The Diaphragm: Two Physiological Muscles in One Mark Pickering and James F

JOA_095.fm Page 305 Thursday, October 3, 2002 2:24 PM J. Anat. (2002) 201, pp305–312 REVIEWBlackwell Science, Ltd The diaphragm: two physiological muscles in one Mark Pickering and James F. X. Jones Department of Human Anatomy and Physiology, University College Dublin, Earlsfort Terrace, Dublin 2, Ireland Abstract To the respiratory physiologist or anatomist the diaphragm muscle is of course the prime mover of tidal air. However, gastrointestinal physiologists are becoming increasingly aware of the value of this muscle in helping to stop gastric contents from refluxing into the oesophagus. The diaphragm should be viewed as two distinct muscles, crural and costal, which act in synchrony throughout respiration. However, the activities of these two muscular regions can diverge during certain events such as swallowing and emesis. In addition, transient crural muscle relaxa- tions herald the onset of spontaneous acid reflux episodes. Studying the motor control of this muscular barrier may help elucidate the mechanism of these episodes. In the rat, the phrenic nerve divides into three branches before entering the diaphragm, and it is possible to sample single neuronal activity from the crural and costal branches. This review will discuss our recent findings with regard to the type of motor axons running in the phrenic nerve of the rat. In addition, we will outline our ongoing search for homologous structures in basal vertebrate groups. In particular, the pipid frogs (e.g. the African clawed frog, Xenopus laevis) possess a muscular band around the oesophagus that appears to be homologous to the mammalian crural diaphragm. This structure does not appear to interact directly with the respiratory apparatus, and could suggest a role for this region of the diaphragm, which was not originally respiratory. Key words crural diaphragm; phrenic nerve; Xenopus. the mesentery of the oesophagus (Langman, 1969). For The two muscles of the diaphragm and reasons outlined later in connection with phylogeny, diaphragmatic development it is of interest to ascertain whether crural myoblasts The mammalian diaphragm has traditionally been are of oesophageal or body wall origin. studied as a respiratory muscle. However, there is mounting evidence that suggests that it should more Motor innervation of the diaphragm correctly be characterized as two separate muscles, the crural diaphragm and the costal diaphragm (De Troyer The diaphragm receives its motor innervation via the et al. 1981; Mittal, 1993). During human development phrenic nerve, with separate branches innervating the of the costal diaphragm, myoblasts originating in the crural and costal regions (Gordon & Richmond, 1990). body wall, probably derived from the third, fourth and An older notion of an extra-phrenic motor innerva- fifth cervical segments, invade two pleuroperitoneal tion has almost disappeared from the literature membranes. The primordial target for phrenic nerve (Sant’Ambrogio et al. 1963). The literature on the outgrowth appears to these pleuroperitoneal folds topography of phrenic innervation is concerned with and not as originally thought the septum transversum three areas: spinal cord organization, nerve root origins (Greer et al. 1999). In contrast, the crura develop in and the projection pattern of phrenic nerve branches. If we consider the diaphragm to be composed of two muscles, the question arises as to whether the phrenic Correspondence nerve represents the fusion of two different nerves. Dr James F. X. Jones, Department of Human Anatomy and Physiology, University College Dublin, Earlsfort Terrace, Dublin 2, Ireland. Tel. Also it is relevant to establish whether there is a distinct 003531 7167423; fax: 003531 7167417; e-mail: [email protected] crural motor nucleus in the spinal cord. Originally, the Accepted for publication 30 July 2002 innervation of the costal and crural diaphragm was © Anatomical Society of Great Britain and Ireland 2002 JOA_095.fm Page 306 Thursday, October 3, 2002 2:24 PM 306 Physiology of the diaphragm, M. Pickering and J. F. X. Jones indeed thought to be segmental. In the dog, the C5 root spindles were located within the crural diaphragm. On has been reported to innervate almost exclusively the other hand, Balkowiec et al. (1995) recorded 13 spindle the costal diaphragm, whilst the C7 root innervates afferents from a single cat phrenic nerve, suggesting a the crural diaphragm (De Troyer et al. 1982). In the cat, spindle density more typical of skeletal muscle (although, Sant’Ambrogio et al. (1963) showed that electrical again, their distribution was predominantly, but not activity of a hemi-diaphragm requires intact C4−6 root- exclusively, crural). However, as the projections of the lets with the vertebral (or crural) region mainly receiv- spindle afferents are unknown, the absolute number ing its innervation from C6 and the costal region from of spindles may not be relevant; a small number of C5. However, later more refined topographical map- afferents may still be capable of exerting an influence ping studies in the cat showed that there was no such on the activity of a large number of motoneurones. simple segmental organization, but that generally the The dramatic findings by Balkowiec et al. (1995) led ventral region of both muscles was innervated by Jammes et al. (2000) to revisit the question of dia- the C5 neurones, and the dorsal portions of both were phragmatic proprioception. In contrast, they found innervated by the C6 neurones (Fournier & Sieck, 1988). that high-frequency diaphragm mechano-stimulation The use of an elegant technique involving electrically had no effect on the activity of the crural or costal evoked glycogen depletion greatly increased the segments whilst the remote intercostal muscles showed resolution of cervical root and phrenic nerve branch a clear increase of activity. Unfortunately, this study was innervation territories (Hammond et al. 1989). Advances performed in a different species (the rabbit) compared have been forthcoming not only in the study of peri- to the study of Balkowiec et al. (1995). What is clear pheral projection of phrenic nerve roots and branches from the history of diaphragmatic proprioception is but also in the analysis of the central origin of crural that all the studies have been undertaken by respir- and costal motoneurones in the spinal cord (Gordon atory physiologists, who are, by default, obsessed with & Richmond, 1990). When three different tracers were respiration. If we consider that the crural diaphragm is applied to cat phrenic nerve branches, retrogradely not a respiratory muscle but a gastrointestinal sphincter labelled motoneurones were found to be quite mixed then the adequate stimulus for crural mechanorecep- throughout the full extent of the phrenic motor tors may be oesophageal distension at the hiatus not nucleus. Therefore, whilst there is a highly delineated vibration of the central tendon; and a more meaningful strip-like peripheral projection to muscle fibres, the output to study may be the manometric profile of motoneurones in the spinal cord are relatively inter- sphincter pressure. mingled rostrocaudally, dorsoventrally and mediolater- The uncertainty as to the role of phrenic afferents is ally (Gordon & Richmond, 1990). Although there are no not helped by the fact that there is evidence that some simple, obvious differences between the anatomical of the afferents are not of diaphragmatic origin. arrangement of the crural and costal motor innerva- Kostreva & Pontus (1993a,b) have shown, in the dog, tion at the spinal cord or root level, recordings of single that the phrenic nerve contains afferents from the motor fibres may yet reveal fundamental differences in pericardium, liver and vena cava. Liver afferents in the their motor control. phrenic nerve were also suggested by Alexander (1940) in the cat. These must be taken into account in any study of phrenic nerve mechanoreceptor afferents. Sensory innervation of the diaphragm The afferent feedback from the diaphragm may give Oesophageal distension and crural diaphragm some clues as to the function of the crural and costal relaxation muscles. Traditionally, diaphragmatic proprioception has been thought to have little or no role in the regu- In order for a food bolus to pass easily into the stom- lation of breathing (Corda et al. 1965). Histological ach, the crural diaphragm briefly ceases to contract studies of muscle spindles in the cat by Duron et al. with the rest of the diaphragm during inspiration, thus (1978) showed a rather sparse distribution of muscle allowing bolus transit across the diaphragm. Dramatic spindles in the cat diaphragm in comparison with other divergence of the activity of the crural and costal skeletal muscles, with a mere 10 spindles identified diaphragm is seen during swallowing and oesophageal in the entire diaphragm. Perhaps significantly, all 10 distension. This selective crural inhibition evoked by © Anatomical Society of Great Britain and Ireland 2002 JOA_095.fm Page 307 Thursday, October 3, 2002 2:24 PM Physiology of the diaphragm, M. Pickering and J. F. X. Jones 307 balloon distension of the oesophagus has been re- skeletal neuromuscular junction (Wang et al. 1995). ported by many researchers (Cherniack et al. 1984; Could nitrergic enteric neurones from the oesophagus Altschuler et al. 1985; Oliven et al. 1989; Oyer et al. 1989a; be innervating and inhibiting the crural diaphragm? Holland et al. 1994; Jones et al. 1994; Liu et al. 2000). This is an intriguing possibility, and suggests that

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