Segregated hemispheric pathways through the optic chiasm distinguish primates from rodents

Abstract

At the optic chiasm retinal fibers either cross the midline, or remain uncrossed. Here we trace hemispheric pathways through the marmoset chiasm and show that fibers from the lateral optic nerve pass directly toward the ipsilateral optic tract without any significant change in fiber order and without approaching the midline, while those from medial regions of the nerve decussate directly. Anterograde labeling from one eye shows that the two hemispheric pathways remain segregated through the proximal nerve and chiasm with the uncrossed confined laterally. Retrograde labeling from the optic tract confirms this. This clearly demonstrates that hemispheric pathways are segregated through the primate chiasm. Previous chiasmatic studies have been undertaken mainly on rodents and ferrets. In these species there is a major change in fiber order pre-chiasmatically, where crossed and uncrossed fibers mix, reflecting their embryological history when all fibers approach the midline prior to their commitment to innervate either hemisphere. This pattern was thought to be common to placental mammals. In marsupials there is no change in fiber order and uncrossed fibers remain confined laterally through nerve and chiasm, again, reflecting their developmental history when all uncrossed fibers avoid the midline. Recently it has been shown that this distinction is not a true dichotomy between placental mammals and marsupials, as fiber order in tree shrews and humans mirrors the marsupial pattern. Architectural differences in the mature chiasm probably reflect different developmental mechanisms regulating pathway choice. Our results therefore suggest that both the organization and development of the primate optic chiasm differ markedly from that revealed in rodents and carnivores.

Figure 1

Fibre alignment at the junction of the optic nerve with the optic chiasm in horizontal section. Optic fibres in this region were aligned in a parallel manner with no indication of any significant change in fibre order as seen in rodents or ferret. The pattern shown here is representative of the full medio-lateral and dorso-ventral extent of this region. Posterior is to the right and anterior to the left. Medial is down and lateral is up. The tissue is stained with p-phenylenediamine (Holland and Vaaland, 1995).

Figure 2

Low power micrograph of the junction of the optic nerve with the optic chiasm in horizontal section. The nerve ends approximately where the scale bar is located. The tissue has been stained to reveal collagen fibres which mark the limits of fascicules (example arrowed). The fascicular organisation of the retinofugal pathway is still present deep into the rostral chiasm. The presence of a fascicular configuration in the tissue would markedly restrict any significant changes in fibre order. Lateral is left and posterior is up.

Figure 3

Patterns of fibre order across the chiasmatic midline, approximately half way along the length of the chiasm in horizontal section. Here crossed fibres from the two eyes inter-digitate to produce a herringbone pattern extending along the length of the midline. Orientation, scale and staining are as in Figure 1.

Figure 4

In lateral chiasmatic regions, patterns of fibre order were markedly different from those across the midline. Here fibres remained aligned along a similar axis as that in the optic nerve and appeared to pass directly from the nerve towards the optic tract without approaching the midline. Orientation, scale and staining are as in Figure 1.

Figure 5

Anterograde labelling of the retinofugal pathway from one eye in horizontal section. The right optic nerve is heavily labelled with proline. However, towards the optic tract the label separates into two pathways. The larger crosses the midline, while a smaller component remains restricted to the right lateral chiasm and approaches the right optic tract without approaching the midline. The outline of the chiasm has been drawn onto regions of the figure which would otherwise not be revealed on such a low power photomicrograph.

Figure 6

A higher power picture of the region in which the crossed and the uncrossed projections divide in a section adjacent to that shown in Figure 6. This confirms that the uncrossed fibres originate laterally in the nerve (right side) and do not approach the midline, which is located on the left of the Figure.

Figure 7

A camera lucida drawing of retrogradely labelled fibres through the optic chiasm following a tracer injection into the right hemispheric pathway as seen in horizontal section. The tract on the right side adjacent to the injection is heavily labelled, but once the label entres the chiasm it divides into two pathways, a slightly larger crossed projection and a smaller uncrossed pathway. From the point at which the uncrossed pathway can be distinguished from the crossed, it remains confined laterally through the chiasm and into the optic nerve. The figure is presented from a camera lucida drawing because label could not be discerned along its pathway at low magnification.

Figure 8

A schematic representation of the uncrossed optic pathway through the optic chiasm in rodents/ferrets (A) and that described here in primate (B). In A there is a change in fibre order in the caudal optic nerve leading to the uncrossed fibres dispersing across this region and mixing with the crossed projection. These fibres then remain widespread across this hemi-chiasm before turning into the ipsilateral optic tract. This does not happen in primate. Here the uncrossed fibres entre the chiasm without significant changes in fibre order and remain confined laterally through the chiasm without approaching the midline.