No crossing at the crossing

by R. W. Guillery

Two papers (1,2), to be published within a fortnight of one another, offer new insights into how the brain processes sensory events. Both report individuals in whom all fibres from the eye pass to the cerebral hemisphere without crossing the midline. The first paper, which will appear in the March issue of The European Journal of Neuroscience, is by Apkarian et al., and is of interest because it deals with two children and gives an indication of how such abnormalities may be spotted. The second, by Williams et al., (page 637 of this issue) describes an inherited abnormality in sheepdogs, offering greater scope for experimental, particularly developmental, studies.

These results bear on a topic with a rich history, for it has long been assumed that our brains need orderly maps of the outside world. Descartes argued that because our lenses reverse the image falling on the retinas, there must be a partial fibre crossing in the brain so that the two reversed images, one from each eye, can be brought into register in the pineal (Fig. 1; see ref. 3 for references). Newton (3), also starting from the optics, proposed that there must be a partial crossing in the optic chiasm, and clearly described the optic chiasm as we now know it in primates. The underlying thought for both was that some surrogate 'person' in the brain must have a map if seeing was to be possible. Convincing experimental evidence about the chiasm was not obtained until the late nineteenth century. Although von Gudden (4) (the psychiastrist who certified 'mad' King Ludwig of Bavaria, and subsequently drowned with the king in Lake Starnberg) identified the partial crossing in rabbits (as in Fig. 2c), it was some years before this pattern was accepted as characteristic of mammals. Birds such as the owl, in which all the fibres cross at the chiasm, remained a puzzle, until is was shown that a partial intracerebral crossing (5) established a pathway rather like that proposed by Descartes. However, owls do not have the completely uncrossed optic nerves of Fig. 1, nor is the pineal still considered relevant to vision.

Thinking about sensory mechanisms continued under the implicit or explicit domination of a cerebral 'being' that needed maps. A striking example was Cajal's suggestion (6) that the combination of reversing lens and the need for maps had led to each hemisphere being connected to the opposite side of the body (see Fig. 2). His explanation has great appeal, and the accumulation of solid evidence for extraordinarily accurate motor and sensory (touch, sight, hearing) maps in the brain has seemed to confirm views that started out as assumptions about perception.

Figure 2 shows that if, as in the children and dogs now described, the entire optic nerve goes to one hemisphere without crossing, there must be a partial map reversal. If, for the mammalian system shown in Fig. 2c, the abnormal pathway maps with normal topography but on the wrong side, then the arrow head would map to regions normally occupied by the tip of the tail, producing a reversal.

The G in Cajal's drawing (Fig. 2c) represents the main relay to the cortex, the lateral geniculate nucleus. This is now known to consist of two sets of stacked layers, not the single continuous layer shown. The stacked layers are shown in Fig. 4 of the paper by Williams et al. (2) (page 639), where the abnormal reversal is evident (Fig. 4b).

How does the brain deal with such reversals? The observation that children and dogs show a nystagmus (an involuntary oscillatory movement of the eyes) demonstrates that subcortical centres controlling eye movements do not compensate for the reversal. This is important because in albinos, who also have an abnormality of the crossing pattern (1,2,7) and a nystagmus, it has never been easy to blame the abnormal crossing for the nystagmus; albinos also have other abnormalities of central vision. The children in the study by Apkarian et al. (1) may demonstrate a clear link between the nystagmus and the reported low visual acuity on the one hand, and the pathway abnormality on the other, thus also providing a useful tool for identifying the abnormality in other species.

The cerebral cortex must be smarter than the subcortical centres. The children report normal visual fields, and our knowledge of the albino mutation suggests that the cortex can deal with the mirror reversal, either by keeping the two maps, one a reversal of the other (one black, one white in Fig. 4c of the paper in this issue) in two separate cortical domains, or else by rewiring the connections going to the cortex so that the numerical sequence running from 8 to 1 in Fig. 4c is re-created as a continuous sequence in the cortex (8,9). The C-shaped fusion of geniculate layers in the dogs point to rewiring, but the critical evidence is not available. The experiment in dogs is simple and is, no doubt, being done.

Developmental mechanisms producing the modified geniculocortical pathways are likely to prove of particular interest, as establishing two independent cortical domains almost cetrainly depends upon visual experience. By contrast, rewiring the geniculocortical pathway is a prenatal event, independent of vision (9, 10).

Perhaps a most telling point in support of the assumptions about maps made over 300 years ago is that a map like that in Williams and colleagues' Fig. 4c, which is part black and part white, containing an internal reversal, cannot be established in the cortex unless one part is very small, or the reveral is corrected (7,10). The internal inconsistency seems to fool the cortex, as Descartes, Newton and Cajal thought it should. However, against their expectations, the brain has a way of dealing with total reversals.

R.W. Guillery is in the Department of Human Anatomy, University of Oxford, South Parks Road, Oxford OX1 3QX, UK.

  1. Apkarian, P., Bour, L. & Barth, P.G. Eur. J. Neurosci. 6, 501-507 (1994).
  2. Williams, R.W., Hogan, D. & Garraghty, P.E. Nature 367, 637-639 (1994).
  3. Polyak, S. The Vertebrate Visual System (University of Chicago Press, 1956).
  4. von Gudden, B. Gesammelte und Hinterlassene Abhandlungen (Bermann, Wiesbaden, 1889).
  5. Pettigrew, J.D. Proc. R. Soc. B204, 435-454.
  6. Cajal, S. Ramon y Histologie du Systeme nerveux de l'Homme et des Vertebres. (Maloine, Paris, 1911).
  7. Guillery, R.W. Trends Neurosci. 9, 364-367 (1986).
  8. Kaas, J.H. & Guillery, R.W. Brain Res. 59, 69-95 (1973).
  9. Hubel, D.H. & Wiesel, T.N. J. Physiol. 218, 33-62 (1971).
  10. Gullery, R.W. & Cassagrande, V.A. J. Comp. Neurol. 174, 15-46 (1977).

Figure 1. Schema proposed by Descartes for bringing two orderly mapped representations of the visual field into register with each other in the pineal gland. Because the lens reverses the image, a partial crossing must occur somewhere to allow a superpostion of the images of the two arrows. Descartes placed the partial crossing in the brain, Newton at the optic chiasm. (Figures 1 and 2 redrawn by Terry Richards from the originals.)

Figure 2. Schemas proposed by Cajal to account for the structure of the optic chiasm, and to explain why each cerebral hemisphere controls the opposite side of the body rather than its own side. Again, the problem is set by the reversing lens, which in a produces a broken arrow in the brain. b, How in vertebrates the problem is resolved by a crossing in the optic chiasm. Now the left hemisphere sees the right part of the world, and the motor (M) and sensory (S) pathways have to be crossed to accommodate the visual crossing. c, What happens when the eyes face forward and both eyes share a part of the visual field. Now some of the fibres cross, other stay on their own side. This is the situation in most mammals. The G in Cajal's figure is the lateral geniculate nucleus, the main relay on the way to the cortex. Here Cajal showed a broken arrow which he puts right by a further crossing on the path to the cortex. We now know that this relay is not a single continuous layer as in c, but two sets of stacked layers, arranged so theat the small piece of each arrow lies directly opposite the visually corresponding part on the long piece (see Fig 4a, page 639). The geniculocortical crossing is not needed in a normal animal, but has been demonstrated in animals having an abnormal chiasm.

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