Anatomical demonstration of ocular dominance columns in striate cortex of the squirrel monkey

Abstract

The squirrel monkey is the only primate reported to lack ocular dominance columns. Nothing anomalous about the visual capacity of squirrel monkeys has been found to explain their missing columns, leading to the suggestion that ocular dominance columns might be "an epiphenomenon, not serving any purpose" (Livingstone et al., 1995). Puzzled by the apparent lack of ocular dominance columns in squirrel monkeys, we made eye injections with transneuronal tracers in four normal squirrel monkeys. An irregular mosaic of columns, averaging 225 microns in width, was found throughout striate cortex. They were double-labeled by placing wheat germ agglutinin-horseradish peroxidase into the left eye and [3H]proline into the right eye. The tracers labeled opposite sets of interdigitating columns, proving they represent ocular dominance columns. The columns were much clearer in layer IVc alpha (magno-receiving) than IVc beta (parvo-receiving). In the lateral geniculate body, the parvo laminae showed extensive mixing of ocular inputs, suggesting that increased label spillover contributes to the blurred columns in layer IVc beta. The cytochrome oxidase (CO) patches were organized into distinct rows, but they bore no consistent relationship to the ocular dominance columns. These experiments indicate that ocular dominance columns are less well segregated in squirrel monkeys than macaques, but they are present. This fact is pertinent to a recent study reporting that ocular dominance columns are absent in normal squirrel monkeys, but induced to form by strabismus (Livingstone, 1996).

Fig. 1.

Brain of squirrel monkey 4 viewed from the rear after perfusion. The V1/V2 boundary (arrowheads) is visible to the naked eye because V1 is slightly darker. The portion of V1 exposed posteriorly on the brain surface is called the operculum (see shaded region in Fig. 3C). Most of V1 is hidden from view, located along the medial surface of the occipital lobe or folded within the calcarine fissure.

Fig. 2.

A, Section from the peripheral left striate cortex of monkey 1 through layer IVcα showing the distribution of WGA-HRP after injection into the right eye. The tracer is organized into a complex mosaic of columns, interrupted by unlabeled gaps. Arrowheads show key blood vessels used for section alignment in panels A–D. B, CO-stained section cut 210 μm more superficially from the same block, showing the array of patches in layer III. C, Adjacent section cut 35 μm deeper than B, showing distinct patches of WGA-HRP, except in the center where the label becomes more confluent as the section grazes the “honeycomb” in layer IVa. All the patches are labeled equally after tracer injection into just one eye, and each labeled patch superimposes on a CO patch in C.D, Comparison between the labeled columns inA, which have been reinforced in white, and the patches in C, which have been outlined inblack. Overall, there is no consistent alignment between the columns and patches, although occasionally they coincide. The mean column width is 220 μm, whereas the patches are spaced ∼500–700 μm apart.

Fig. 3.

A, Montage of WGA-HRP label from the left eye in layer IVcα of the right cortex of monkey 4. Faint columns are visible throughout most of the montage. Therectangle delineates the portion of the flat-mount shown at higher power in Figure 4. B, Montage of autoradiographs through layer IVcα showing columns of [³H]proline label from the right eye. C, Sketch of the columns labeled in V1, prepared by combining the WGA-HRP data in A and the proline data in B. The contrast of the columns in B was reversed so that theblack columns throughout the figure represent the ocular dominance columns of the right eye. They form an irregular array of short stripes and islands, with a mean diameter of 225 μm. Theshaded area corresponds to the operculum, grossly visible in Figure 1, representing the central 3–4°. Figure 3continues.

Fig. 3.

A, Montage of WGA-HRP label from the left eye in layer IVcα of the right cortex of monkey 4. Faint columns are visible throughout most of the montage. Therectangle delineates the portion of the flat-mount shown at higher power in Figure 4. B, Montage of autoradiographs through layer IVcα showing columns of [³H]proline label from the right eye. C, Sketch of the columns labeled in V1, prepared by combining the WGA-HRP data in A and the proline data in B. The contrast of the columns in B was reversed so that theblack columns throughout the figure represent the ocular dominance columns of the right eye. They form an irregular array of short stripes and islands, with a mean diameter of 225 μm. Theshaded area corresponds to the operculum, grossly visible in Figure 1, representing the central 3–4°. Figure 3continues.

Fig. 4.

A, Single section outlined by therectangle in Figure 3A passing mostly through layer IVcα showing columns of yellow WGA-HRP reaction product from the left eye. At this magnification, the blood vessels used in each panel for section alignment are visible (arrowheads). B, Single autoradiograph from an adjacent section showing columns of [³H]proline label from the right eye. C, Single section cut 245 μm more superficially from the same block showing the CO patches in layer III. A glimpse of the V1/V2 border is seen at the top left (arrow). D, Schematic diagram showing columns of WGA-HRP label (A) inyellow and columns of [³H]proline (B) in blue. The two patterns dovetail, indicating that they represent alternating inputs from the left and right eyes, respectively. The blobs drawn inbrownish-orange represent the CO patches inC. We found no correspondence between patches and ocular dominance columns.

Fig. 5.

Nissl sections of the left (A) and right (B) lateral geniculate bodies showing a single fused dorsal parvocellular mass, without fibrous interlaminar zones to limit spillover of label. The two ventral magnocellular laminae are separated by a fibrous interlaminar zone (arrows). Autoradiographs of these sections are shown in C andD. Laminae 3 and 4 on each side are comprised of an archipelago of labeled and unlabeled islands, partly merging these laminae and increasing the opportunity for label spillover. The autoradiographs were stripped of their emulsion and stained with cresyl violet to prepare the Nissl sections. Scale bar, 1 mm.

Fig. 6.

A, Single CO section from the right cortex of monkey 4, the same flat-mount illustrated in Figure 3, showing the patches in the upper layers. The CO stripes in V2 are also visible. B, Sketch of the patches in V1 and the stripes in V2. There are 2857 patches organized into rows, perpendicular to the V1/V2 border (arrows). The density of patches is uniform throughout V1. In V2, the thin stripes are darker than the thick stripes.