Development of the larynx

For many years embryologists have avoided a mechanistic analysis of craniofacio-cervical morphogenesis, largely because of the three-dimensional complexity of these regions. Despite its anatomical intricacy, development is more profitably explained in molecular or genetic terms and the genome is often analogized as a genetic blueprint. Genes involved in embryogenesis, however, more accurately serve as a set of assembly rules whose implementation and interaction govern the transition from one-dimensional information of the genotype into the three-dimensional complexity of the phenotype (Thorogood & Ferreti, 1992). The analysis of the development of the embryo is often achieved by the use of model systems or is extrapolated from the study of nonhuman vertebrates. Since evolution is a conservative process retaining and refining efficient morphogenetic processes, causal mechanisms are conserved over many years simply because they generate a successful phenotype. This appears to be true for the mammalian larynx where much of our knowledge has come from a detailed study of the human embryo. Although the development of the human larynx was described in 1820 by Fleischmann (cited by Soulie & Bardier, 1907) it was not until the pioneer work of His in 1885 on the development of the gastrointestinal tract and pharyngeal arches that serious attention was paid to the larynx.

For much of the twentieth century biologists resisted the concept that humans and other animals were part of an evolutionary continuum. They accepted that humans evolved from an ape-like ancestor but regarded tool use, culture and language as uniquely human. More recently, the size and nature of the ‘hiatus’ between humans and non-humans, specifically the great apes, has exercised the minds of workers in many disciplines (Gibson & Ingold, 1993). Research has shown that other primates show evidence of cognitive skills such as tool use or language; this concept is, however, resisted by those who believe that such attributes only occurred with the advent of Homo sapiens. The belief that ‘humanness’ appeared de novo, fully developed within the modern human brain and separating ‘Man’ from his ancestors, ignores the palaeoanthropological evidence but fuels philosophical discussion!

Much of the evidence for the origin of modern humans rests on the interpretation of fragments of bone, enigmatic archaeological discoveries or DNA gels. Whilst these provide intriguing signposts to the past and our relationships to the greatapes, they do nothing to explain ‘Man's’ bipedal stance, large brain and other human characteristics. The theory of ‘punctuated equilibrium’ suggests that all species undergo spurts of evolutionary change. These may be initiated by environmental changes – Leakey & Lewin (1992) proposing that global cooling was the driving force behind the evolution of humans.

In 1929 Victor Negus, a Junior Surgeon for Diseases of the Throat and Nose, Kings College Hospital, London, published a book entitled The Mechanism of the Larynx. Part of this was based on his research for a Degree of Master of Surgery in the University of London. However, this 528 page volume contained unique observations on the comparative morphology of a wide range of animal larynges, cumulating in a fundamental account of the origin, development and mechanism of this unique organ.

Early in my own laryngological career, I had read and marvelled at the erudition of this ‘amateur comparative anatomist’, ultimately hoping to extend his research by utilizing modern techniques and a wider range of animals. As Professor of Laryngology and Otology at the Institute of Laryngology and Otology in London, I had developed a laboratory for sectioning human larynges removed for cancer. This was for an investigation into the manner by which neoplasia spreads through this organ. On completion of this research in 1976, these facilities became available for detailed examination of other mammalian larynges. Specimens were collected over the following 17 years from zoological institutions, game parks and helpful friends throughout the world. Most, however, came from post-mortems carried out in the Pathology Department of the Zoological Society of London. Without the enormous support and good will of this institution and many other helpful people, this unique collection of mammalian larynges would have been impossible; my gratitude is infinite.

In order to confirm the cause of death and absence of infectious disease the majority of animals dying in zoological collections undergo detailed pathological examination. This provides a rich source of material for comparative studies and the majority of the 1410 mammalian larynges studied by the author over the past 18 years have come from the Pathology Department of the Zoological Society of London. Specimens have also been donated by many other zoos, university departments of anatomy and zoology as well as interested individuals from around the world. Some of the more unusual specimens were obtained ‘fresh’ within the game parks of Kenya and South Africa; only goodwill between many colleagues made this unique collection possible.

Where technically feasible the trachea was removed with the larynx and tongue base, allowing concurrent studies of tracheal morphology and the related recurrent laryngeal nerves. Together with the 1410 non-human larynges, a further 140 laryngectomy specimens were removed from patients with malignant disease (Harrison, 1983) and another 104 larynges removed from infants registered as having died from sudden infant death syndrome (SIDS) plus a control set of larynges from a similarly aged group of 20 infants dying from congenital heart disease (provided by five Paediatric Pathologists within the United Kingdom).

An essential feature has been the need for accurate identification of individual species, together with recording of sex, age and dead weight of each animal, all requiring a high degree of interpersonal expertise.

The development of comparative anatomy has been neither progressive nor continuous. Progress has been halted by intellectual stagnation, by failure to capitalize on earlier discoveries and by religious and political intolerance. Rarely can major advances be attributed to individuals but are usually the outcome of centuries of human endeavour. The eight centuries of Greek objectivity were followed by a period of scientific and artistic stasis which lasted for more than a thousand years.

It is unclear as to whether the earliest studies of animal anatomy were based primarily on a desire to study animal structure per se, or because of a hope that light might be thrown on the morphology of man. Animal dissections by both zoologists and anatomists date at least from the time of Aristotle (c. 384 BC) and reveal an objectivity common with other facets of Greek culture. However, the foundations for much of this scientific thought were developed in the earlier civilizations of Babylon and Egypt and were then developed by Greek philosophers primarily to assist and explain human problems. Aristotle's contributions to both zoology and comparative anatomy were extensive and his History of Animalsy the Parts of Animals and the Generation of Animals establish him beyond question as the founder of the biological sciences. Descriptions of the nictitating membrane of the eye, os cordis of the horse and ox and the os penis found in many carnivores were based upon his own dissections, although subsequent errors in translations of his works have seriously reduced our knowledge of the actual number of animals Aristotle studied.

It is widely accepted that the larynx evolved around the time that the respiratory system changed from gills to lungs. The earliest larynx consisted of a cartilaginous plate suspended from the vertebral column, as is found Protopterusy the lung fish. With increasing muscular activity, a more dynamic system was needed to provide a wider opening to the lungs and bilateral movable cartilages developed along the sides of the air passage. Sphincteric muscles wrapped around these lateral cartilages provided a means of closing the entrance to the lungs. Later, these fused to form the cricoid ring carrying or articulating with arytenoids on its upper surface. The more developed species formed a protective thyroid cartilage which ultimately articulated independently with the cricoid; this being the basic design of all present day mammalian larynges (Negus, 1949). Although this is so, morphological variations are common, being related in part to life-style and particularly dietary needs.

Most mammals have a well developed epiglottis protruding into the nasopharynx thereby enhancing olfaction and allowing respiration during feeding. The vocal cords vary in length and although arytenoids, corniculate and cuneiform cartilages are usually present, their size and shape depends upon the age and species of the animal. Large arytenoids surmounted by large corniculate cartilages provide a high posterior wall to the larynx, allowing masticated food to flow to the stomach by way of lateral channels on either side of the glottis.