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 INTRODUCTION

In the anatomy of living beings, form has a meaning, a purpose. Maintaining useless designs would cost extra energy that could compromise the survival of a species. Accordingly, if the design of the anatomical components is optimized to serve a physiological role, why does the human spinal cord not completely occupy the inside of the vertebral canal ? And why is the caudal end of the spinal cord, the conus medullaris or medullary cone (MC), located between the T12 and L3 vertebrae ? (1)

According to Haeckel’s biogenetic law, ontogeny recapitulates phylogeny. (2) The morphological changes that occur during the embryonic development and growth of an individual (ontogeny) reproduce, in an abbreviated form, the evolutionary history of their species (phylogeny). Although formulated in the 18th and 19th centuries, the foundations of this theory retain much of their validity today. For this reason, the study of human phylogeny and ontogeny can help us understand the relationships between the structure and function of the spinal column and the spinal cord.

 PHYLOGENY OF THE VERTEBRAL COLUMN AND THE SPINAL CORD

Over the course of the evolution of species, the appearance of new biological structures and functions did not always mean the disappearance of the old ones, but rather that these –not always evident– persisted under the modern ones. As we outline below, in the anatomy of the human spine and spinal cord, several strategies have been adopted by evolution to protect the spinal cord from gait movements.

First chordates : Chordates (phylum : Chordata) first appeared in the Cambrian period (525 mya). Their anatomy resembled that of the current amphioxus (Branchiostoma lanceolatum). They lacked a skull, vertebrae, and a differentiated brain, but did have a primitive spinal cord located under the notochord, an elastic anatomical structure whose function is to return the spine to its original shape during lateral bending movements. In the amphioxus, the notochord and the spinal cord are approximately the same length.

Fish : At the end of the Cambrian period, the first chordates gave rise to the first vertebrates, the fish. The spine of the fish replaced the notochord as the primary axis of the body. In fish, as in other vertebrates, remains of the notochord are present in the nuclei pulposus of the intervertebral discs. Similar to amphioxus, fish move through the water by lateral-bending movements of the spine (Fig. 1A). Their swimming muscles attach to an axial skeleton composed of vertebrae that have a neural arch in the upper area. A succession of neural arches forms the vertebral canal, which houses the spinal cord. In fish, the spinal column and spinal cord are the same length.

Fig 1 A. Lateral bending of the spine of fish during swimming. - Fig 1 B. Lateral bending of the spine of salamanders during gait. The limbs act as points of support.

Amphibians and reptiles : Later, in the Devonian period (395 mya), some benthic fish that moved along the bottom of rivers and lakes, supported by their front fins, were able to come ashore by virtue of their rudimentary lungs. These so-called lungfish evolved into amphibians and reptiles. All four limbs of caudate amphibians (salamanders and newts) and of quadruped reptiles are involved in gait, although, as in fish, the main propellant is the lateral-bending movement of the spine (Fig. 1B). In most fish, caudate amphibians, reptiles and birds, the spinal cord occupies almost the entire interior of the vertebral canal.

Mammals : The next stage in the evolution of vertebrates was the emergence of quadruped mammals in the Cretaceous period (145 mya). After the mass extinction of the dinosaurs in the Palaeocene period (66 mya), mammals expanded to fill the ecological niches left vacant by the dinosaurs.

Similar to quadruped caudate amphibians and reptiles, quadruped mammals move by lateral-bending movements of the spine, which is associated with ventral (or anterior) and dorsal (or posterior) flexion movements. Thus, the spinal column moves by opening and closing like a drawing compass, whose hinge is located in the area between the thorax and the abdomen. This adaption required the development of vertebral curvatures and for the spinal muscles to migrate from the posterior to the anterior area of the spine.

The mammalian spinal cord is shorter than the vertebral column. Thus, for example, in pigs (Sus scrofa domestica) the MC is located at the level of L3-L5 ; (3) in guinea pigs (Cavia porcellus) at L2-L5 ; (3) in dogs (Canis familiaris) at L3-L7 ; (3) in the maned wolf (Chrysocyon brachyurus) at L3-L6 ; (4) in the horse (Equus ferus caballus) at L5-S2 ; (5) in the cat (Felis catus) at L6-S2 ; (6) in the rabbit (Oryctolagus cuniculus) at L6-L7 ; (5) in the paca (Agouti paca) at L5-L7 ; (7) in the buffalo (Bubalus bubalis) at S3 ; (8) in the sheep (Ovis aries) at S2 ;8 in the South American fur seal (Arctocephalus australis) at T6-T7 ; (9) in the echidna (Tachyglossus aculeatus) at T710 and in the platypus (Ornithorhynchus anatinus) at the sacral level. (10)

It is striking that in the echidna and the South American fur seal the MC is located at the thoracic level. The echidna is a primitive mammal that, together with the platypus, belongs to the taxonomic order of monotremes (egg-laying mammals). These two species of monotremes have the MC located at different levels of the spine : the echidna in the thoracic spine and the platypus in the lumbar spine. Why do these two species have the MC located at different levels ? According to Kappers, (11) the MC of the echidna is located at the thoracic level because it has a shorter (and atrophic) tail than the platypus. According to Mitchelle, (12) this hypothesis is incorrect, as the MC of other tailless mammals, including humans, is found in the lumbar area. Ashwell (10) has attributed the short length of the spinal cord in echidna to the fact that, when threatened, the echidna rolls up like a ball. According to this author, if the echidna’s spinal cord were to occupy the lumbar vertebral canal, this forced vertebral flexion could damage it.

A similar situation is found in the South American fur seal. Its MC is located at the thoracic level, (8) vertebrae higher than in the dog and the wolf, two animals belonging to the same taxonomic suborder, the caniform carnivores. As we shall propose later, this location of the MC would be explained by the large, turning body movements made by the South American fur seal. If the MC were at the lumbar level, the twisting of the spinal cord would cause injury.

Primates : The first primates arose in the Palaeocene period (66 mya), shortly after the extinction of the dinosaurs. They were small quadruped mammals that walked along the branches of trees with their bodies in a horizontal position (Fig. 2 above). They had a long lumbar spine, a short clavicle, shoulder blades arranged laterally on the thorax, and lateralized eyes. Some of these primates evolved by adapting their bodies to climb trees in an upright position. To do this, their head bent forwards and their eyes migrated frontally. Verticalization facilitated brachiation, a form of arboreal locomotion in which primates move along the branches with their hands and arms outstretched (Fig. 2 lower left).

Fig. 2. Primate skeletons. Above : quadruped. Bottom left : brachiator. Bottom right : biped (man). Reproduced by permission of the artist : Mauricio Antón (13)

Primate brachiators have long fingers to grasp branches, a developed shoulder girdle, a flattened dorsoventral thorax, shoulder blades on the rear of their backs, and long clavicles. They show significant lumbo-sacral rigidity, as their lumbar spine is shorter than that of their predecessors and the sacrum is verticalized. (14) As a result of this rigidity the lumbar vertebrae rotate en bloc in the same direction as the dorsal vertebrae during brachiation, and both pelvic and scapular girdles also rotate in the same direction.

Today’s primates have between 4 and 7 lumbar vertebrae. The level of the MC also varies considerably. In the common chimpanzee (Pan troglodytes) the MC is found at L2 ; (15) in the macaque (Macacus rhesus) at L4 ; (15) in the baboon (Papio papio) and the galago (Galago senegalensis) at L6 ; (15) in the marmoset (Callithrix jacus jacus) at L2-L44 and in the squirrel monkey (Saimiri sciureus) at S3 – Cc1. (4)

Hominids : In Europe, 11.62 million years ago, a species of bipedal brachiator primate walked upright on the branches of trees with their legs extended. Their first toe was highly developed, which allowed them to support their body weight. The lumbar spine was relatively long, with lordotic curvature, similar to that of more evolved hominids. (16)

From 5 to 10 million years ago, some non-biped brachiator primates descended from the trees, alternating between arboreal and terrestrial life. As they moved along the ground, the verticalization of the spine and brachiation movements were no longer useful, so they resorted to quadruped gait, this time resting on the dorsal aspect of the middle phalanges of the fingers (knuckle-walking), as in the case of today’s gorillas and chimpanzees. The vertebral column of those primates only had a slight dorsal-lumbar curvature with anterior concavity (Fig. 3 left).

The oldest known bipedal hominids –the Australopithecus– appeared about 4 million years ago. There is currently no consensus among anthropologists as to the origin of Australopithecus. Some claim that they evolved from terrestrial quadruped primates, whereas others speculate that they evolved from bipedal brachiator primates that walked upright in the trees.

Australopithecus slept in the trees. (17) Their pelvis was shorter than that of their ancestors and similar to that of modern man. Their lumbar spine consisted of 5-6 lumbar vertebrae, longer than in gorillas and chimpanzees (with 3-4 vertebrae). They walked slightly leaning forwards, as they did not yet present the lumbar lordotic curvature typical of humans.

Modern man : Finally, about 200.000 years ago, Homo sapiens, modern man, emerged. Man is the only primate that walks fully upright, thanks to lumbar lordosis (vertebral curvature with posterior concavity) (Fig. 3 right), which brings the load line closer to the body’s center of gravity (located inside the pelvis, close to S2).

Fig. 3 Left. Gorilla skeleton. Slight dorsolumbar curvature of anterior concavity and sloping body. Right. Human skeleton. Lumbar lordosis and upright posture. Drawings made in 1863 by Waterhouse.(18)

Humans retain much of the anatomical structures of their brachiator ancestors. As Arsuaga recalls (17) "To a great extent we are morphologically brachiators from the waist up, and bipeds from the waist down (including the pelvis), although the curvatures of our spine are an adaptation to standing gait".

Humans are not good swimmers, land runners, climbers or brachiators ; however, they are the only animals that can move using any of these four modes of locomotion, giving them great versatility to explore different environments. (19)

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 ONTOGENY OF THE SPINE AND THE SPINAL CORD

On the 16th day of gestation of the human embryo, the ectoderm thickens, giving rise to the neural plate. Shortly afterwards, the neural groove is formed, followed by the neural tube between day 19 and 21, from which the brain and spinal cord will emerge. During days 20 and 21 the head is flexed forward (ventrally). On the 27th day, the two neuropores of the neural tube are closed. Between days 28 and 30, the body will have completely folded, giving rise to a single ventral curvature. In the 5th week of gestation, the first outlines of the four limbs appear, whose shapes resembles the fins of fish.

During the first weeks of gestation, the spinal cord and the spine of the embryo are the same length (Fig. 4). From the 8th week onwards, the growth of the spinal cord is slower than that of the spine, giving rise to an apparent ascent of the MC through the interior of the vertebral canal. In its ascent, the MC drags behind it the roots of the spinal nerves (Fig. 7.5) and the caudal end of the dura mater (Fig. 7.7) and spinal pia mater, giving rise to the cauda equina and the filum terminale (Fig. 7.8).

In the 16th week, the MC is already positioned at the level of S1-S2 (Fig. 5), in the newborn at L2-L3 (Fig. 6), and in adults usually at L1-L2 (Fig. 7).

In childhood and adolescence, the ascent of the MC can strain the roots of the lumbosacral spinal nerves, causing pain and other neurological disorders. (20-21)

Fig. 4. First weeks of the embryo. The spinal cord and the spinal canal are the same length.

Fig. 5. Four-month-old embryo. MC at S1-S2.

Fig. 6. New-born. MC at L2-L3.

Fig. 7. Adult. MC at L1-L2.

– 1. Spinal cord.
– 2. Medullary cone.
– 3. Dura mater.
– 4. Filum terminale internum (inside dural sac).
– 5. Nerve root.
– 6. Nerve ganglion.
– 7. Base of dural sac.
– 8. Filum terminale externum (outside of the dural sac).
– 9. Coccygeal ligament.

The spine of newborns (Fig. 8a) has a curvature with ventral concavity and a MC located at L2-L3. At 3 months of age, a lordotic cervical curvature (posterior concavity) begins to develop, which enables the infant to turn their head.

Between the 5th and 13th month, the lumbar spine straightens (Fig. 8b). Around the 6th-10th month (Fig. 8c) children start to crawl, leaning on their hands ; and soon after, they begin to walk upright on their feet.

From 3 years of age (Fig. 8d) the lumbar lordotic curvature begins to form, adopting its final shape at 10 years of age (Fig. 8f).

Fig. 8. Ontogenesis of the curvatures of the spine. Reproduced from Kapandji22 with the permission of Editorial Maloine.. – a - 1 day – b - 5 months – c - 13 months – d - 3 years – e - 8 years – f - 10 years

The spine of the adult has 4 curvatures (cervical, dorsal, lumbar and sacral) and the MC is located between L3 and D12 (frequently at L1-L2). The spinal cord measures 42-45 cm and the filum, 20 cm. The dura and arachnoid mater extend as far as S2.

 RECAPITULATION OF PHYLOGENY AND ONTOGENY

Human phylogeny and ontogeny provide evidence for the existence of a close relationship between the level of the MC and the movements of the spine.

Throughout the evolution of vertebrates, the MC has progressively moved upwards inside the vertebral canal, in parallel with the increase in the width of the movements of anteroposterior flexion and rotation of the spine.

Fish, the first vertebrates, have a rectilinear spine that only allows them to make lateral-bending movements of the spine. The spine and spinal cord in fish are the same length.

Caudate amphibians (salamanders and newts) walk on all fours with lateral-bending movements of their spine and tail (Fig. 1B) and, as in fish, the spine and the spinal cord are approximately the same length

Other types of movements appear as we ascend the vertebrate phylogenetic ladder, such as anteroposterior flexion and spinal rotation. Within the same taxonomic group, the species with the greatest width in movements of their spinal column have the MC located at a higher level. For example, echidnas and seals can make large bending and rotating movements, and their MC is located at the thoracic level

Humans are unique among hominids, as the lumbar lordosis enables simultaneous rotating and counter-rotating movements of the spine. Among the hominids studied, the location of the MC is highest in man.

The direct relationship between vertebral movements and the location of the MC can also be observed in human ontogeny. During embryonic development the level of the MC rises inside the vertebral canal as the embryo increases the degree of flexion of the spine. A baby’s lumbar spine recapitulates the evolution of the spine in hominids. While the baby is crawling, the spine is straight and there are no changes in the position of the MC. When the baby begins to walk upright, curvatures appear in the spine, and the MC continues to ascend. This ascent stops when lumbar lordosis is fully consolidated.

 BIOMECHANICS OF THE SPINE AND THE SPINAL CORD IN MAN

To complete the study of the MC level, we shall briefly review some aspects of the biomechanics of bipedal gait.
The articular facets of the L4 and L5 vertebrae are orientated vertically, preventing the vertebrae from rotating on their axis. Lovett (23) discovered that the lumbar vertebrae rotate during lateral bending movements of the lumbar spine. The direction of rotation varies depending on the previous position of the spine : in the anatomical and ventral flexion positions, the lumbar vertebrae rotate in the opposite direction to the lateral bending, whereas in dorsal flexion position, they rotate in the same direction as the lateral bending.

Fig. 9. Rotational and counter-rotational movements of the shoulder and pelvic girdles during gait. Image reproduced with the permission of Serge Gracovetsky. (24).

According to Gracovetsky (24), each step of gait involves three synchronous movements (Fig. 9) :
– lateral flexion of the lumbar spine on the side of the leading foot (left) (Fig. 9. 1a)
– rotation of the pelvic girdle in the opposite direction to the front foot : from left to right (Fig. 9.1b) and from right to left (Fig. 9.2b)
– rotation of the shoulder girdle in the same direction as the forward foot (from left to right) (Fig. 9.2c).

Thus, the pelvic and shoulder girdles rotate in the opposite direction, as if they were two open drawing compasses joined by their hinges at the level of L3, the vertex of the lumbar lordosis (Fig. 10).

Fig. 10 A - Rotation and counter-rotation movements of two drawing compasses that make contact through their hinges (L3). B - At L3 the hinges of the two drawing compasses are joined. The upper one rotates in the direction of the shoulder girdle and the lower one in the direction of the pelvic girdle.

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L3 es la vértebra con mayor movilidad de la columna lumbar. Sus carillas articulares están horizontalizadas y paralelas entre sí, permitiéndole una gran capacidad de rotación. (22) Está situada cerca del centro de gravedad corporal. Funcionalmente es un punto de transición entre la zona superior e inferior del raquis. Según Kapandji.(22) L3 sirve de relevo muscular entre los haces lumbares del dorsal ancho (se insertan en las apófisis transversas de L3) y los haces del espinoso dorsal (se inserta en la apófisis espinosa de L3) (fig. 11).

L3 is the most mobile vertebra of the lumbar spine, as the articular facets are horizontally parallel to each other, allowing a great capacity for rotation. (22) L3 is located near the body’s center of gravity and, functionally, it is the transition point between the upper and lower area of the spine. According to Kapandji. (22) L3 serves as a muscular relay between the lumbar bundles of the latissimus dorsi (inserted into the transverse processes of L3) and the spinous dorsal bundles (inserted into the spinous process of L3) (Fig. 11).

Fig. 11. L3 is a transitional vertebra, both anatomically and functionally, where part of the upper and lower musculature of the spine converge. Original image by Kapandji. (22 Reproduced with permission of Editorial Maloine).

 WHY IS THE HUMAN MEDULLARY CONE LOCATED ABOVE L3 ?

According to Rubinstein (25) (cited by Roth),(26) the low sensitivity of nerve tissue to growth hormone is responsible for the asynchrony between the growth of the spine and the spinal cord. In mammals, however, this hypothesis does not explain the variability in the MC level that is evident among some species of the same taxonomic group. As we discuss below, a possible explanation for the location of the human MC above L3 is to prevent spinal twists that could injure the spinal cord when rotational and counter-rotating movements of the spine occur.

The spinal cord is suspended within the spinal canal by dentate ligaments, nerve root attachments, and the filum terminale. Flexion and rotation movements of the spine produce spinal tractions and rotations that reduce the diameter of the medullary blood vessels (Fig. 13). (27) The axons and medullary blood vessels are arranged in a zigzag pattern (Fig. 12) to prevent spinal movements from injuring the spinal cord. (27)

Fig. 12. Sagittal section of the cervical spinal cord at the level of C6. - A (left) Ventral flexion. Medullary axons straighten and tighten. - B (right) Dorsiflexion. Medullary axons fold in a zig-zag pattern. With permission, Breig 1978, Shacklock 2007. (28)

Fig. 13. Medullary blood vessels. Left. Ventral flexion movements of the spine tighten the spinal cord, reducing blood vessels diameter and flow. Right. Dorsiflexion movements of the spine decrease spinal tension, increasing the diameter and flow the blood vessels. With permission, Breig 1978, Shacklock 2007 (28)

If the spinal cord completely occupied the interior of the vertebral canal (Fig.15B), the rotational and counter-rotating movements of the spine produced during walking would twist the cord in a similar way to a towel that we twist with our hands (Fig. 14). Ischemia and spinal tissue injury would occur after multiple twists.

Fig. 14. Rotation and counter-rotation movements of the hands, twisting a towel.

A biomechanical solution to spinal twisting is to place the MC above the neutral point (with respect to rotation and counter-rotation) of the lumbar spine (Fig. 15 C) ; that is, above L3, such that the entire spinal cord rotates in only one direction (that of the shoulder girdle).

Congenital diseases, such as tethered cord syndrome, that present with adhesions that attach the spinal cord, meninges and filum terminale to the walls of the vertebral canal, favor the appearance of spinal cord torsions, through a similar mechanism to that shown in Figure 15 B.

Fig. 15 – A - Rotation and counter-rotation movements of two drawing compasses that make contact at their hinges. – B - Spinal cord completely occupying the interior of the lumbar vertebral canal (MC located below L3). Rotating and counter-rotating movements of the pelvic and shoulder girdles twist the spinal cord. – C - The spinal cord occupies the upper area of the lumbar vertebral canal (MC located above L3). The filum terminale (FT) is located below L3. The spinal cord rotates in the same direction as the shoulder girdle, and so spinal torsion does not occur.

 CONCLUSIONS

Despite great advances in the anatomy and physiology of the central nervous, much remains to be done in the field of spinal cord biomechanics.

Over the course of evolution, vertebrate species emerged that were capable of performing movements of rotation and anteroposterior flexion of the vertebral column, their spinal cord being shorter than their spine. This relative shortening of the spinal cord was an effective evolutionary strategy to prevent the spinal cord from twisting movements during walking, which could cause injury.

Comparative anatomy allows us to verify that the greater the width of these spinal movements, the shorter the length of the spinal cord with respect to the spine and, consequently, the higher location of the MC.

What is the clinical interest in knowing why the human MC is above L3 ? This interest lies in providing a greater pathophysiological understanding of ischemic myelopathies of tethered cord syndrome and also some lumbar syringomyelias. Understanding how body movements affect the physiology of the central nervous system should permit the design of less iatrogenic medical and surgical treatments (arthrodesis, orthopedic corsets, rehabilitation, osteopathy, chiropractic, etc). It can also be useful in sports practice, as it can help in the design of healthy physical exercises for people with different types of back injury/pain.

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