Comparative anatomy and physiology of excitatory conduction in the heart: Francis Davies and Eric Francis in Sheffield

‘Have you ever tied a Stannius ligature?’, is a conversation stopper. If the answer is ‘yes’ then you know the person you are talking to studied physiology at some time in the past and that a practical class was concerned with the workings of the frog’s heart—an organ ideal for hamfisted students since it beats spontaneously in isolation and they can learn a great deal about how hearts work in a couple of hours*. However, amphibian and reptilian hearts differ in a number of respects from those of birds and mammals.

One of the key players in the comparative anatomy and physiology of the heart is not remembered by the herpetologists, for example, although his great friend and collaborator is. Francis Davies (1897-1965) was at first sight a classical human anatomist—indeed he became co-editor of Gray’s Anatomy. He was born at Merthyr Tydfil, studied medicine in Cardiff and then University College London. In 1924 he became Senior Demonstrator in anatomy at UCl; he then moved to King’s College London as Reader. In 1935 he arrived in Sheffield as Professor; there he stayed until retirement in 1962. In Sheffield Davies worked on the heart with his friend, Eric Thomas Brazil Francis (1900-1993) who became Reader in Zoology until he retired in 1965.

Together, Davies and Francis studied the hearts of amphibians and reptiles in order to determine how the signal from the pacemaker that sets the heart rate passes first to the atria and then to the ventricle (single in amphibians and most reptiles) or ventricles (in crocodiles as in birds and mammals). Earlier in the 20th century Sir Thomas Lewis (1881-1945) had worked out what happened in mammals: specialised heart muscle cells form a dividing bundle of fibres (the Bundle of His) that convey the message to contract to all parts of the ventricles from the atrio-ventricular node. However, there are no special fibres from the pacemaking sino-atrial node to the atrio-ventricular node; impulses pass across the atria from muscle cell to muscle cell like a Mexican wave. It was Lewis’s brilliant work which made not only the physiology textbooks; the research explained a number of conditions that account for heart disease.

Conduction in the mammalian heart
The structures shown in BLACK are not present in
amphibians and reptiles.
from my 1961 edition of the classical physiology textbook
'BDS'

Francis had already published his book, The Anatomy of the Salamander, and their first joint work, published in 1941, was on the heart of that species (Salamandra salamandra). Francis and Davies concluded that in amphibians and reptiles there is no special conducting system in the heart responsible for spreading the process of excitation to the ventricles; the waves of excitation pass directly but relatively slowly from heart muscle cell to heart muscle cell. In other words, the Mexican wave of contraction continues across the whole heart in contrast to birds and mammals where a specialised bundle of fibres takes over.

Davies and Francis proposed that the reason for this major difference in the heart between ectothermic amphibians and reptiles, on the one hand, and endothermic birds and mammals on the other, is the the pace of life; heart rates are lower in the former than in the latter. Relying on a Mexican wave is just too slow for high heart rates to be achieved. They also suggested that the development of a special conducting system was a relatively recent evolutionary change. Their views still hold good.

But what about crocodilians with their two ventricles? Do they have a system like that in birds and mammals, or one characteristic of extant reptiles? Davies and Francis had that covered. They showed that crocodilians have no specialised conducting pathways.

Francis Davies and Eric Francis were not exemplars of the dyed-in-the-wool anatomists who never lifted their eyes from the dissecting table; nor did they confine their studies to comparative anatomy. Both stressed form and function. Davies while undoubtedly seen as a human anatomist of the old school, stressed in teaching anatomy to medical students ‘living’ functional anatomy. Francis was a zoological polymath. In their work on the vertebrate heart, they threw every technique then available at the problem of how excitation by the pacemaker is conducted to all parts: gross observation, dissection, serial sections for histology, histochemistry, slow-motion cinephotography, in-vitro physiology and electrocardiography.

Francis Davies had been unwell for some years when when he retired in 1962. He died in 1965. Eric Francis wrote his obituary for the Journal of Anatomy.

ETB Francis's drawing of the Salamander heart from the 1941 paper

*By tying two ligatures Hermann Friedrich Stannius (1808-1883) showed that the pacemaker of the frog’s heartbeat is in the sinus venosus and that impulses pass from there to the atria and then the ventricle. By isolating regions of the heart these two ligatures also showed that the chambers beat to their own rhythm spontaneously in the absence of input from the pacemaker. The first Stannius ligature is tied between the sinus venosus and the right atrium; the second between the atria and the ventricles. As a hoax the late Jim Linzell and I, in response to a letter asking for exhibits for a museum, put a length of cotton thread in an envelope and sent it along with the explanation that this was Stannius’s third ligature which he never got round to using because his wife had sent a message telling him to get home before his dinner got cold. It was dated 1 April. We never had a reply.

Davies F, Francis ETB. 1941. The heart of the salamander (Salamandra salamandra L.), with special reference to the conducting (connecting) system and its bearing on the phylogeny of  the conducting systems of mammalian and avian hearts. Philosophical Transactions of the Royal Society B 232, 99-130.

Davies F, Francis ETB. 1946. The conducting system of the vertebrate heart. Biological Reviews 21, 173-188

Davies F, Francis ETB, King TS. 1951. Electrocardiogram of the crocodilian heart. Nature 167, 146.

Davies F, Francis ETB, King TS. 1952. The conducting (connecting) system of the crocodilian heart. Journal of Anatomy 86, 152-161.

Francis, ETB. 1965. In memoriam: Francis Davies. Journal of Anatomy 99, 913-915.

Jensen B, Boukens BJD, Postma AV, Gunst QD, van den Hoff MJB, Moorman AFM, Wang T, Christoffels VM. 2012. Identifying the evolutionary building blocks of the cardiac conduction system. PLoS ONE 7(9): e44231. doi:10.1371/journal.pone.0044231