An ancestral axial twist explains the contralateral forebrain and the optic chiasm in vertebrates

in Animal Biology
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Among the best-known facts of the brain are the contralateral visual, auditory, sensational, and motor mappings in the forebrain. How and why did these evolve? The few theories to this question provide functional answers, such as better networks for visuomotor control. However, these theories contradict the data, as discussed here. Instead we propose that a 90-deg turn on the left side evolved in a common ancestor of all vertebrates. Compensatory migrations of the tissues during development restore body symmetry. Eyes, nostrils and forebrain compensate in the direction of the turn, whereas more caudal structures migrate in the opposite direction. As a result of these opposite migrations the forebrain becomes crossed and inverted with respect to the rest of the nervous system. We show that such compensatory migratory movements can indeed be observed in the zebrafish (Danio rerio) and the chick (Gallus gallus). With a model we show how the axial twist hypothesis predicts that an optic chiasm should develop on the ventral side of the brain, whereas the olfactory tract should be uncrossed. In addition, the hypothesis explains the decussation of the trochlear nerve, why olfaction is non-crossed, why the cerebellar hemispheres represent the ipsilateral bodyside, why in sharks the forebrain halves each represent the ipsilateral eye, why the heart and other inner organs are asymmetric in the body. Due to the poor fossil record, the possible evolutionary scenarios remain speculative. Molecular evidence does support the hypothesis. The findings may shed new insight on the problematic structure of the forebrain.

An ancestral axial twist explains the contralateral forebrain and the optic chiasm in vertebrates

in Animal Biology

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Figures

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    Ramón y Cajal’s theory for the contralateral organisation of the forebrain. He proposed that the contralateral somatosensory and motor representations are adaptations to the visual system (see text for explanation). O, optic tract; C, primary and secondary visual centres; M, decussating motor pathways; S, decussating sensory pathways; R, motor efferents of the spine; G, spinal ganglions and sensory afferents. Note that Cajal drew the spinal section upside down and the cortical hemispheres as fused. The secondary visual centres presumably refer to primary motor and somatosensory cortex. Reproduced from Ramón y Cajal (1898).

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    Model of the compensations to a axial turn in the early vertebrate development; (A-C) The embryo viewed from above, with rostral up. Black zone: dorsal; white zone: ventral; spotted: right side; dotted: prospective eye region. The embryo turns anti-clockwise, on its left side, as indicate by the stick-arrows in (A). The turn is compensated by anti-clockwise (filled arrows) and clockwise (dashed arrows) movements (B). Consequently, the rostral region is inverted with respect to the rest of the body (C). The optic vesicles (ov) emerge and evaginate. (D-E) Development of the optic tract, in ventral view (D) and dorsal view (E). The optic tracts (ot) originate from the retinas and grow medially towards the inverted “dorsal” of the forebrain region (black zone in ventral view). After the chiasm the optic nerves (on) project toward the dorsal optic tectum (te) of the opposite side (panel E). Note that the optic nerves also target the lateral geniculate nucleus of the thalamus (LGN).

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    Generalised schema of the 5-vesicle embryological stage of the vertebrate brain in medial view. The cerebellar, posterior and habenular commissures are located dorsally, whereas the anterior commissure is located ventral from the longitudinal axis of the brain (dotted line). Arrows: hypothetical location of the twist. inf: infundibulum. Redrawn from Von Kupffer (1906, fig. 13).

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    Antero-dorsal view on the head and anterior trunk region of a zebrafish embryo (Danio rerio) on the egg surface (see supplementary movies 1 and 2). The embryo is drawn in grey, the prospective eye regions white. Dashed contours show the previous location of the embryo. The location of the body on the back side of the egg is drawn dotted. Compensatory movements can be observed between 14:40 and 16:40 p.f. During this period those cells that will form the eyes migrate anti-clockwise (perspective of the embryo), whereas the future mid- and hindbrain cells migrate clockwise between 15:15 and 16:40 h (arrows). The right eye is initially invisible because it is hidden below the cells that will form the forebrain. The first 5 frames are interleaved by 30 min, the last one is 10:15 h later. Drawn from Keller et al. (2008: supplementary movie no. 2).

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    Stages of the early embryological development of the chick. (A) Anti-clockwise (embryo’s perspective) compensatory movements in the rostral region between stage 4 and 8 (presented is stage 6). A1: schematic dorsal view of the embryo. The white disk shows the location of a quail graft, implanted 24 h before (stage 3b) at the rostral end of the primitive streak. The dark spots are marked quail cells. The horizontal bars show the locations of transverse sections A2 and A3. Dashed lines mark the primitive streak (midline) and the borders of the region with quail cells in the rostral section (A2), used for alignment of the sections with the dorsal view. A2, A3: the two layers depict ectoderm and endoderm, with quail cells in black. Arrows: hypothetical anti-clockwise movements of rostral head region. (B) Overview of the sections in the stages 9, 10, 11, 13 and 14 of panels C and D. (C) Clockwise compensatory movements during stage 9-11. The ventricle (v) and truncus arteriosus (ta) are drawn in the same orientation in each stage, whereas the embryo migrates around this orientation (arrow). The atrium (a) is located in a different section in after stage 10. Shown are the neural tube (n) flanked by the otic vesicles (from stage 10), the notochord and pharynx (ph), flanked by the two dorsal aortas. e = endoderm. (D) During stage 13-17 a left-turn of the body occurs (presented are stage 13 and 14). As shown by the arrows, the heart also turns. Panel A: adapted from Lopez-Sanchez et al. (2001). Panels B-D: adapted from Bellairs and Osmond (2005). Scale bars are 300 μm.

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    Possible evolutionary scenarios. Panels show schematic frontal views displaying eyes, nostrils, mouth, and fin rays. One eye and one nostril are dotted to show that they do flip bodysides. (A) A deep bodied, free-swimming, early vertebrate (1) turned on its left side (2), for example to hide on the sea floor like a flatfish. The direction of compensation (3) of the mouth and external body parts (e.g. tail fin and dorsal and anal fins) is clockwise (perspective of the animal), as indicated with filled arrows. The eyes and the nostrils migrate in the opposite, anti-clockwise, direction (open arrows). (B) A benthic animal (1) might have turned on its left side to swim stretches or to capture prey (2). A more active form specialized on the locomotory orientation compensated the turn, again with the eyes and nostrils compensating anti-clockwise (open arrows), and the mouth and fins compensating clockwise (closed arrows, panel 2-3).

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