as revealed by anatomical and electrophysiological mapping techniques. A, B: medial parabrachial‐Kölliker‐Fuse complex; C, D: dorsal respiratory group; E, F: ventral respiratory group. Filled triangles, cell bodies; solid lines, axons and axon collaterals; Y‐shaped endings, axonal terminations. BC, brachium conjunctivum; Böt. C, Bötzinger complex; NPA, nucleus para‐ambigualis; NPBM, nucleus parabrachialis medialis; NRA, nucleus retroambigualis; NTS, nucleus tractus solitarius.

From Kalia 275. Reproduced with permission from Annu. Rev. Physiol, vol. 43. © 1981 by Annual Reviews, Inc


Figure 7.

Projections of different groups of medullary respiration‐related neurons. A: inspiratory bulbospinal neurons of nucleus para‐ambigualis (NPA) of the ventral respiratory group. B: early‐burst inspiration‐related neurons of NPA. (Main axonal branches probably cross midline at level rostral to obex, not as indicated here.) C: inspiratory bulbospinal neurons of nucleus tractus solitarius (NTS) of dorsal respiratory group. D: expiratory bulbospinal premotor neurons of nucleus retroambigualis (NRA) of ventral respiratory group, insp, Inspiratory; exp, expiratory. Large filled circles, cell bodies; small filled circles, axonal terminations.

Adapted from Merrill 364


Figure 8.

Locations of transverse lesions used to interrupt inputs to nucleus retroambigualis expiration‐related neurons in experiments described in text.

From Merrill 364


Figure 9.

Medullary projections of expiration‐related neurons of the Bötzinger complex (Böt). Projections to contralateral ventrolateral nucleus tractus solitarius (NST) and ipsilateral caudal nucleus retroambigualis (NRA) have been established with electrophysiological techniques. Projections to ipsilateral inspiratory (insp) nucleus para‐ambigualis regions appear likely. Projections to phrenic motoneuron pool have subsequently been established and reported to be inhibitory, exp, Expiratory.

From Merrill 365


Figure 10.

Inspiratory Rα neuron. Traces A and B (top to bottom): neuron discharge, phrenic neurogram, “integrated” phrenic activity, and intratracheal pressure. A: respirator driven by “integrated” phrenic activity and switched off during middle of 3 inspirations with no change in initial rate of increase of activity. Prolongation of inspiration due to lack of volume feedback. B: respirator driven by sine wave generator; no influence by inflations and deflations on discharge rate. Neuron could not be driven by electrical stimulation of vagus nerves. C: driven spike in response to single shocks to contralateral ventrolateral funiculus of cervical cord at the 4th cervical segment. Latency, 1.1‐1.4 ms at conduction distance of 42 mm; time, 2,000 cycles/s.

From Euler et al. 173


Figure 11.

Discharge patterns of 2 Rβ neurons in cat under pentobarbital anesthesia paralyzed and artificially ventilated by respirator governed by efferent phrenic activity. Trace A (top to bottom): instantaneous frequency record, neuron discharge, “integrated” phrenic activity, and intratracheal pressure. During first 2 inspiratory discharges, respirator was inflating lungs (with some time lag). During last inspiration, respirator was switched off so that neuron received central inspiratory activity input, giving a slower rate of increase of inspiratory activity, which reaches roughly the same value as in first 2 breaths, but after a longer time. Inspiration terminates when discharge rate reaches approximately the same level with or without volume feedback. Traces B and C (top to bottom): neuron discharge, efferent phrenic neurogram, intratracheal pressure (with some delay), and “integrated” phrenic activity. This Rβ neuron has somewhat higher threshold than that in A. B: respirator driven by “integrated” phrenic activity (after slight time lag). C: respirator driven by sine wave generator. Neuron discharge modulated by both inspiratory activity (central inspiratory activity input) and lung volume variations. Note that deflation coinciding with peak phrenic activity reduces neuron discharge and prolongs inspiratory phase. Neuron is responsive during postinspiration inspiratory activity.

Adapted from Euler et al. 173


Figure 12.

Representation of Rβ neurons and their function as a summarizer of central inspiratory activity (CIA) corollary activity and pulmonary stretch‐receptor (PSR) afferent activity. The CIA corollary activity is probably not mediated by the Rα inspiratory premotor neurons; Rα and Rβ neurons probably share a common CIA input. IBS, inspiratory bulbospinal neuron.



Figure 13.

Discharge patterns (cycle‐triggered histograms) of early expiration‐related neurons in response to 2 kinds of reflex modulations of expiratory duration (TE). A: withholding inflation in inspiration (I) causes lengthening of inspiratory duration and proportional prolongation of TE. B: inflation during expiratory phase elicits a TE‐prolonging reflex. TE(C), average control TE; TE (T), average test TE. Test inflation (ITP) indicated in inset; duration, 80 ms; averages of 8 cycles.

From Feldman and Cohen 185


Figure 14.

Excitatory and synaptic inhibitory activity patterns of medullary respiration‐related neurons during inspiratory (I) and expiratory (E) phases (E1 and E2 denote subdivisions of expiratory phase). Note that there is some uncertainty about whether early expiration‐related (ER) neurons are different from postinspiration inspiratory activity (PIIA)‐related early expiratory neurons or whether they are the same neurons obtained under different experimental conditions with prolonged and normal PIIA, respectively. Vertical hatching, pattern of excitatory synaptic discharge; horizontal hatching, pattern of active synaptic inhibition. Note that during inspiratory phase the late‐onset inspiration‐related (IR) neurons receive augmenting excitation but are kept silent by dominating inhibition. During the first part of the expiratory phase, inspiratory bulbospinal (BS) neurons receive some synaptic inhibition with the synaptic excitation giving rise to their PIIA. PB, propriobulbar; Böt. C, Bötzinger complex.

Data based on Richter and Ballantyne 427 and K. Budzińska, C. von Euler, T. Pantaleo, and Y. Yamamoto, unpublished observations


Figure 15.

Superimposed records of moving averages of vagal afferent (Vagal aff) activity mainly from pulmonary stretch‐receptor afferents and phrenic efferent (Phr eff) activity during inflation (1) and withholding inflation in inspiration (2). This illustrates the threshold character of the Hering‐Breuer inspiration‐terminating reflex. No sign of inhibition of inspiratory activity before the inspiratory off‐switch effect close to the peak of phrenic activity in the presence of inflation and afferent feedback of pulmonary stretch‐receptor activity. (From C. von Euler and T. Trippenbach, unpublished observations.)



Figure 16.

Moving averages of inspiratory phrenic activity in the absence of cyclic, vagal, volume‐related feedback. A: 6 records of inspiratory trajectories at different alveolar partial pressures of CO2 () show that the rate of rise of inspiratory activity increases with increasing . B: upper trace, computer average of 30 phrenic trajectories at a partial pressure of CO2 () of 46 mmHg; lower trace, corresponding standard deviations magnified 10 times. Note that broad and rounded peak of averaged phrenic trajectories does not correspond to any such shape in any of the individual traces but is due to variations in the inspiratory off‐switch events and thus in durations of the inspiratory ramps. These variations are reflected by high values of the standard deviations.

From Bruce et al. 79


Figure 17.

Initial rate of rise of inspiratory activity, i.e., “integrated” phrenic activity (Int Phr ampl), in cat under light pentobarbital anesthesia made apneustic by bilateral lesions of the inspiratory off‐switch promoting sites in medial parabrachial structures and bilateral vagotomy. Effects of changes in alveolar (A) and body temperature (B). Open circles and dashed lines, half times for “integrated” phrenic activity (in relative units) to reach its apneustic plateaus. Note that the half time stays almost constant in A but is markedly shortened with increased temperature (B). insp, Inspiration.

Adapted from Euler et al. 176


Figure 18.

Effects on respiratory activity of unilateral moderate focal cooling (20°C) in the region of the nucleus paragigantocellularis lateralis. Moving average of phrenic efferent activity contralaterally (Phr contra) and of abdominal muscle activity ipsilaterally (Abd ipsi). (From K. Budzińska, C. von Euler, T. Pantaleo, and Y. Yamamoto, unpublished observations.)



Figure 19.

Lung volume of dog under pentobarbital anesthesia after bilateral vagotomy during resting condition (R), breathing CO2‐enriched gas (C), and exercise while inhaling CO2‐enriched gas (C + X).

Adapted from Kao et al. 279


Figure 20.

Inspiratory trajectories of moving average of efferent phrenic activity with and without brief tetanic stimulation of the right vagus nerve. A: stimulus intensity 2 dB higher than threshold for the coarsest vagal afferents (coarsest pulmonary stretch‐receptor afferents) causes transient graded stage 1 inhibition of inspiratory activity, resulting in resetting of the trajectory. Note that peak amplitude of reset trajectory reaches roughly the same height as that of unstimulated one. B: stimulus intensity 6 dB higher than threshold for the coarsest pulmonary stretch‐receptor afferents elicits inspiration‐facilitating response that in turn causes complete inspiratory off‐switching. This is probably the result of combined action of transient coactivation of pulmonary stretch‐receptor afferents and reflex increase of central inspiratory activity input. Solid bar, time and duration of stimulus (St). (From E. N. Bruce, C. von Euler, and J. R. Romaniuk, unpublished observations.)



Figure 21.

Moving average of phrenic (Phr) and inspiration‐related inferior laryngeal nerve (Lar inf) activity in presence (1) and absence (2) of cyclic volume feedback from lungs.



Figure 22.

Curvilinear (approximately hyperbolic) time dependence of Hering‐Breuer inspiration‐inhibiting reflex in cat (A) and human (B). Volume levels (a‐d) at which off‐switch threshold is attained versus corresponding inspiratory durations (TI). A: in absence of vagal feedback (broken lines), e.g., after vagotomy, TI may be relatively constant (TI,vgt). If tidal volume (VT) is altered by changing chemical drive, TI,vgt may exhibit drive dependence, an index of some mismatch between drive influence on the rate of rise of inspiratory activity and on inspiratory off‐switch threshold (see Match or mismatch between drive dependence of inspiratory off‐switch threshold and rate of CIA augmentation, p. 35). With higher volumes, inspiration‐facilitating reflexes may be elicited, providing range 3 VT‐inspiration duration relationship. B: Hering‐Breuer reflex in humans not apparent at low and moderate VT levels (range 1) but at higher volumes (range 2) is similar to that in cat. C: scatter of TI and VT in cats under light pentobarbital anesthesia at 2 different steady states of alveolar CO2 concentrations (). Volume‐time courses were not recorded, only the break points at inspiratory off‐switch. Triangles: 43 breaths, = 5.4%, TI = 1.48 s ± 0.08 (SD), VT = 31.7 ml ± 1.3 (SD). Squares: 37 breaths, = 6.5%, TI = 1.13 s ± 0.04 (SD), VT = 46.4 ml ± 1.7 (SD). Note that scatter of TI is considerably greater in states of low than with higher chemical drive. This may be because inspiratory off‐switching is more susceptible to noise variations in conditions when its threshold is approached and attained at a relatively slow rate compared to higher rate of rise of excitatory input to off‐switch mechanisms at higher . This results from both increased augmentation rate of postulated central inspiratory activity input and increased contribution from pulmonary stretch receptors. [From Bradley et al. 66.]

Data from Clark and Euler 105


Figure 23.

Tidal volume (VT)‐inspiration duration (TI) and TI‐expiration duration (TE) relationships in adult male without (open circles, solid line) and with (filled circles, dashed line) vibration stimulus. Note that with vibration stimulus, Hering‐Breuer threshold curve is shifted downward and range 1 of VT‐TI relationship (left) is almost abolished. Expiration duration is almost unaffected by vibration. Change in the TI‐TE relationship (right) is almost solely due to change in TI.

Adapted from Homma 252


Figure 24.

A: time course of fall in thresholds of inspiratory off‐switch mechanism to stimulation at optimal site in medial parabrachial nucleus (ordinate) at different times during inspiratory phase (TI, abscissa) with (filled circles) and without (open circles) phasic vagal feedback. Difference between the 2 threshold curves (hatched area) is vagal contribution to excitability of inspiratory off‐switch mechanism; its time course is represented by thick line. Stimulus strength (Stim strength) in volts above lowest threshold obtained that was equal with and without vagal feedback (0.22 V). B: corresponding curves for “integrated” phrenic activity (thick lines) with (I) and without (II) phasic vagal feedback with amplitude scale (Phr ampl) in relative units at right. Superimposed is mirror image of all threshold points from A (increasing stimulus strength downward) showing similarity in time courses between “integrated” phrenic activity and off‐switch excitability in absence of phasic vagal feedback (open circles).

From Euler and Trippenbach 179


Figure 25.

“Integrated” phrenic activity (Phr ampl) in cat without phasic vagal feedback. Circles, excitability (thresholds) for inspiratory off‐switch mechanism to medial parabrachial nucleus stimulation at of 32 mmHg (A) and 53 mmHg (B). Scales of phrenic activity in relative units at right. Stimulus strength (Stim strength) with increasing values downward in volts above lowest threshold obtained that was equal at both levels (0.24 V). TI, inspiration duration.

From Euler and Trippenbach 179


Figure 26.

“Integrated” phrenic activity (Phr ampl) in cat without phasic vagal feedback at 2 different body temperatures. Thresholds plotted for inspiratory off‐switch mechanism to medial parabrachial nucleus stimulation at 36.1 °C (circles) and 40.2°C (squares). Scale of phrenic activity in relative units at right. Stimulus strength (Stim strength) with increasing values downward in volts above lowest threshold obtained (0.18 V at 40.2°C; 0.19 V at 36.1 °C).

From Euler and Trippenbach 179


Figure 27.

Tidal volume (VT)‐inspiration duration (TI) relationship (A, C, D) and expiration duration (TE)‐TI relationship (B). Transient effects in cat under light pentobarbital anesthesia showing typical hysteresis loop in response to step changes in inhaled CO2 concentration (A) and corresponding TE‐TI relationship (B). Crosses, response to rapid increase in from 3.8% (breathing air) to 8.0%; triangles, response back to breathing air with of 3.8%. Effects in decerebrate cat after bilateral vagotomy with no anesthesia (C) and after administration (15 mg/kg) of pentobarbital (D). Response shown to step increase (crosses) and decrease (squares) in inhaled CO2 concentration as changed from 3.5% to 6.2% and back to 3.4%. Note that slight prolongation of TI with increased in unanesthetized condition changed to shortening of TI after pentobarbital.

From Bradley et al. 65


Figure 28.

Projections of cat pulmonary stretch‐receptor (PSR) afferent in nucleus tractus solitarius (NTS) region as a result of microstimulation, and antidromic responses from single PSR afferent ganglion cell in nodose ganglion. Map represents extent of NTS in relation to view of medullary dorsal surface. Penetrations of microstimulation electrodes from which response contours of point (filled circles) or field (filled diamonds) type were produced or from which no antidromic responses were evoked (open circles) are shown and a likely course of the axon and its branches indicated. Main axon within tractus solitarius (TS) seems to branch both to lateral and medial subnuclei of NTS complex. Latencies of antidromic response from each site in milliseconds in parentheses. Note that latencies increase at terminal sites compared to stimulation of main axon. Scales give distances in millimeters rostral (R), caudal (C), and lateral to obex. N Comm, nucleus commisuralis; IV, 4th ventricle.

From Donoghue et al. 145


Figure 29.

Two hypotheses for functional organization of inspiratory off‐switch mechanism (I O‐S) of respiratory central pattern generator (CPG). Both diagrams include inputs to inspiratory off‐switch mechanism from pulmonary stretch receptors (PSR) and parabrachial‐Kölliker‐Fuse nuclear complex (NPB‐KF) in rostral pons. A: I O‐S receives its non‐PSR increase in excitability from recurrent feedback from central inspiratory activity (CIA) integrator itself, suggested by Bradley et al. 67 and Euler and Trippenbach 179. B: alternative and more complex hypothesis of separate inspiratory ramp (I ramp) integrator and timer for I O‐S mechanism, suggested by Younes et al. 529 and d'Angelo 130. Chemoreceptive inputs excite CIA integrator (and timing integrator) and inhibit I O‐S mechanism. A depicts possibility that PSR and CIA‐related inputs to I O‐S are mediated by Rβ neurons (Σ CIA, PSR). However, this hypothesis is not essential for the model; convergence of these 2 inputs could just as well take place in I O‐S itself (as shown in B). Pools probably have many other different inputs, both excitatory and inhibitory. Different pools do not represent any anatomically defined structures. I, inspiration‐inhibiting areas; E, expiration‐inhibiting areas of NPBM‐KF; IBS, inspiratory bulbospinal neuron; synch, synchronizing connections.



Figure 30.

Discharge patterns (cycle‐triggered histograms) and corresponding phrenic (Phr) activity in presence and absence of cyclic pulmonary stretch‐receptor feedback, i.e., during inflation (thin lines) and during withholding of inflation (thick lines). Discharge pattern of late‐onset inspiration‐related (putative off‐switch) neuron (A) is enhanced and that of early‐burst inspiration‐related neuron (B) is decreased by lung inflation. Richter 425 suggested that inhibition of late‐onset neurons during early part of inspiratory phase is mediated by early‐burst neurons. Time scale same for A and B.

Adapted from Cohen and Feldman 119


Figure 31.

Initial rising and early plateau parts of apneustic activity at different values in cat with bilateral parabrachial lesions (at sites where low‐intensity stimulation yielded pure inspiration‐inhibiting effects) and bilateral vagotomy. After levels had been constant for a while, apneusis was broken by a reflex elicited by pressing on lower part of chest. (From C. von Euler, I. Marttila, J. E. Remmers, and T. Trippenbach, unpublished observations.)



Figure 32.

Effects of changes in body temperature on duration of apneusis in “integrated” phrenic nerve activity. Values from cat with critical apneusis‐promoting lesions bilaterally in medial parabrachial nucleus, paralyzed and artificially ventilated with phrenic‐governed respirator that permits withholding lung inflations in the inspiratory phases. Note that gain of phrenic signal in F is half those of A‐E. Bars, absence of vagal volume feedback (servorespirator switched off). At right of each record is temperature, end‐tidal CO2 concentration, and in A and F, duration of 1st apneustic breath.

From Euler et al. 176


Figure 33.

Oscillatory apneustic activity, possibly reflecting negative‐feedback regulation of inspiratory activity around the inspiratory off‐switch threshold. Values from cat under light pentobarbital anesthesia, paralyzed and ventilated with phrenic (Phr)‐governed servorespirator. Apneustic activity caused by superficial unilateral cooling in dorsomedial part of medulla caudal to obex in region of nucleus gracilis, combined with withholding inflation (infl) during inspiratory phase by stopping respirator (as indicated by flow record). Insp, inspiration; Exp, expiration. (From K. Budzińska, C. von Euler, I. Homma, T. Pantaleo, and Y. Yamamoto, unpublished observations.)



Figure 34.

Schematic representation of volume (V), flow (V), and muscle pressure (Pmus) during inspiratory (Insp) and expiratory (Exp) phases in a normal spontaneous breath. E1 and E2 denote subdivisions of expiratory phase. Dashed lines, patterns that would occur if expiration were not broken by activity of inspiratory and laryngeal muscles.

Adapted from Mead and Agostoni 357


Figure 35.

A: inspiratory phrenic nerve activity. Records 1‐3 at 3 different time scales. B: efferent inspiratory phrenic activity (upper tracings in each pair) and corresponding expiratory internal intercostal nerve activity (lower tracings in each pair) at increasing levels from records 1 to 3.

From Richter 425


Figure 36.

Pattern of membrane potential (MP) and “integrated” efferent phrenic activity (‘Int’ Phr) of an inspiration‐related, augmenting propriobulbar neuron of thoracotomized cat under pentobarbital anesthesia. Intratracheal pressure (PTr) indicates pattern of artificial respiration. Membrane potential of this neuron shows progressively increasing excitation during inspiratory phase and abrupt inhibition that is strongest initially in the first part of the expiratory phase but lasts the whole expiratory phase.

Adapted from Richter and Ballantyne 427


Figure 37.

Pattern of membrane potential (MP) and “integrated” phrenic nerve activity (‘Int’ Phr) of an early expiration‐related, postinspiration inspiratory activity propriobulbar neuron of thoracotomized cat under pentobarbital anesthesia. Intratracheal pressure (PTr) indicates pattern of artificial respirator.

Adapted from Richter and Ballantyne 427


Figure 38.

Hypothetical variations in central inspiratory inhibition (CII) elicited by inflations (A‐C) and deflations (D‐F) during expiratory phase. A: inflation pulse (1) and small inflation step (2) applied during expiration. B, C: corresponding afferent pulse and step inputs integrated centrally to change CII and thereby expiratory duration (TE). D: subthreshold (3) and suprathreshold (4) deflation steps applied during expiration. E, F: resulting reductions in CII leading to shortening of TE. Response to subthreshold deflation gives graded decrease in TE seen in E, whereas suprathreshold deflation elicits almost immediate cessation of expiration and onset of new inspiration (F). As size and timing of volume maneuvers are varied, time course of the decay rate of CII changes and effect on TE is altered correspondingly. TEC, expiratory duration of control breaths.

Adapted from Knox 294


Figure 39.

Hypothetical changes in process (Φ) controlling expiration duration (TE), i.e., central inspiratory inhibition (CII), in response to rostral pontine stimuli that shorten TE (left) and prolong TE (right). The Φ, or CII, is considered to decay exponentially (time constant, 1.5 s) from its maximum value (1.0) at onset of expiratory phase. Control TE is 3.0 s, which with the time constant sets threshold value for onset of inspiration (ΦTHR) at 0.135. Left top, arrowed lines: pulse inputs that cause 0.250 reduction in Φ, followed by rebound increase of 0.125. Left bottom: shortening of TE produced by stimuli delivered at different times after onset of expiration (tE→ST). Right top, arrowed lines: pulse inputs that cause 0.250 increase in Φ. Right bottom: lengthening of TE produced by rostral pontine stimuli at different times. E, expiratory; I, inspiratory; TEC, expiratory duration of control breath; TEST, expiratory duration of stimulated breath.

From Cohen and Feldman 119


Figure 40.

Functional control of central inspiratory inhibition (CII) and expiratory duration emphasizing roles of magnocellular (FTM) and gigantocellular (FTG) tegmental fields. I O‐S, inspiratory off‐switch mechanisms; CIA, generator of control inspiratory activity; IBS, inspiratory bulbospinal premotor neurons; NPB‐KF, parabrachial‐Kölliker‐Fuse nuclear complex; open triangles, excitation; filled circles, inhibition. Note that CII‐related neurons are normally inhibited during inspiration and have peak discharge rate very early in expiration; thereafter discharge declines slowly. These characteristics correspond to those of early expiration‐related pro‐priobulbar neurons [185; see Fig. 14]. Diagram takes into account the possibility that I O‐S receives its pulmonary stretch‐receptor (PSR) input, combined with CIA‐related input, from Rβ neurons, whereas CII probably receives its PSR input from other nucleus tractus solitarius P‐cell interneurons (P). It cannot be excluded that effects of FTM and FTG lesions and stimulations are due to passing fibers coming from the lateral tegmental fields and projecting to respiratory interneurons. I, inspiratory phase; E, expiratory phase; Temp, temperature‐related inputs from anterior hypothalamus.

Adapted from Knox 295


Figure 41.

“Integrated” expiratory muscle activity of internal intercostal muscle (‘Int’ exp EMG) as function of expiratory duration (TE). During constant drive conditions, peak expiratory muscle activity increases with increasing TE. Changes in TE are produced by changes in lung volume. Inset: simultaneous records of “integrated” phrenic activity (‘Int’ Phr) and “integrated” internal intercostal muscle activity (‘Int’ IIC.) at 3 different TE values. (From A. F. DiMarco, C. von Euler, J. R. Romaniuk, and Y. Yamamoto, unpublished observations.)

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Article Title: Brain Stem Mechanisms for Generation and Control of Breathing Pattern
 

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Curt Von Euler. Brain Stem Mechanisms for Generation and Control of Breathing Pattern. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 1-67. First published in print 1986. doi: 10.1002/cphy.cp030201