Axial twist theory


The []axial twist theory is a proposed scientific theory to explain a range of unusual aspects of the body plan of vertebrates. It states that the rostral part of the head is "turned around" regarding the rest of the body. This end-part consists of the face as well as part of the brain. 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. None of the proposed theories explaining this phenomenon, including axial twist theory, have gained general recognition. 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, 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

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. This theory, the visual map theory, proposes that the optic chiasm restores the retinal image on the visual cortex. Cajal's theory remained virtually undisputed for more than a century. However, more ideas have been put forward.

Embryology

Although the embryological development of the axial twist has not been studied explicitly, there are clear indications from the zebrafish and the chick. The twist begins briefly after the neurulation and commences in a rostrocaudal direction.
Philipp Keller's group traced each cell of developing zebrafish embryos until the first heartbeat. 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, those of the right eye region moved out- and upwards, as visualized by a time-lapse video. On the other hand, the surface cells of the hind side of the head moved to the left, consistent with an axial twist.
The chick development has been studied well. The development is usually described according to the Hamburger–Hamilton stages. The twisting begins during stage 6 on the rostral side of the head region and commences until stage 14 towards the heart region. 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.

Genetic mechanisms

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:
  • the asymmetric growth in the anterior tip of the primitive node,
  • the left-right situs of the organs and
  • the right-side-turn of the body.
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. The Nodal gene and a zinc finger gene control the asymmetric development of the heart. The right-side-turn of the body is tightly linked to the same genetic mechanisms.

Developmental malformations

In holoprosencephaly, the hemispheres of the cerebrum 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, and
may occur when the cerebrum does not turn during early embryology.
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. 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.

Evolution

The axial twist is thought to have evolved in a common ancestor of all vertebrates, but the mechanism remains speculative. However, twisting and asymmetric development are well known from other deuterostomes, such as Echinodermata, Cephalochordata, and Tunicata; as well as from gastropods.
De Lussanet et al. posit two possible evolutionary origins: one, that an ancestral vertebrate turned to its left side during the transition from a free-swimming larva to a bottom-feeding adult stage, like modern-day flatfishes. The other hypothesis is that an ancestor of vertebrates was a bottom-feeder that turned to the left to move around, with this body position evolving to the orientation of the free-swimming last common ancestor. This second hypothesis would connect to the lifecycle of the closely related Cephalochordata, which have a mouth that is initially on the left side before moving to ventral position but lack an axial twist. Following the hypothesis of Dzik et al., de Lussanet suggests that if the second hypothesis is correct, then the first stage was the enigmatic Ediacaran fossil Dickinsonia, and the second stage is represented by the early Cambrian Yunnanozoon.
Even the most distant clades of vertebratesthe agnathan lampreys and hagfishpossess an optic chiasm and contralateral brain organization, as well as a left-sided heart and asymmetric bowels. Also, every vertebrate has a contralateral organization of the forebrain. Fossil skull impressions of early vertebrates from the Ordovician and later show the presence of an optic chiasm.

Morphology

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 and functional selection. The evolutionary pressure decreases with better symmetry. Accordingly, the pressure decreases as a body part is less associated with the body surface and the locomotor system. 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.

Brain torque and spinal asymmetry

The forebrain predominantly represents the opposite side of the body. 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.
The Yakovlevian torque, 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. Such a rotation is exactly as predicted by the axial twist theory, given that the cerebrum is not a superficial structure.
The torque is also known as "occipital bending" 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 were on average asymmetric, such that the mid-line points to the right. Thus, the Yakovlevian torque and the spinal asymmetry are in opposite direction, just as predicted by the axial twist theory.

Central nervous system decussations

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.
Anatomically, the contralateral organization of the forebrain is manifested by major decussations and chiasmas. 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. Thus, motor, somatosensory, auditory, and visual primary regions in the forebrain predominantly represent the contralateral side of the body.
Most afferent and efferent connections of the forebrain have bilateral components, especially outside the primary sensory and motor regions.

Visual system

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.
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.
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. All other cranial nerves originate from regions of the central nervous system that lie behind the twist.
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. Thus, the optic tract largely follows the prediction of the axial twist theory. The branch towards the LGN exists only in tetrapods and is therefore generally understood as acquired later in the evolution of vertebrates and thus makes an exception.
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. 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.