Control of abdominal muscles
Introduction
Abdominal muscles contribute to ventilation when respiratory drive increases (e.g., exercise, diaphragmatic fatigue), are critical for protective reflexes such as coughing, sneezing, and vomiting, and, depending on one’s viewpoint, contribute to one of humanity’s best or worst attributes—speech. Despite their importance, however, much less is known about their control compared to that of the intercostal and phrenic motoneurons. We know virtually nothing about the inputs to their medullary premotor neurons and the organization, at the spinal level, of the connections between their afferents, interneurons, and motoneurons within and between segments and this is reflected in the limited attention they receive in most recent reviews (Feldman, 1986; Shannon, 1986; Duffin et al., 1995; Berger and Bellingham, 1995; Bianchi et al., 1995; Hilaire and Monteau (1997), including one related to birds (Gleeson and Molony, 1989). Four exceptions are those of Monteau and Hilaire (1991)and Hilaire and Monteau (1997), a recent, but brief (84 references) review by Bishop (1997), an update of an earlier one (Bishop, 1963) by her, and that by Leevers and Road (1995a)on reflex influences on muscles of the chest wall. In contrast, just four of 603 references by Bianchi et al. (1995)refer explicitly to abdominal muscles although another 54 are indirectly related, primarily because of results related to pre-motor neurons. In one review, only the locations of their motoneurons (Berger and Bellingham, 1995) are described; in another, only the drives to phrenic and intercostal, but not abdominal, motoneurons (Monteau and Hilaire, 1991). The neglect of abdominal motor control is typified by a recent review of respiratory rhythmogenesis; a schematic of the “main groups of respiratory neurons in mammalian brainstem and spinal cord” omits abdominal motoneurons (Duffin et al., 1995). Research on proprioceptive inputs from respiratory muscles emphasizes those from the diaphragm and intercostals (e.g. Duron et al., 1978; Duron, 1981; Jammes et al., 1983a; Jammes and Speck, 1995; Hussain and Roussos, 1995; Revelette and Davenport, 1995; Jammes, 1995). Shannon, who, with his colleagues, has done much of the work on abdominal afferents (Shannon, 1980; Shannon and Freeman, 1981; Shannon and Lindsey, 1983; Hernandez et al., 1989), devotes eleven pages to thoracic, but only one to abdominal, receptors in his review (Shannon, 1986). A recent review of the respiratory responses to loads concentrates on the diaphragm (Bazzy and Feldman, 1991).
Contraction of the abdominal muscles contributes to inspiration by lengthening the diaphragm (or reducing or preventing its shortening at increased lung volumes, whether caused by loads, changes in posture, or airway obstruction), thereby maintaining the diaphragm closer to its optimal length for tension generation (contractility). Abdominal tone also reduces the compliance of the abdominal compartment (Goldman et al., 1986a), enabling the region in contact with rib cage (the area of apposition) to act as a fulcrum for expansion of the lower rib cage during inspiration. These considerations account for the use of abdominal muscle binders in quadriplegics (e.g. Goldman et al., 1986b). Finally, by forcing lung volume below the passive end-expiratory position, the onset of the next inspiration is passive, resulting from the outward recoil of the respiratory system when abdominal muscles relax. Dogs (De Troyer et al., 1989) and horses (Koterba et al., 1988) use this breathing pattern at rest; man (Henke et al., 1988) and dogs (Ainsworth et al., 1989a), but not ponies (Gutting et al., 1991), use it during exercise. The net effect is to distribute the work of breathing between the two sets of muscles or, in the case of human subjects whose use of abdominal muscles at rest is minimal, to share it at higher ventilatory levels. All these points are made by many, if not most, researchers studying this aspect of respiratory function, are covered in a recent paper by Aliverti et al. (1997)and recent reviews describing the complexity of their action (De Troyer and Loring, 1986; Grassino and Goldman, 1986; De Troyer and Loring, 1995; De Troyer, 1997; Decramer, 1997), and are not presented in more detail here.
Abdominal activity, either measured directly from electromyographic (EMG) recordings or deduced from either the pressures (which are related to discharge rate and recruitment of abdominal motor units during voluntary increases in abdominal pressure; Sant’Ambrogio et al., 1967) or configuration of the abdomen (Grimby et al., 1976; see also Aliverti et al., 1997for references to related works), is present under conditions unrelated to such specific behaviors as coughing, sneezing, vomiting and straining, and vocalization. Patients with airway obstruction (or chronic obstructive pulmonary disease) typically have active abdominal muscles (Martin et al., 1980, Martin et al., 1983; Dodd et al., 1984; Lopata et al., 1985b; Vergeret et al., 1987; Ninane et al., 1992; Breslin, 1992), their use depending on the degree of obstruction (Martinez et al., 1990). In such patients, they are recruited during exercise (Dodd et al., 1984) or application of continuous positive airway pressure (CPAP) (Petrof et al., 1990) when their activity may offset the benefits (reduced dyspnea) resulting from CPAP. Activity is also present in patients with cystic fibrosis (Cerny et al., 1992), generalized muscle weakness of diverse origins (Grinman and Whitelaw, 1983; Passerini et al., 1985; Rimmer and Whitelaw, 1993), under conditions of impaired diaphragmatic function (including diaphragmatic fatigue) (Yan et al., 1993a, Yan et al., 1993b; Katagiri et al., 1994; Sliwinski et al., 1996), and after maximal voluntary ventilation (Kyroussis et al., 1996) and thoracic surgery (Simonneau et al., 1983; Duggan and Drummond, 1987, Duggan and Drummond, 1989; Couture et al., 1994; Clergue et al., 1995). Despite their clinical significance, isolated examples of which are provided in several recent reviews (Slack and Shucart, 1994; Brown, 1994; Teitelbaum and Borel, 1994; Carter and Noseworthy, 1994; Zulueta and Fanburg, 1994; Kaplan and Hollander, 1994; Lynn et al., 1994), these will not be discussed further because they provide little information about the underlying neurophysiological control mechanisms at the central or spinal level.
Some studies document remarkably little effect of their absence on ventilation, probably because other respiratory muscles, including the pectorals, compensate (Ainsworth et al., 1992a, Ainsworth et al., 1992b). For example, quadriplegics defend ventilation as well as control subjects against an expiratory load (O’Donnell et al., 1993). Subjects lacking abdominal muscles (prune belly syndrome) have only modest impairments of ventilatory performance and exercise capacity (∼80% of predicted) (Ewig et al., 1996). Anesthetized supine dogs with paralyzed abdominal muscles still can generate satisfactory tidal volumes (Vt) (Warner et al., 1991; Brichant et al., 1993; but see Schroeder et al., 1991; Farkas and Schroeder, 1993); sudden loss of expiratory muscle activity, perhaps because of subtle changes in posture, has no effect on Vt, inspiratory flow, or end-tidal CO2 in awake dogs (Saupe et al., 1992). In healthy men, blockade of intercostal nerves T6–12 with local anesthetic has little effect on peak expiratory flow and none at all on the ventilatory response to CO2 or exercise (Hecker et al., 1989), possibly because lumbar innervation (see below) was not blocked or because accessory expiratory muscles such as triangularis sternis (TS) were recruited. Nevertheless, the significance of the contribution of abdominal muscles is illustrated by the respiratory difficulties encountered by patients with spinal cord injuries (Slack and Shucart, 1994), degenerative diseases (Grinman and Whitelaw, 1983; Rimmer and Whitelaw, 1993; Teitelbaum and Borel, 1994; Carter and Noseworthy, 1994; Zulueta and Fanburg, 1994; Kaplan and Hollander, 1994; Lynn et al., 1994), or after upper abdominal surgery (see Ford et al., 1993for review). Physiotherapy of abdominal muscles improves exercise capacity and maximal expiratory pressure generation in patients with chronic obstructive pulmonary disease (Vergeret et al., 1987). Recently, magnetic stimulation has been used to activate abdominal muscles, the resulting pressures and flows being similar to those observed in natural cough (Kyroussis et al., 1997; Lin et al., 1998); such a procedure has an obvious application to individuals with disrupted control of expiratory motoneurons (e.g. spinal cord injury).
The three preceding paragraphs testify to the many conditions when abdominal muscles are used but, as indicated earlier, the control mechanisms operating under these conditions are unknown. In this review, I concentrate on the abdominal muscles and their innervation, the locations and characteristics of their motoneurons, the medullary pre-motor neurons (discharge patterns, projections, inputs), the responses of both premotor neurons and motoneurons to various inputs which affect their discharge patterns during eupnea, their responses to changes in lung volume and respiratory drive (hypercapnia and hypoxia), and their roles in such specific activities as straining and vocalization. Puckree et al. (1998)have recently described task-specificity of individual abdominal motor units in upright humans; units recruited during a respiratory manoeuvre (an increase in end-expiratory lung volume) are not recruited during a postural one (leg lift). Readers interested in details about their roles in postural control are directed to the literature on this topic (e.g. Carman et al., 1972; Grillner et al., 1978;de Sousa and Furlani, 1982; De Troyer, 1983; Thorstensson et al., 1985; Goldman et al., 1987; Oddsson and Thorstensson, 1987, Oddsson and Thorstensson, 1990; Cresswell et al., 1994; Hodges et al., 1997) and recent reviews of the role of the vestibular system in the control of expiratory premotor neurons (Shiba et al., 1996a) and respiratory muscles (e.g. Huang et al., 1991, Yates and Miller, 1997; Yates et al., 1993; Rossiter et al., 1996) by Yates and Miller (1996), Yates and Miller (1997). In addition, the reader is referred to recent brief reviews of such protective respiratory reflexes as cough and sneezing by Shannon et al., 1996, Shannon et al., 1997and an earlier and exhaustive review by Korpás and Tomori, 1979. Vomiting has been the subject of several recent reviews (Grélot and Miller, 1994, Grélot and Miller, 1997; Miller, 1995; Miller and Grélot, 1996).
Section snippets
Anatomy
The respiratory abdominal muscles comprise two outer (external oblique, EO, and rectus abdominis, RA) and two inner (internal oblique, IO, and transversus abdominis, TA) muscles. A generic description of their anatomical arrangements is provided by Monteau and Hilaire (1991)but the anatomy varies considerably between species (Rizk, 1980); in some species of bats, for example, the EO is poorly developed (Lancaster and Henson, 1995a). A complete description (architecture, fiber type, and
Background
Of recent reviews of respiratory control and rhythmogenesis (Euler, 1986; Feldman, 1986; Ezure, 1990; Monteau and Hilaire, 1991; Berger and Bellingham, 1995; Dick et al., 1995; Bianchi et al., 1995; Ramirez and Richter, 1996; Bianchi and Pásaro, 1997; Harper, 1997; Denavit-Saubié and Foutz, 1997; Rekling and Feldman, 1998), Long and Duffin (1986)provide the most detailed review of E neurons of the caudal ventral respiratory group (cVRG) and the reader is referred to it for most material more
Inputs to abdominal motoneurons
In the lumbar spinal cord, all motoneurons with respiratory-related discharges are abdominal motoneurons; in the mid- to lower thoracic cord, abdominal motoneurons co-exist with intercostal motoneurons, the discharges of which vary as a function of rostral-caudal location and laterality (Le Bars and Duron, 1984). Thus, to identify a motoneuron unambiguously, one has to antidromically activate the motoneuron from a branch of the nerve at its entrance to an identified muscle.
Limitations
Differences in experimental procedures and conditions limit our ability to compare and interpret the effects of various interventions on abdominal activities from different laboratories. These include: uncontrolled or unknown central respiratory drive(s), recording techniques, quantification and expression of EMG or neural activities, end-expiratory lung volume and posture (including segmental proprioceptive effects; Section 10), and status of the upper airway (intact or bypassed), blood
State
State refers to the level of arousal of the organism; it includes variations associated with attention, sleep state, and type and level of anesthesia, all of which affect interpretation of the responses of expiratory muscles. In assessing the effects of changes in state, one must determine if they are direct, i.e. due to altered synaptic inputs from CNS neurons whose activities change with alterations of state, or indirect, i.e. due to changes in feedback due to state-induced changes in other
Shifts in end-expiratory lung volume
Abdominal expiratory muscles are activated by increases in EELV whether evoked by inflation (Russell and Bishop, 1976) or various types of positive pressure breathing (CPAP, PPB, PEEP) or ETL (Bishop, 1964; Bishop, 1967; Bishop and Bachofen, 1972a; Urbscheit et al., 1973; Mortola and Sant’Ambrogio, 1973; Kelsen et al., 1977; Baker et al., 1979; Davies et al., 1980; Farber, 1982; Jammes et al., 1983a, Jammes et al., 1983b; DiMarco et al., 1984; Finkler and Iscoe, 1984; Farber, 1986; South et
Chemical drive
In this section, I review the control of abdominal motoneurons and muscles and E premotor neurons by central and peripheral chemoreceptors; literature which focuses on inspiratory (phrenic or diaphragmatic, occasionally intercostal) activity is therefore excluded. The roles of hypoxia and hypercapnia in respiratory control are detailed in recent reviews (Haddad and Rosen, 1991; Bisgard and Neubauer, 1995; Nattie, 1995).
Straining
Straining involves prolonged co-contraction of the abdominal (and often expiratory muscles of the rib cage) and the diaphragm against a closed glottis in order to increase abdominal pressure. This increased pressure causes, depending on the circumstances (contents of the gut, bladder, or uterus, and degree of contraction or relaxation of various sphincters), defecation, vomiting, micturition, or parturition. In contrast, transport of esophageal contents into the stomach requires an increased
Background
The presence of abdominal segmental reflexes is suggested by several findings. First, the abdominal response to PPB is abolished by dorsal rhizotomy (T8 to L3) in anesthetized cats (Bishop, 1964); second, after cervical spinal transection in anesthetized dogs, increases in EELV still elicit abdominal activity, albeit at lower levels and in phase with inspiratory muscles (Reinoso et al., 1996); and third, abdominal activity during vomiting persists even after transection of the spinal cord at T2
Conclusions
Our expectations of the properties and connections of expiratory premotor neurons and abdominal muscles are based in large measure on their behavior(s) under conditions which eliminate much if not most of what they do. Deep barbiturate anesthesia, decerebration less so, reduces respiratory neuronal discharge patterns to those essential for respiration; this facilitates our understanding of the processes underlying breathing but necessarily eliminates the non-respiratory functions in which they
Acknowledgements
This review is in honour of Morton I. Cohen, on the occasion of his 75th birthday. My research has been supported by the Medical Research Council of Canada, the Ontario Thoracic Society (both directly and through grants to Queen’s University), the Canadian Lung Association, and Queen’s University (the Advisory Research Committee, Botterell Foundation, and R.K. Start Memorial Fund). I thank Sheila Gordon and Jeremy Simpson for their assistance with production and/or modification of figures. Many
References (751)
- et al.
The effects of locomotion on respiratory muscle activity in the awake dog
Respir. Physiol.
(1989) - et al.
The effects of chemical versus locomotory stimuli on respiratory muscle activity in the awake dog
Respir. Physiol.
(1989) - et al.
Morphological and physiological properties of caudal medullary expiratory neurons of the cat
Brain Res.
(1987) - et al.
Locations of medullary neurons with non-phasic discharges excited by stimulation of central and/or peripheral chemoreceptors and by activation of nociceptors in cat
Brain Res.
(1988) - et al.
Possible locations of pH-dependent central chemoreceptors: Intramedullary regions with acidic shift of extracellular fluid pH during hypercapnia
Brain Res.
(1989) - et al.
The increased expiratory muscle use in upright dogs: role of cardiovascular receptors
Respir. Physiol.
(1987) - et al.
Behavior of expiratory neurons in response to mechanical and chemical loading
Respir. Physiol.
(1979) - et al.
Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat
Brain Res.
(1988) - et al.
Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: viscerotopic, somatotopic and functional organization
Progr. Brain Res.
(1991) - et al.
Electrical and mechanical output of the expiratory muscles in anesthetized dogs
Respir. Physiol.
(1991)
Dorsal respiratory group neurons in the medulla of cat: Spinal projections, responses to lung inflation and superior laryngeal nerve stimulation
Brain Res.
Distribution of carotid sinus nerve afferent fibers to solitary tract nuclei of the cat using transganglionic transport of horseradish peroxidase
Neurosci. Lett.
Respiratory neurons in the region of the rectrofacial nucleus: pontile, medullary, spinal and vagal projections
Neurosci. Lett.
Medullary axonal projections of respiratory neurons of pontile pneumotaxic center
Respir. Physiol.
Suppression of rhythmic discharges of medullary neurones in organotypic cultures of new-born rats by calcium antagonists
Neurosci. Lett.
Effects of electrical and chemical stimulation of the Bötzinger complex on respiratory activity in the cat
Brain Res.
Expiration-related neurons in the caudal ventral respiratory group of the cat: Influences of the activation of Bötzinger complex neurons
Brain Res.
Depressant effects on inspiratory and expiratory activity produced by chemical activation of Bötzinger complex neurons in the rabbit
Brain Res.
Role of the arterial chemoreceptors in controlling lung volume in the dog
Respir. Physiol.
The pattern of respiratory muscle recruitment during pursed-lip breathing
Chest
Respiratory dysfunction in Parkinson’s disease
Clin. Chest Med.
Afferent projections to the dorsal and ventral respiratory nuclei in the medulla oblongata of the cat studied by the horseradish peroxidase technique
Brain Res.
Excitation of neurones in a restricted portion of the midbrain periaqueductal grey elicits both behavioural and cardiovascular components of the defence reaction in the unanaesthetised decerebrate cat
Neurosci. Lett.
Anatomical evidence that hypertension associated with the defense reaction in the cat is mediated by a direct projection from a restricted portion of the midbrain periaqueductal grey to the subretrofacial nucleus of the medulla
Brain Res.
Somatic and autonomic integration in the midbrain of the unanesthetized decerebrate cat: A distinctive pattern evoked by excitation of neurones in the subtentorial portion of the midbrain periaqueductal grey
Brain Res.
Ventilatory dysfunction in multiple sclerosis
Clin. Chest Med.
Modification of medullary respiratory-related discharge patterns by behaviors and states of arousal
Brain Res.
The carotid sinus connections: A WGA-HRP study in the cat
Brain Res.
The role of the midbrain in courtship behavior of the female ring dove (Streptopelia risoria): evidence from radiofrequency lesion and hormone implant studies
Brain Res.
Differential respiratory activity of four abdominal muscles in humans
J. Appl. Physiol.
Inspiratory neuron activity in the ventrolateral medulla of the dog
J. Appl. Physiol.
Vagal contributions to respiratory muscle activity during eupnea in the awake dog
J. Appl. Physiol.
Vagal modulation of respiratory muscle activity in awake dogs during exercise and hypercapnia
J. Appl. Physiol.
Regulation of respiratory muscle activities during chemoreceptor stimulation in adult horses
Am. J. Vet. Res.
Human respiratory muscle actions and control during exercise
J. Appl. Physiol.
Hyperoxia and moderate hypoxia fail to affect inspiratory muscle fatigue in humans
J. Appl. Physiol.
Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones
J. Physiol. (London)
Inhibition of caudal medullary expiratory neurones by retrofacial inspiratory neurones in the cat
J. Physiol. (London)
Medullary activation of intercostal fusimotor and alpha motoneurones
J. Physiol. (London)
Respiratory responses to tracheobronchial stimulation during sleep and wakefulness in the adult cat
Sleep
Rapid and transient excitation of respiration mediated by central chemoreceptor
J. Appl. Physiol.
Transverse abdominis length changes during eupnea, hypercapnia, and airway occlusion
J. Appl. Physiol.
Effect of mechanical loading on expiratory and inspiratory muscle activity during NREM sleep
J. Appl. Physiol.
The effect of carbon dioxide on the tonic and the rhythmic discharges of expiratory bulbospinal neurons
J. Physiol. (London)
On the transmission of the stimulating effects of carbon dioxide to the muscles of respiration
J. Physiol. (London)
Expiratory bulbospinal neurons of dogs. I. Control of discharge patterns by pulmonary stretch receptors
Am. J. Physiol.
Interaction between chemoreceptor and stretch receptor inputs at medullary respiratory neurons
Am. J. Physiol.
Synaptic rhythm of caudal medullary expiratory neurones during stimulation of the hypothalamic defence area of the cat
J. Physiol. (London)
The non-uniform character of expiratory synaptic activity in expiratory bulbospinal neurones of the cat
J. Physiol. (London)
Control of breathing patterns and abdominal muscles during graded loads and tilt
J. Appl. Physiol.
Cited by (177)
Neuroanatomical frameworks for volitional control of breathing and orofacial behaviors
2024, Respiratory Physiology and NeurobiologyAcute intermittent hypoxia evokes ventilatory long-term facilitation and active expiration in unanesthetized rats
2021, Respiratory Physiology and Neurobiology