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Coordination of Breathing with Nonrespiratory Activities

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Abstract

Many articles in this section of Comprehensive Physiology are concerned with the development and function of a central pattern generator (CPG) for the control of breathing in vertebrate animals. The action of the respiratory CPG is extensively modified by cortical and other descending influences as well as by feedback from peripheral sensory systems. The central nervous system also incorporates other CPGs, which orchestrate a wide variety of discrete and repetitive, voluntary and involuntary movements. The coordination of breathing with these other activities requires interaction and coordination between the respiratory CPG and those governing the nonrespiratory activities. Most of these interactions are complex and poorly understood. They seem to involve both conventional synaptic crosstalk between groups of neurons and fluid identity of neurons as belonging to one CPG or another: neurons that normally participate in breathing may be temporarily borrowed or hijacked by a competing or interrupting activity. This review explores the control of breathing as it is influenced by many activities that are generally considered to be nonrespiratory. The mechanistic detail varies greatly among topics, reflecting the wide variety of pertinent experiments. © 2012 American Physiological Society. Compr Physiol 2:1387‐1415, 2012.

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Figure 1. Figure 1.

Electromyographic activities of laryngeal and respiratory muscles during quiet respiration and periaqueductal gray (PAG) stimulation in a spontaneously breathing, decerebrate cat. TA, thyroarytenoid muscle; PCA, posterior cricoarytenoid muscle; DIA, diaphragm; EA, external oblique abdominal muscle. Adapted, with permission, from Nonaka et al. 205.

Figure 2. Figure 2.

Block diagram emphasizing the complexity of information processing involved in playing a wind instrument. Dashed lines indicate likely feedback loops. Adapted, with permission, from Bouhuys 33.

Figure 3. Figure 3.

Schematic view of the head of a sperm whale showing an acoustic recording “tag” attached by a suction cup for studies during free dives up to 650 meters. B, brain; Bl, blowhole; Di, distal air sac; Fr, frontal air sac; Ju, junk; Ln, left naris; Ma, mandible; Mo, monkey lips; MT, muscle/tendon layer; Ro, rostrum; Rn, right naris; So, spermaceti organ; T, tag. Arrows indicate the sound path of clicks produced by the monkey lips. For further explanation, see text. Adapted, with permission, from Madsen et al. 170.

Figure 4. Figure 4.

Integrated phrenic nerve activity, tracheal pressure and intravesical pressure (IVP) in a decerebrate, paralyzed, vagally intact cat, ventilated by a servo‐respirator in accordance with phrenic activity during isovolumetric spontaneous bladder contractions. As positive end‐expiratory pressure (PEEP) was increased from 2.5 to 10.0 cmH2O, phrenic activity became progressively more periodic in both amplitude and frequency. Adapted, with permission, from Gdovin et al. 98.

Figure 5. Figure 5.

Integrated phrenic and hypoglossal nerve activities, tracheal pressure and intravesical pressure (IVP) in a decerebrate cat with intact vagi, ventilated by a servo‐respirator as in Figure 4. Note that as lung inflation was withheld prior to the second spontaneous, isovolumetric bladder contraction (SBC), both phrenic and hypoglossal nerve activities per breath increased. The same noninflation maneuver during the third SBC evoked a smaller phrenic response, no hypoglossal response and a reduction in respiratory frequency. Adapted, with permission, from Gdovin et al. 98.

Figure 6. Figure 6.

Intrauterine pressure and uterine elecromyogram (EMG) records of two unanesthetized rats during natural labor. (A) Records of a rat with bilateral pelvic nerve section, showing uterine contractions, but no reflex “pushing.” (B) Records of a sham‐operated rat with intact pelvic nerves, showing brief pushing events that sum with uterine contractions to increase intrauterine pressure. Adapted, with permission, from Mackay et al. 168.

Figure 7. Figure 7.

Thoracic and abdominal pressure swings, measured via indwelling vena cava catheters, and diaphragm elecromyogram (EMG) bursts accompanying 14 retches followed by a single expulsive event in a decerebrate cat induced to vomit by intramuscular injection of Veriloid, a mixture of veratrum alkaloids. Adapted, with permission, from McCarthy et al. 181.

Figure 8. Figure 8.

Raw data (upper panels) and power spectra (lower panels) for three 10‐s periods of stereotyped arm movement by a standing human subject. Breathing was stimulated by progressive hypercapnia, induced by a large dead space. During the first period (left), all variables showed periodicity at the frequency of the arm movements. However, with progressive hypercapnia (middle and right) neither rib cage movement nor diaphragm elecromyogram (EMG) showed a peak in the power spectrum at the frequency of arm movements. Flexor EMG, deltoid EMG; TrA, transversus abdominis; ES, erector spinae. Adapted, with permission, from Hodges et al. 132.

Figure 9. Figure 9.

Integrated genioglossus elecromyogram (EMG) and tracheal pressure as influenced by opening and closing a tracheostomy and spontaneous change in head position in an unanesthetized, freely moving cat. Note that the muscle activity is influenced both by head position and by the state of the tracheostomy. Adapted, with permission, from Bonora et al. 31.

Figure 10. Figure 10.

Study of a seated human subject. Elecromyogram (EMG) of the right parasternal intercostal muscle in the second interspace was recorded, along with airflow and forward force of the left and right shoulders. After three breaths in a neutral posture, the subject was asked to hold his breath at end expiration, turn to the right (ipsilateral rotation) or left (contralateral rotation) while apneic, and then resume quiet breathing while rotated. The parasternal intercostal muscle was phasically active during inspiration, confirming that it is an inspiratory muscle. Rotation to the right (shaded area in A) tonically activated the EMG and increased phasic inspiratory EMG activity during rotated breaths. Rotation to the left (shaded area in B) induced no activity in the muscle, and phasic inspiratory activity in the rotated position was reduced. The interplay between respiratory and postural requirements suggests an integration at the spinal level. Adapted, with permission, from Hudson et al. 137.



Figure 1.

Electromyographic activities of laryngeal and respiratory muscles during quiet respiration and periaqueductal gray (PAG) stimulation in a spontaneously breathing, decerebrate cat. TA, thyroarytenoid muscle; PCA, posterior cricoarytenoid muscle; DIA, diaphragm; EA, external oblique abdominal muscle. Adapted, with permission, from Nonaka et al. 205.



Figure 2.

Block diagram emphasizing the complexity of information processing involved in playing a wind instrument. Dashed lines indicate likely feedback loops. Adapted, with permission, from Bouhuys 33.



Figure 3.

Schematic view of the head of a sperm whale showing an acoustic recording “tag” attached by a suction cup for studies during free dives up to 650 meters. B, brain; Bl, blowhole; Di, distal air sac; Fr, frontal air sac; Ju, junk; Ln, left naris; Ma, mandible; Mo, monkey lips; MT, muscle/tendon layer; Ro, rostrum; Rn, right naris; So, spermaceti organ; T, tag. Arrows indicate the sound path of clicks produced by the monkey lips. For further explanation, see text. Adapted, with permission, from Madsen et al. 170.



Figure 4.

Integrated phrenic nerve activity, tracheal pressure and intravesical pressure (IVP) in a decerebrate, paralyzed, vagally intact cat, ventilated by a servo‐respirator in accordance with phrenic activity during isovolumetric spontaneous bladder contractions. As positive end‐expiratory pressure (PEEP) was increased from 2.5 to 10.0 cmH2O, phrenic activity became progressively more periodic in both amplitude and frequency. Adapted, with permission, from Gdovin et al. 98.



Figure 5.

Integrated phrenic and hypoglossal nerve activities, tracheal pressure and intravesical pressure (IVP) in a decerebrate cat with intact vagi, ventilated by a servo‐respirator as in Figure 4. Note that as lung inflation was withheld prior to the second spontaneous, isovolumetric bladder contraction (SBC), both phrenic and hypoglossal nerve activities per breath increased. The same noninflation maneuver during the third SBC evoked a smaller phrenic response, no hypoglossal response and a reduction in respiratory frequency. Adapted, with permission, from Gdovin et al. 98.



Figure 6.

Intrauterine pressure and uterine elecromyogram (EMG) records of two unanesthetized rats during natural labor. (A) Records of a rat with bilateral pelvic nerve section, showing uterine contractions, but no reflex “pushing.” (B) Records of a sham‐operated rat with intact pelvic nerves, showing brief pushing events that sum with uterine contractions to increase intrauterine pressure. Adapted, with permission, from Mackay et al. 168.



Figure 7.

Thoracic and abdominal pressure swings, measured via indwelling vena cava catheters, and diaphragm elecromyogram (EMG) bursts accompanying 14 retches followed by a single expulsive event in a decerebrate cat induced to vomit by intramuscular injection of Veriloid, a mixture of veratrum alkaloids. Adapted, with permission, from McCarthy et al. 181.



Figure 8.

Raw data (upper panels) and power spectra (lower panels) for three 10‐s periods of stereotyped arm movement by a standing human subject. Breathing was stimulated by progressive hypercapnia, induced by a large dead space. During the first period (left), all variables showed periodicity at the frequency of the arm movements. However, with progressive hypercapnia (middle and right) neither rib cage movement nor diaphragm elecromyogram (EMG) showed a peak in the power spectrum at the frequency of arm movements. Flexor EMG, deltoid EMG; TrA, transversus abdominis; ES, erector spinae. Adapted, with permission, from Hodges et al. 132.



Figure 9.

Integrated genioglossus elecromyogram (EMG) and tracheal pressure as influenced by opening and closing a tracheostomy and spontaneous change in head position in an unanesthetized, freely moving cat. Note that the muscle activity is influenced both by head position and by the state of the tracheostomy. Adapted, with permission, from Bonora et al. 31.



Figure 10.

Study of a seated human subject. Elecromyogram (EMG) of the right parasternal intercostal muscle in the second interspace was recorded, along with airflow and forward force of the left and right shoulders. After three breaths in a neutral posture, the subject was asked to hold his breath at end expiration, turn to the right (ipsilateral rotation) or left (contralateral rotation) while apneic, and then resume quiet breathing while rotated. The parasternal intercostal muscle was phasically active during inspiration, confirming that it is an inspiratory muscle. Rotation to the right (shaded area in A) tonically activated the EMG and increased phasic inspiratory EMG activity during rotated breaths. Rotation to the left (shaded area in B) induced no activity in the muscle, and phasic inspiratory activity in the rotated position was reduced. The interplay between respiratory and postural requirements suggests an integration at the spinal level. Adapted, with permission, from Hudson et al. 137.

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Donald Bartlett, James C. Leiter. Coordination of Breathing with Nonrespiratory Activities. Compr Physiol 2012, 2: 1387-1415. doi: 10.1002/cphy.c110004