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Chiasm Formation in Man Is Fundamentally Different from That In Eye (2007) 21, 1264–1270 & 2007 Nature Publishing Group All rights reserved 0950-222X/07 $30.00 www.nature.com/eye 1,2 1 CAMBRIDGE OPHTHALMOLOGY SYMPOSIUM Chiasm formation MM Neveu and G Jeffery in man is fundamentally different from that in the mouse Abstract Eye (2007) 21, 1264–1270; doi:10.1038/sj.eye.6702839 At the optic chiasm axons make a key binary Keywords: optic chiasm; visual evoked decision either to cross the chiasmal midline to potential; anophthalmia; albino innervate the contralateral optic tract or to remain uncrossed and innervate the ipsilateral optic tract. In rodents, midline interactions between axons from the two eyes are critical for normal chiasm development. When one eye is removed early in development the Mammalian optic chiasm hemispheric projections from the remaining The retinofugal fibres in the mammalian visual eye are disrupted, increasing the crossed system make a binary decision to either cross projection at the expense of the uncrossed. the chiasmal midline and project to the This is similar to the abnormal decussation contralateral hemisphere or remain uncrossed pattern seen in albinos. The decussation and project to the ipsilateral hemisphere. The pattern in marsupials, however, is markedly percentage of fibres that remain uncrossed different. Early eye removal in the marsupial varies between species depending upon how has no impact on projections from the lateral the eyes are placed in the head. This remaining eye. These differences are related to partial decussation of optic fibres at the chiasm the location of the uncrossed projection forms the basis for normal binocular vision. through the chiasm. In rodents, axons that will The developmental mechanisms that form the uncrossed projection approach the determine the choice of projection in rodents chiasmal midline, while in marsupials they and ferrets are similar. In rodents and ferrets the remain segregated laterally through the retinotopic order present in the optic nerve is 1 Institute of Ophthalmology, chiasm. Histological analysis of the optic lost before the nerves fuse at the anterior University College London, chiasm in man provides anatomical evidence chiasm1–3 and the two projections from each eye London, UK to suggest that, unlike in rodents, uncrossed mix through each hemi-chiasm (Figure 1).4–6 axons are confined laterally from the optic 2Electrophysiology The marsupial chiasm is distinctly different nerve through to the optic tract and do not mix Department, Moorfields Eye from that in the rodent and ferret. The Hospital, London, UK in each hemi-chiasm. This is a pattern similar architecture of the chiasm is a central core and to that found in marsupials. two lateral appendages. Axonal projections Correspondence: Electrophysiological evidence in human destined for different hemispheres remain MM Neveu, anophthalmics shows that the failure of one strictly segregated along the complete length of Electrophysiology eye to develop in man has no impact on the Department, the optic nerve and through each hemi-chiasm Moorfields Eye Hospital, hemispheric projections from the remaining (Figure 2). Retinal ganglion cell axons destined London EC1V 2PD, eye. This strongly suggests that the for the ipsilalateral hemisphere never approach UK mechanisms regulating chiasmal development the chiasmal midline and remain confined Tel/Fax: þ 0207 253 3411. in man differ from those in rodents, but may laterally in the proximal optic nerve and chiasm. E-mail: Magella.Neveu@ be similar to marsupials. This implies that moorfields.nhs.uk In the chiasm they course through the lateral optic chiasm formation in rodents and ferrets appendages, which are segregated from the Received: 7 March 2007 is not common to placental mammals in contralaterally projecting axons by astrocytic Accepted: 21 March 2007 general. processes.7,8 Midline interactions in human chiasm formation MM Neveu and G Jeffery 1265 Primate optic chiasm Fibres patterns in the non-human primate have been studied more extensively.12–15 Horton12 examined There have been very few examinations of fibre order anterograde labelling patterns through the primate through the human optic chiasm. However, the results chiasm and showed that the findings described by obtained remain controversial. One of the earliest studies Wilbrand and Saenger9 in the human were an artefact by Wilbrand and Saenger9 showed that some axons resulting from neuronal degeneration following located laterally in the nerve cross the chiasmal midline monocular enucleation. These data12 supported a and that many crossed axons coursed through the number of other studies undertaken in Old World proximal contralateral nerve before approaching the Primates, suggesting that the two hemispheric optic tract. However, this analysis was undertaken in projections from each eye are largely segregated through tissue from a subject who had lost one eye 24 years before the chiasm, with the uncrossed projection confined death. Clinical studies cast further light on patterns of laterally, similar to that seen in the marsupial. Early fibre organisation through the human optic chiasm. studies on the Macaque monkey induced retinal lesions at Patients with pituitary tumours have a suprasellar specific locations to trace the patterns of nerve fibre extension from the pituitary fossa, which gives rise to degeneration through the optic nerve and chiasm. The central chiasmal compression. This primarily disrupts studies confirmed that temporal retinal lesions result in the crossed projection, while aneurysms impinging on degeneration confined to the lateral optic nerve and the lateral chiasm primarily disrupt uncrossed axons.10,11 lateral chiasmatic regions alone. Lesions of the nasal Such data are consistent with at least a partial separation retina, that have no involvement from axons originating of the two projections. from the temporal region, result in degeneration only in the medial or central optic nerve and in the central chiasmatic regions.13,14 Further studies by Naito15 on the Macaque, showed that when retinal ganglion cells in the temporal retina are labelled following small tracer injections into the thalamus, the labelled axons course laterally through the chiasm, while the chiasmatic pathways of more centrally located ganglion cells do not enter this region. These data suggest that the fibre architecture of the primate optic chiasm is consistent with that seen in the marsupial. Figure 1 The distribution of uncrossed fibres in the rodent hemi-chiasm. The midline is to the left and the chiasm has been Monocular enucleation studies sectioned transversally. In rodents and ferrets these fibres are distributed widely rather than grouped laterally. Scale bar, It appears that there may be at least two structural 250 mm (from Baker and Jeffery4). forms to the mammalian chiasm; one present in Figure 2 Coronal section through the marsupial optic chiasm, showing the main body of the chiasm and two lateral components (left, scale bar 0.25 mm). The fibres that will cross to the contralateral hemisphere are contained within the main body. The fibres that will project to the ipsilateral hemisphere are contained within the two lateral appendages. The arrow indicates the location of the fissure that divides the main body of the chiasm from the lateral body. This is detailed in the photomicrograph (right, scale bar 40 mm), where the fissure is continuous along the dorsoventral axis (from Jeffery and Harman7). Eye Midline interactions in human chiasm formation MM Neveu and G Jeffery 1266 rodents and ferrets and the other in marsupials Histological analysis of human nerve fibre patterns and perhaps man. Monocular enucleation studies Histological analysis of nerve fibres in the optic chiasm have also shown that the developmental mechanisms was carried out to investigate the decussation pattern of of optic chiasm formation are fundamentally different the visual pathways in the human.24 Fibres were in these animals. In rodents and ferrets, where silver-stained and the fibre patterns at the proximal optic crossed and uncrossed fibres are intermingled at the nerve, chiasm and distal optic tract were examined. chiasmal midline, monocular enucleation early in Detailed analysis of these regions demonstrated that the development reduces the uncrossed projection in human optic chiasm contains two spatially distinct favour of the crossed.16,17 This is similar to the fibre retinal axon trajectory patterns that probably represent pattern found in albinism, where disruption of the course of the crossed and uncrossed hemispheric melanin synthesis, due to a mutation of the Tyrosinase projections (Figure 4). These appear to be largely gene, results in an abnormal projection of the separate, with the uncrossed projection confined laterally, retinofugal fibres at the optic chiasm (Figure 3).18 while the crossed projection occupies more central However, in marsupials, where uncrossed axons locations. Groups of axons in the central region are are segregated laterally and do not approach the interdigitated in regular plaits across the full length of chiasmal midline, early eye removal has no impact the midline, demonstrating that axons from each eye on the projections from the remaining eye.19 Hence, intermingle in this region as they course through to the there are at least two separate mechanisms regulating contralateral optic tract. Axons located laterally could be chiasm formation. One in rodents and ferrets where traced in clear parallel lines through from the junction midline interactions are significant, and another in with the nerve towards the optic tract, and at no point marsupials where they are not. did they appear to deviate from this lateral region and approach the midline (Figure 4). However, there was no obvious morphological feature separating the two Fibre patterns in the human optic chiasm projections as found in the marsupial.7 Rodent and ferret models of chiasm development Further, there is no obvious change in axon order in the have been regarded as typical of most mammals, proximal optic nerve that might represent a shift away including man.20–23 However, there is evidence that from the retinotopic pattern found along the length of the the human chiasm is fundamentally different.
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