A gastrointestinal role for the amphibian ‘diaphragm’ of Xenopus laevis

Abstract

The 'diaphragm' of Xenopus laevis has close anatomical relations to the lower end of the oesophagus. In mammals, the crural diaphragm acts as a pinch valve at the gastro-oesophageal junction and is an important component of the gastro-oesophageal reflux barrier. The present study analysed the effect of amphibian 'diaphragm' contraction on oesophageal pressure using a superfused in situ oesophago-diaphragmatic preparation of large female Xenopus. Three-dimensional reconstruction of the oesophageal pressure profile was performed using four-port oesophageal infusion manometry. Bilateral electrical stimulation of the nerves supplying the 'diaphragm' of Xenopus increased the pressure volume vector of 5 mm of oesophagus (centred around the insertions of the diaphragm) from 20.4 ± 16 to 553.6 ± 232 mm · mmHg 2 (mean ± SD). This was a statistically significant increase and statistically significantly higher than that evoked by electrical stimulation of both vagi (28.1 ± 30.7 mm · mmHg 2 ). The amphibian 'diaphragm' seems to be functionally similar to the mammalian crural diaphragm. By analogy, we suggest that the original role of the diaphragm was not respiratory but gastrointestinal.

A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles

“…In anamniote tetrapods, some frogs (in particular Xenopus ) have a ‘diaphragm’ that covers the lungs cranially (Keith, ; Pickering & Jones, ; Pickering et al ). Because this structure of Xenopus , like the mammalian diaphragm, is located caudal to the pericardial cavity, homology between these two tissues has been proposed repeatedly (Keith, ; Eisler, ; Pickering & Jones, ).…”

A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles

“…In anamniote tetrapods, some frogs (in particular Xenopus ) have a ‘diaphragm’ that covers the lungs cranially (Keith, ; Pickering & Jones, ; Pickering et al ). Because this structure of Xenopus , like the mammalian diaphragm, is located caudal to the pericardial cavity, homology between these two tissues has been proposed repeatedly (Keith, ; Eisler, ; Pickering & Jones, ).…”

On the anuran muscle pulmonum proprius

“…Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004). Although the latter authors have demonstrated that m. pulmonum proprius acts as a lower oesophageal sphincter, they did not rule out other physiological roles such as preventing aerophagy or retracting the stomach after vomiting.…”

“…These observations raise the following question: is the lung-inserted muscle of Bombina, Pelophylax and Rana homologous to the m. pulmonum proprius described by Beddard for Pipa and Xenopus? Few works dealing with the axial musculature in anurans were published and only some of them had studied the m pulmonum proprius with either Xenopus or Pipa as model organism (Dunlap, 1960;de Jongh, 1972;Snapper, Tenney and McCann, 1974;De Troyer et al, 1981;Pickering, Campion and Jones, 2004;Uriona and Farmer, 2006;Kimura, 2010). Most of them have referenced the work of Keith (1905) although without mentioning where the presence of m. pulmonum proprius is demonstrated for non pipid anurans.…”

“…With respect to the function of the m. pulmonum proprius, most studies dealing with this aspect used Xenopus as the model organism (Snapper et al, 1974;Pickering et al, 2004). Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004).…”

Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis)

“…Diaphragm-like muscles have been identified in some frogs (Xenopus laevis and Pipa pipa) (Keith, 1905;Snapper et al, 1974), and some testudines (e.g. Trionix) (Gaunt and Gans, 1969;George and Shah, 1959) and prior studies implicate a respiratory or gastrointestinal function in these lineages (Pickering et al, 2004;Pickering and Jones, 2002;Snapper et al, 1974). However, electrical activity of the amphibian diaphragm suggests a role for this muscle in aquatic locomotion (De Jongh, 1972) and we have measured electrical activity in the chelonian diaphragmaticus that is coincident with changes in pitch and roll during aquatic locomotion (T.J.U.…”

A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles

“…In anamniote tetrapods, some frogs (in particular Xenopus ) have a ‘diaphragm’ that covers the lungs cranially (Keith, ; Pickering & Jones, ; Pickering et al ). Because this structure of Xenopus , like the mammalian diaphragm, is located caudal to the pericardial cavity, homology between these two tissues has been proposed repeatedly (Keith, ; Eisler, ; Pickering & Jones, ).…”

On the anuran muscle pulmonum proprius

“…Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004). Although the latter authors have demonstrated that m. pulmonum proprius acts as a lower oesophageal sphincter, they did not rule out other physiological roles such as preventing aerophagy or retracting the stomach after vomiting.…”

“…These observations raise the following question: is the lung-inserted muscle of Bombina, Pelophylax and Rana homologous to the m. pulmonum proprius described by Beddard for Pipa and Xenopus? Few works dealing with the axial musculature in anurans were published and only some of them had studied the m pulmonum proprius with either Xenopus or Pipa as model organism (Dunlap, 1960;de Jongh, 1972;Snapper, Tenney and McCann, 1974;De Troyer et al, 1981;Pickering, Campion and Jones, 2004;Uriona and Farmer, 2006;Kimura, 2010). Most of them have referenced the work of Keith (1905) although without mentioning where the presence of m. pulmonum proprius is demonstrated for non pipid anurans.…”

“…With respect to the function of the m. pulmonum proprius, most studies dealing with this aspect used Xenopus as the model organism (Snapper et al, 1974;Pickering et al, 2004). Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004).…”

Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis)

“…Diaphragm-like muscles have been identified in some frogs (Xenopus laevis and Pipa pipa) (Keith, 1905;Snapper et al, 1974), and some testudines (e.g. Trionix) (Gaunt and Gans, 1969;George and Shah, 1959) and prior studies implicate a respiratory or gastrointestinal function in these lineages (Pickering et al, 2004;Pickering and Jones, 2002;Snapper et al, 1974). However, electrical activity of the amphibian diaphragm suggests a role for this muscle in aquatic locomotion (De Jongh, 1972) and we have measured electrical activity in the chelonian diaphragmaticus that is coincident with changes in pitch and roll during aquatic locomotion (T.J.U.…”

A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles

“…In anamniote tetrapods, some frogs (in particular Xenopus ) have a ‘diaphragm’ that covers the lungs cranially (Keith, ; Pickering & Jones, ; Pickering et al ). Because this structure of Xenopus , like the mammalian diaphragm, is located caudal to the pericardial cavity, homology between these two tissues has been proposed repeatedly (Keith, ; Eisler, ; Pickering & Jones, ).…”

On the anuran muscle pulmonum proprius

“…Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004). Although the latter authors have demonstrated that m. pulmonum proprius acts as a lower oesophageal sphincter, they did not rule out other physiological roles such as preventing aerophagy or retracting the stomach after vomiting.…”

“…These observations raise the following question: is the lung-inserted muscle of Bombina, Pelophylax and Rana homologous to the m. pulmonum proprius described by Beddard for Pipa and Xenopus? Few works dealing with the axial musculature in anurans were published and only some of them had studied the m pulmonum proprius with either Xenopus or Pipa as model organism (Dunlap, 1960;de Jongh, 1972;Snapper, Tenney and McCann, 1974;De Troyer et al, 1981;Pickering, Campion and Jones, 2004;Uriona and Farmer, 2006;Kimura, 2010). Most of them have referenced the work of Keith (1905) although without mentioning where the presence of m. pulmonum proprius is demonstrated for non pipid anurans.…”

“…With respect to the function of the m. pulmonum proprius, most studies dealing with this aspect used Xenopus as the model organism (Snapper et al, 1974;Pickering et al, 2004). Two main functions have been suggested for the m. pulmonum proprius: respiratory (Snapper et al, 1974) and gastrointestinal (Pickering et al, 2004).…”

Recruitment of the diaphragmaticus, ischiopubis and other respiratory muscles to control pitch and roll in the American alligator (Alligator mississippiensis)

“…Diaphragm-like muscles have been identified in some frogs (Xenopus laevis and Pipa pipa) (Keith, 1905;Snapper et al, 1974), and some testudines (e.g. Trionix) (Gaunt and Gans, 1969;George and Shah, 1959) and prior studies implicate a respiratory or gastrointestinal function in these lineages (Pickering et al, 2004;Pickering and Jones, 2002;Snapper et al, 1974). However, electrical activity of the amphibian diaphragm suggests a role for this muscle in aquatic locomotion (De Jongh, 1972) and we have measured electrical activity in the chelonian diaphragmaticus that is coincident with changes in pitch and roll during aquatic locomotion (T.J.U.…”