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Axial twist
Schema of the proposed development of the axial twist. Developmental phases are (from top to bottom): (1) the embryo turns on its left side; (2) the anterior head grows in the same direction, but the rest of the body grows oppositely into a twist. So that ultimately (3) external bilateral symmetry is regained. Note, that there is no evolutionary pressure for internal symmetry so the heart (and other organs) remain asymmetric.
Details
Systemvertebrate body plan
Anatomical terminology

The axial twist theory (a.k.a. axial twist hypothesis) is a scientific theory put forward to explain a range of unusual aspects of the body plan of vertebrates (including humans).[1] It proposes that the rostral part of the head is "turned around" regarding the rest of the body.[2] This end-part consists of the face (eyes, nose, and mouth) as well as part of the brain (cerebrum and thalamus). According to the theory, the vertebrate body has a left-handed chirality.

The axial twist theory competes with a number of other proposals that focus on more limited, specific aspects, most of which explain contralateral forebrain organization, the phenomenon that the left side of the brain mainly controls the right side of the body and vice versa.[3] None of the proposed theories explaining this phenomenon, including axial twist theory, have gained general recognition.[4] The genetic basis underlying the proposed developmental twist is not yet understood.

The axial twist theory would explain various anatomical phenomena, and addresses how and when the proposed twist between the end of the head and the rest of the body develops. It also addresses the possible evolutionary history. One prediction of the theory was the aurofacial asymmetry, which was then found empirically,[5] albeit by one of the authors of the original theory.

Phenomena the theory can explain include:

According to the axial twist developmental model, the anterior part of the head turns against the rest of the body, except for the inner organs. Due to this twist, the forebrain and face are turned around such that left and right, but also anterior and posterior are flipped in the adult vertebrate.

History

[edit]

In the end of the 19th century, the famous neuroscientist and Nobel prize winner Santiago Ramón y Cajal proposed a theory to explain the contralateral organization of the forebrain that was rapidly and widely accepted.[6][4] This theory, the visual map theory, proposes that the optic chiasm restores the retinal image on the visual cortex,[7] Cajal's theory remained virtually undisputed for more than a century.[8][9] However, more ideas have been put forward (see section #Relation to other theories and hypotheses).

Embryology

[edit]
Antero-dorsal view on the head and anterior trunk region of a zebrafish embryo (Danio rerio) on the egg surface. Source: figure 4 of reference [1]

Although the embryological development of the axial twist has not been studied explicitly, there are clear indications from the zebrafish and the chick.[1] The twist begins briefly after the neurulation and commences in a rostrocaudal (front-to-tail) direction.[10]

Philipp Keller's group traced each cell of developing zebrafish embryos until the first heartbeat.[11] Tracing the movements of the cells in the future eye region and the hind part of the head, revealed opposite movement directions, in accordance with an axial twist. Whereas the left-eye eye-region cells tendentially moved outwards and downwards (ventrally), those of the right eye region moved out- and upwards, as visualized by a time-lapse video.[12] On the other hand, the surface cells of the hind side of the head moved to the left, consistent with an axial twist.[1]

The chick development has been studied well. The development is usually described according to the Hamburger–Hamilton stages.[13] The twisting begins during stage 6 on the rostral side of the head region[14] and commences until stage 14 towards the heart region.[10] Whereas the anterior head region rotates with the right side moving in an upward direction and the left side downward, the heart region moves in the opposite direction. In the end, the chick is turned on its right side, whereas the heart, not taking part in the twisting, has landed on the left side of the body.[1]

Genetic mechanisms

[edit]
Main articles: Nodal signaling pathway and Left-right asymmetry

The axial twist emerges through opposite asymmetric development. This can be observed as a wave moving across the embryo from anterior to posterior. It is now well established, that the Nodal signaling cascade and the right-to-left flow produced by ciliated cells in the primitive streak are central in setting up the asymmetric organization. Three aspects of this growth wave are:[1]

Nodal, FGF8, and shh as well as the motor protein Kif5c have been associated with the asymmetric growth of the anterior primitive node, although only Nodal seems to be expressed before the initiation of the asymmetry.[15][16] The Nodal gene and a zinc finger gene (cSnR) control the asymmetric development of the heart.[17] The right-side-turn of the body is tightly linked to the same genetic mechanisms.[17]

Developmental malformations

[edit]

In holoprosencephaly, the hemispheres of the cerebrum (or part of it) are not aligned on the left and right sides but only on the frontal and occipital sides of the skull, and the head usually remains very small. According to the axial twist theory, this represents an extreme case of Yakovlevian torque,[18] and may occur when the cerebrum does not turn during early embryology.[1]

Cephalopagus or janiceps twins are conjoined twins who are born with two faces, one on either side of the head. These twins have two brains and two spinal cords, but these are located on the left and the right side of the body.[19] According to the axial twist model, the two nervous systems could not turn due to the complex configuration of the body and therefore remained on either side.[1]

Evolution

[edit]

The axial twist is thought to have evolved in a common ancestor of all vertebrates, but the mechanism remains speculative.[1] Anatomy indicates that all vertebrates are twisted, but also most sister clades to vertebrates show similar forms of asymmetric, twisted development.[citation needed]

Even the most distant clades of vertebrates — the agnathan lampreys and hagfish — possess an optic chiasm and contralateral brain organization,[20] as well as a left-sided heart and asymmetric bowels.[21] Also, every vertebrate has a contralateral organization of the forebrain.[20] Fossil skull impressions of early vertebrates from the Ordovician and later show the presence of an optic chiasm.[22]

Twisting and asymmetric development are well known from other deuterostomes — such as Hemichordata, Echinodermata, Cephalochordata, and Tunicata.[citation needed] Turning toward the side or upside-down occurs also in these clades:

  • Sea stars turn their mouth downwards, after the larva has briefly been attached to a substrate by a rudimentary stalk, with the mouth turned up.[23]
  • The adult lancelet buries itself with its back downward and their mouth reaching out (cf. Lancelet#Habitat).[citation needed]

Some fish species tend to turn around when feeding from the water surface.[citation needed]

Morphology

[edit]
Caricature showing the external asymmetries due to the axial twist

The axial twist takes place in the early embryo of a vertebrate. There is an evolutionary pressure for animals towards bilateral symmetry, due to sexual selection (better looks to potential mates) and functional selection (e.g., better locomotion). The evolutionary pressure decreases with better symmetry. Accordingly, the pressure decreases as a body part is less associated with the body surface (less sexual selection) and the locomotor system (less functional selection).[5] Consequently, the axial twist theory predicts that small, systematic asymmetries remain on the outside of the body and that these asymmetries are larger on the inside of the body.[1][24][5]

Brain torque and spinal asymmetry

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Opposite rotational asymmetries as viewed from below. Left: the Yakovlevian torque in the cerebrum (exaggerated). Redrawn from Toga & Thompson.[25] Right: the opposite, rightward asymmetry of the thoracal spine.[26] Source: figure 4 of reference [5]
Main article: contralateral brain

The forebrain (cerebrum and thalamus) predominantly represents the opposite side of the body (and the visual world). However, motor control usually requires information from both sides of the body, and so the contralateral representation is by no means absolute. Rather, almost every region of the brain connects to both sides of the body.[27]

The Yakovlevian torque[25] (a.k.a. "counterclockwise brain torque"[28] refers to an anatomical peculiarity of the normal brain. On average, the frontal lobes are asymmetric to the left (the right lobe appears slightly larger than the left), whereas the occipital lobe is asymmetric to the right; the central sulcus and temporal lobe of the right cortical hemisphere are further to the front than those on the left. Overall, these asymmetries are equivalent to a slight rotation of the cerebrum (i.e. torque). Such a rotation is exactly as predicted by the axial twist theory, given that the cerebrum is not a superficial structure.[citation needed]

The torque is also known as "occipital bending"[29] if it is more strongly expressed on the occipital side than on the frontal side.

The spine is slightly asymmetric. In healthy subjects, the thoracic vertebrae (vertebra T6-T12) were on average asymmetric, such that the mid-line points to the right (2.5° in T6).[26] Thus, the Yakovlevian torque and the spinal asymmetry are in opposite direction, just as predicted by the axial twist theory.[citation needed]

Central nervous system decussations

[edit]
Some afferent decussations.
Pyramidal decussations.
Main article: decussation

If the right forebrain represents predominantly the left body and the left forebrain the right body, there should be positions of major nerve crossings behind the forebrain.[citation needed]

Anatomically, the contralateral organization of the forebrain is manifested by major decussations (based upon the Latin notation for ten, 'deca,' as an uppercase 'X') and chiasmas (after the Greek uppercase letter 'Χ,' chi). A decussation denotes a crossing of bundles of axonal fibers inside the central nervous system. As a result of such decussations: The efferent connections of the cerebrum to the basal ganglia, the cerebellum, and the spinal cord are crossed; and the afferent connections from the spine, the cerebellum, and the pons to the thalamus are crossed.[20] Thus, motor, somatosensory, auditory, and visual primary regions in the forebrain predominantly represent the contralateral side of the body.[citation needed]

Most afferent and efferent connections of the forebrain have bilateral components, especially outside the primary sensory and motor regions.[27]

Visual system

[edit]
Main articles: Visual system and optic chiasm
See also: Contralateral brain § The contralateral organization is incomplete

In the visual system, the eyes and its muscles lie in front of the twist, while the sensory and motor centers lie behind the twist. Thus, the developing nerves are predicted to seek their insertion on the opposite side of their origin.[citation needed]

Four of the cranial nerves serve the eye directly: one sensory and three motor nerves. The optic nerve is sensory and crosses the midline in the optic chiasm. The oculomotor nerve, trochlear nerve, and abducens nerve are motor nerves that control one or more of the eye muscles. The oculomotor nerve crosses the midline before leaving the central nervous system. The trochlear nerve crosses the midline in a chiasma on the dorsal side and the abducens innervates an eye muscle on the same side.[30]: Fig. 17.8 

In the light of the axial twist theory, this complicated pattern can be understood. The eyes, like the mouth and the nose originate from the anterior head region, i.e. in front of the twist. The only cranial nerve that originates from the forebrain is the olfactory nerve (see below). All other cranial nerves originate from regions of the central nervous system that lie behind the twist.[1]

The optic nerve inserts on the optic tectum of the midbrain. In tetrapods and bony fish it also branches off to the LGN of the thalamus in the forebrain, but not in other vertebrates such as sharks and skates). In sharks, the visual center in the cerebrum obtains its fibers from the optic tectum. On the way, these fibers cross the midline again so that each hemisphere of the cerebrum of sharks represents the eye on the same side.[31][32] Thus, the optic tract largely follows the prediction of the axial twist theory. The branch towards the LGN exists only in tetrapods[30] and is therefore generally understood as acquired later in the evolution of vertebrates and thus makes an exception.[citation needed]

The abducens nucleus is located in the pons. The abducens nerve innervates the lateral rectus muscle of the eye in most vertebrates, except lampreys and hagfishes.[21] It thus seems that the lateral rectus muscle evolved later and independently of the other eye muscles, and presents an exception to the axial twist model.[1]

Olfactory system

[edit]
See also: Olfactory system § Clinical significance
The olfactory (smelling) tracts do not chiasmate

The olfactory tracts run parallel to the optic tract but do not form a chiasm. Accordingly, each olfactory bulb connects to the same-side centers of the frontal cerebrum. This is entirely consistent with the axial twist theory because the nose is part of the anterior head region which twists along with the forebrain.[citation needed] Since the primary olfactory centers are at home in the cerebrum (olfaction is the only sense that originates in the cerebrum), each olfactory lobe is predicted to be represented by the cerebrum on the same side, which is indeed the case: whereas the olfactory tracts neighbour the optic tracts directly they do not chiasmate but insert on the ipsilateral side of the cerebrum (See figure).[citation needed]

Aurofacial asymmetry

[edit]
Exaggerated schema of the aurofacial asymmetry as predicted by the axial twist theory. During embryology and development, the face elements (red) are predicted to move toward the center from the left, with respect to the mid-plane between the ears. Source: figure 1c of reference[5]
Main article: facial symmetry § aurofacial asymmetry

The aurofacial asymmetry expresses the position of the face (eyes, nose, mouth) with respect to the plane perpendicular to the axis through the ears. As shown in the graph, the asymmetry decreases until the age of 13. Since the axial twist is located between the ears and the face, it is predicted that the face grows from the left to the midline, as is indeed the case.[5]

Orientation of internal organs

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Diagram of the human stomach, intestines, and rectum.
Main article: Heart development

The inner organs of the trunk are the regions on the body that are least mechanically associated with locomotion and the external body, and so are predicted by the axial twist theory to be the most asymmetric regions of the body. Other bilaterally symmetric animals such as insects and annelids are bilaterally symmetric also on the inside. The asymmetric development of the heart is well-researched.[17][33]

The question of why the heart should have a left-sided orientation, has been topic of scientific research before the axial twist theory was published, but none of the hypotheses could stand critical testing.[34]

The asymmetric orientation and position of the gastrointestinal tract arises during development by rotation (see Development of the digestive system). The lateral positions of the digestive organs are on the same side in all vertebrates liver and gall bladder on the right side and the stomach, pancreas, spleen and the final loop of the colon on the left side.[35]

Relation to other theories and hypotheses

[edit]
See also: Contralateral brain § Theories

There are no other theories or hypotheses that explain the entire spectrum covered by the axial twist theory,[citation needed] but a number of theories and hypotheses address isolated aspects in various depths.

Inversion hypothesis

[edit]
Main article: Inversion (evolutionary biology)

In 1822 the French zoologist Étienne Geoffroy Saint-Hilaire noted that the organization of dorsal and ventral structures in the crayfish (an arthropod) is opposite that of mammals, and he proposed that mammals and other vertebrates are turned upside down.[36][37] As explained above, Marcel Kinsbourne proposed that the body (soma) but not the anterior head is inverted (hence somatic twist hypothesis).[2]

There is molecular evidence for the inversion hypothesis in almost all groups of deuterostomes.[38][39]

Somatic twist hypothesis

[edit]

Marcel Kinsbourne's somatic twist hypothesis is most closely related to the axial twist theory. Both theories were presented as an improvement to the dorsoventral inversion hypothesis by the early 19th-century naturalist Étienne Geoffroy Saint-Hilaire[1][2] In contrast to the axial twist, the somatic twist does not address the developmental aspects. Also, it only explains the contralateral brain but not the orientation of the internal organs.[24]

Asymmetry of the spine

[edit]

No hypotheses have been published for the asymmetry of the spine. There is no other theory to explain the left position of the heart or the asymmetric orientation of the bowels and related organs.[26][5]

Contralateral forebrain

[edit]

Several hypotheses have proposed a function for (certain aspects of) the contralateral brain (i.e. the left forebrain representing mostly the right body and the right forebrain representing mostly the left body). Most prominent is Cajal's.[citation needed]

Cajal's visual map theory

[edit]

The visual map theory by Santiago Ramón y Cajal proposes that the optic chiasm restores the retinal image on the visual cortex.[7][8] Even though the theory is still supported,[4] several studies have pointed out the serious flaws in the theory.[1][2][40] Most importantly, the loop of the optic radiation undoes the potential repair of the optic projection on the cortex, which is the central idea of the theory. Also, the theory does not hold for important groups of vertebrates such as sharks because their cerebrum has an ipsilateral visual representation but a contralateral somatosensory and motor representation.[31][32]

Other functional hypotheses

[edit]

Functional[41][42] or topological[43] explanations fail because same-side connections are just as important as crossing ones.[44] Moreover, these explanations leave open why the brainstem and the cerebellum have a same-side organization of the body.[1]

Brain lateralization

[edit]

The Yakovlevian torque is often thought to reflect the lateralization of specific functions in the brain.[25]

The parcellation theory proposes that an increasing brain size can conserve coincidental contralateral organization,[27] but does not explain the optic chiasm, nor that most vertebrates have a rather small forebrain, especially the early forms.[45]

Open questions

[edit]

The axial twist theory is a novel scientific discipline and very few scientific papers have presently addressed it directly.[1][2][24][5] Although a considerable volume of research exists on the genetic and embryological mechanisms of asymmetric development, an open question is how the twist is initiated and how the inversion of the left-right and up-down axes in the anterior head region is established.[citation needed]

The embryology of the twisting has been addressed only rudimentarily in the chick and the zebrafish.[1] The differences in timing and mechanisms across the vertebrate clades are completely unknown.[citation needed]

The evolution of the axial twist is an open question. The founders of the axial twist idea (de Lussanet & Osse, and Kinsbourne) agree that the axial twist is universal in vertebrates and probably is a feature of all chordates.[1][2] Although the asymmetric development of other chordates such as the Lancelet has been studied in detail, no study has analysed this development in the light of the axial twist theory. Moreover, even other deuterostomes, i.e. the echinoderms (sea stars, sea lilies, etc.) show a marked asymmetric development and even an axial twist.[46] This twist has remarkable similarities to that in vertebrates, but no study has addressed this at present. Lastly, the asymmetric and twisted development is well known from gastropods and the relation to asymmetric development in vertebrates is an important question.[citation needed]

It has been proposed that problems in the axial twist development may play a central role in developmental malformations such as holoprosencephaly[1] and skoliosis[5] but these have not been looked into.[citation needed]

See also

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References

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Further reading

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