Activity of abdominal muscle motoneurons during hypercapnia

doi:10.1016/0034-5687(92)90049-3

Respiration Physiology

Volume 89, Issue 2, August 1992, Pages 179-194

Respiration Physiolo...

https://doi.org/10.1016/0034-5687(92)90049-3 Get rights and content

Abstract

Our purpose was to examine the influence of hypercapnia on the activity of motoneurons innervating the transversus abdominis and internal oblique abdominal muscles, and of integrated phrenic and abdominal motor nerve activities. Studies were done in nine adult cats that were decerebrated, vagotomized, thoracotomized, paralyzed and ventilated mechanically. Of 42 motoneurons examined, 24 showed strong respiratory modulation (RM neurons), with the discharge confined primarily to the central expiratory period. The remaining 18 motoneurons discharged tonically, and failed to show respiratory modulation even at increased levels of central respiratory drive. Hyperoxic hypercapnia augmented the activities of the phrenic and abdominal nerves and increased the early expiratory discharge frequency of the RM neurons. The hypercapnia-induced increase in firing frequency during early expiration was accompanied by a corresponding decline in late expiration, and a virtual abolition of the inspiratory activity in the few neurons that discharged in this phase under normocapnic conditions. Finally, hypercapnia induced an increase in the number of spikes generated during each expiratory period in about half of the RM neurons, whereas the remaining cells showed a decrease. Thus, the increased peak activity of the integrated whole abdominal nerve burst with hypercapnia was brought about by a shift in the temporal pattern of motoneuron firing, or by an increase in the number of spikes generated during the expiratory period. The steep rate of rise and the pronounced early expiratory peak observed in the integrated abdominal nerve burst during hypercapnia in this preparation are consistent with thw increase in motoneuron firing frequency during the early stages of the expiratory phase.

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Fig. 2A–C shows the discharge pattern of the abdominal muscle nerves in the decerebrate cat. There are augmenting (Fig. 2A middle and right panel), plateau (Fig. 2B), spindle (Fig. 2A left panel) and decrementing (Fig. 2C) patterns although the decrementing pattern seemed to occur more often (Figs. 4 and 10 in Fregosi et al., 1987; Figs. 1, 2 and 7 in Fregosi and Bartlett, 1988; Figs. 3 and 4 in Fregosi et al., 1992), with an augmenting pattern observed in only one figure (Fig. 1 in Fregosi et al., 1987). They have noted marked inter-animal variability in the shape of the abdominal ENG, and found that it often changed with time in a given cat, even under conditions of constant chemical drive (Fregosi et al., 1992).
The abdominal muscles form part of the expiratory pump in cooperation with the other expiratory muscles, primarily the internal intercostal and triangularis sterni muscles. The discharge of abdominal muscles is divided into four main patterns: augmenting, plateau, spindle and decrementing. The patterns tend to be species-specific and dependent on the state of the central nervous system. Recent studies suggest that the abdominal muscles are more active than classically thought, even under resting conditions. Expiratory bulbospinal neurons (EBSN) in the caudal ventral respiratory group are the final output pathway to abdominal motoneurons in the spinal cord. Electrophysiological and anatomical studies indicated the excitatory monosynaptic inputs from EBSN to the abdominal motoneurons, although inputs from the propriospinal neurons seemed to be necessary to produce useful motor outputs. Respiration-related sensory modulation of expiratory neurons by vagal afferents that monitor the rate of change of lung volume and the end-expiratory lung volume (EELV) play a crucial role in modulating the drive to the abdominal musculature. Studies using in vitro and in situ preparations of neonatal and juvenile rats show bi-phasic abdominal activity, characterized by bursting at the end of expiration, a silent period during the inspiratory period, and another burst that occurs abruptly after inspiratory termination. Since the abdominal muscles rarely show these post-inspiratory bursts in the adult rat, the organization of the expiratory output pathway must undergo significant development alterations.
Drive to the human respiratory muscles
2007, Respiratory Physiology and Neurobiology
The motor control of the respiratory muscles differs in some ways from that of the limb muscles. Effectively, the respiratory muscles are controlled by at least two descending pathways: from the medulla during normal quiet breathing and from the motor cortex during behavioural or voluntary breathing. Neurophysiological studies of single motor unit activity in human subjects during normal and voluntary breathing indicate that the neural drive is not uniform to all muscles. The distribution of neural drive depends on a principle of neuromechanical matching. Those motoneurones that innervate intercostal muscles with greater mechanical advantage are active earlier in the breath and to a greater extent. Inspiratory drive is also distributed differently across different inspiratory muscles, possibly also according to their mechanical effectiveness in developing airway negative pressure. Genioglossus, a muscle of the upper airway, receives various types of neural drive (inspiratory, expiratory and tonic) distributed differentially across the hypoglossal motoneurone pool. The integration of the different inputs results in the overall activity in the muscle to keep the upper airway patent throughout respiration. Integration of respiratory and non-respiratory postural drive can be demonstrated in respiratory muscles, and respiratory drive can even be observed in limb muscles under certain circumstances. Recordings of motor unit activity from the human diaphragm during voluntary respiratory tasks have shown that depending on the task there can be large changes in recruitment threshold and recruitment order of motor units. This suggests that descending drive across the phrenic motoneurone pool is not necessarily consistent. Understanding the integration and distribution of drive to respiratory muscles in automatic breathing and voluntary tasks may have implications for limb motor control.
Influence of hypercapnic acidosis and hypoxia on abdominal expiratory nerve activity in the rat
2007, Respiratory Physiology and Neurobiology
We studied the influence of hypercapnic acidosis and hypoxia on the neural drive to abdominal muscles in anesthetized and decerebrate rats; this information is unavailable despite widespread use of the rat as an experimental model in respiratory physiology and neurobiology. To minimize confounding influences from receptors in the lungs and chest wall, the animals were vagotomized, paralyzed and mechanically ventilated, and electrical activity was recorded from abdominal muscle nerves. In anesthetized and decerebrate rats, both stimuli evoked steady, low amplitude expiratory discharge that persisted throughout the expiratory phase (E-all activity), but was inhibited during inspiration. We also observed late expiratory, high-amplitude bursts (E2 activity) superimposed on this steady activity, but only at the highest levels of respiratory drive. Hypoxia enhanced abdominal motor activity transiently, whereas hypercapnic acidosis caused a sustained increase in activity. Thus, both hypercapnic acidosis and hypoxia activate abdominal muscle motoneurons in the absence of phasic afferent inputs.
Respiratory drive in hindlimb motoneurones of the anaesthetized female cat
2006, Brain Research Bulletin
Anatomical studies have shown a monosynaptic projection from nucleus retroambiguus (NRA) to semimembranosus (Sm) motor nucleus in female cats, which is stronger in oestrus. Expiratory bulbospinal neurones are the best documented functional cell type in the NRA. If these cells participate in this projection, an expiratory drive would be expected in Sm motoneurones and this drive would be expected to be stronger in oestrus. In anaesthetized, paralyzed, ovariohysterectomized female cats, artificially ventilated to produce a strong respiratory drive (as monitored by phrenic nerve discharges), intracellular recordings were made from Sm motoneurones and from motoneurones in the surrounding hindlimb motor nuclei that are outside the focus of the NRA projection. The animals comprised two groups: either treated for 7 days with oestradiol benzoate (oestrous) or untreated (non-oestrous).
Central respiratory drive potentials (CRDPs) were observed in most motoneurones of both groups, with amplitudes larger for the oestrous than for the non-oestrous group (1.58 ± 1.34 mV versus 0.89 ± 0.79 mV, mean ± S.D.). However, the CRDPs most often consisted of a maximum depolarization in early expiration, which declined in late expiration and into inspiration. This pattern is different from the incrementing firing pattern of most expiratory bulbospinal neurones. The CRDPs in Sm and semitendinosus motoneurones (located in the same motor column) were of similar size and frequency to CRDPs in motoneurones outside that column. The hypothesis that expiratory bulbospinal neurones are significantly involved in the projection was rejected. Alternative sources and possible functional roles for the CRDPs are discussed.
Commentary on eupneic breathing patterns and gasping
2003, Respiratory Physiology and Neurobiology
The term “eupneic activity pattern” is a trivial phenotypical description of a particular activity pattern in respiratory nerves as recorded under in vivo like experimental conditions. This term is, however, inadequate, because Eupnea describes a behavioral breathing performance that is trouble-free occurring without conscious effort. Obviously, the term “eupneic activity pattern” is meant to describe a neural activity that is normal and comparable with quiet breathing conditions. The various in vivo, in situ and in vitro preparations all generate their specific “normal” activity patterns, when the conditions are undisturbed. The commentary describes some of the numerous reasons why such normal activity patterns must be different in the various preparations without indicating their pathological operation. The conclusion is that special considerations are necessary for any extension of the in vitro and in situ findings into in vivo situations, because the capacity of the respiratory network is greatly reduced and thus not comparable with conditions leading to “eupneic breathing” in the fully intact animal.
Modulation of expiratory motor output evoked by chemical activation of pre-Bötzinger complex in vivo
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We have previously demonstrated that chemical stimulation of the pre-Bötzinger complex (pre-BötC) in the anesthetized cat produces either phasic or tonic excitation of phrenic nerve discharge. This region is characterized by a mixture of inspiratory-modulated, expiratory-modulated, and phase-spanning (including pre-inspiratory (pre-I)) neurons; however, its influence on expiratory motor output is unknown. We, therefore, examined the effects of chemical stimulation of the pre-BötC on expiratory motor output recorded from the caudal iliohypogastric (lumbar, L₂) nerve. We found that unilateral microinjection of DL-homocysteic acid (DLH; 10 mM; 10–20 nl) into 16 sites in the pre-BötC enhanced lumbar nerve discharge, including changes in timing and patterning similar to those previously reported for phrenic motor output. Both increased peak amplitude and frequency of phasic lumbar bursts as well as tonic excitation of lumbar motor activity were observed. In some cases, evoked phasic lumbar nerve activity was synchronized in phase with phrenic nerve discharge. These findings demonstrate that chemical stimulation of the pre-BötC not only excites inspiratory motor activity but also excites expiratory motor output, suggesting a role for the pre-BötC in generation and modulation of inspiratory and expiratory rhythm and pattern.

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Activity of abdominal muscle motoneurons during hypercapnia

Abstract

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

Respir. Physiol.

J. Pharmacol. Methods

Respir. Physiol.

Reflex control of abdominal muscles during positive-pressure breathing

J. Appl. Physiol.

Vagal control of ventilation and expiratory muscles during elevated pressure in the cat

J. Appl. Physiol.

The respiratory muscles: mechanics and neural control

The activity respiratory muscles in upright and recumbent man

J. Appl. Physiol.

Multiple regression and the analysis of variance and covariance

Brain stem mechanism for regeneration and control of breathing pattern

Hypoxia inhibits abdominal expiratory nerve activity

J. Appl. Physiol.

Central inspiratory influence on abdominal expiratory nerve activity

J. Appl. Physiol.

Internal intercostal nerve discharges in the cat: influence of chemical stimuli

J. Appl. Physiol.