In addition to showing that ocular dominance is organized in slabs and that orientation preferences are organized in linear sequences likely to reflect slabs, Hubel and Wiesel (1974a) discussed the intriguing possibility that slabs of orientation might intersect slabs of ocular dominance at some consistent angle. Advances in optical imaging now make it possible to test this possibility directly. When maps of orientation are analyzed quantitatively, they appear to arise from a combination of at least two competing themes: one where orientation preferences change linearly along straight axes, remaining constant along perpendicular axes and forming iso-orientation slabs along the way, and one where orientation preferences change continuously along circular axes, remaining constant along radial axes and forming singularities at the centers of the spaces enclosed. When orientation patterns are compared with ocular dominance patterns from the same cortical regions, quantitative measures reveal (1) that singularities tend to lie at the centers of ocular dominance columns, (2) that linear zones (arising where orientation preferences change along straight axes) tend to lie at the edges of ocular dominance columns, and (3) that the short iso-orientation bands within each linear zone tend to intersect the borders of ocular dominance slabs at angles of approximately 90 degrees.

We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracelhrlarly before being filled with HRP. Light microscope and computer reconstructions of filled processes reveal highly stereotyped patterns of arborization and suggest that there are at least five discrete populations of lateral geniculate nucleus (LGN) afferent axon: (1) those to layer 4Cp, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4Ca) but which have not been shown to project to other laminae; (2) afferents to layer 4A, which in some cases send fine ascending collaterals into layer 2-3 and which do not, apparently, send collaterals to other laminae; (3) afferents to layer 1, which are fine, extend over large distances horizontally, and send collaterals to layer 6A; (4) afferents to the lower two-thirds of layer 4Ca, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4Ca, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4Cp (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4Ca all had transient, broad band and highly contrast-sensitive receptive fields. These properties are consistent with derivations from somata in the parvocellular and magnocellular divisions of the LGN, respectively. Afferents to 4Ca were found to cover approximately 6 times as much surface area as afferents to 4Cp. The preterminal trunks of all axons were found to follow tortuous paths through the neuropil-paths that may derive from axon segregation during development. The wide ranging, patchy distributions of single afferents in 4C~u suggest that individual 4& axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4Ca axon was mapped against the transneuronally determined pattern of ocular dominance, three separate patches of terminal boutons were indeed found to coincide with the bands of one eye.The primate visual system is characterized by successive and discrete transformations in the neural representation of visual space. One such transformation occurs between the lateral geniculate nucleus (LGN) and cells in the thalamo-recipient laminae of striate cortex. Even though the receptive fields of cells in layer 4C-the layer that receives most of the LGN input-lack orientation selectivity and to some extent resemble those of the LGN, the transfer of information seems not to occur in

Numerous highly angled electrode penetrations through the opercular region of macaque striate cortex reveal that layers 4A, 4C alpha, and 4C beta--the primary input sublaminae for axons from the lateral geniculate nucleus (LGN)--are retinotopically organized on a fine scale and populated mostly by monocularly driven cells having small receptive fields and lacking orientation selectivity. Layer 4B, which does not receive a direct thalamic input, contains orientationally selective cells, and many of these are also direction selective. To a significant degree the response properties of cells in layers 4C alpha and 4C beta reflect the response properties of their respective afferent inputs, from the magno- and parvocellular laminae of the LGN. Accordingly, cells in layer 4C alpha have lower contrast thresholds and larger minimum response fields than do the cells in layer 4C beta. In contrast to this clear-cut separation, the cells of layer 4A (whose major source of direct LGN input arises from the parvocellular layers) exhibit both high and low contrast thresholds. With regard to the precision of retinotopic mapping that is seen in lamina 4C, it is noteworthy that there is substantial overlap among the minimum response fields of neighboring neurons. Due to a larger mean receptive field size, this overlap is greater in layer 4C alpha than it is in 4C beta. In either sublamina, however, the minimum cortical distance that separates different and nonoverlapping parts of the visual field corresponds closely--within a factor of 2--to the known arborizational spreads of single geniculate afferents.

We have studied the intrinsic organization of macaque striate cortex by tracing the pattern of horseradish peroxidase (HFiP)-labeled axons and cell bodies produced by microinjections of HRP into single cortical laminae. Both anterograde and retrograde transport results were used to examine: (1) the pattern of projections from lamina 4C to the superficial layers; (2) the projection from lamina 4C to deeper cortical layers; and (3) the projections to lamina 4C from other cortical laminae.Laminae 4C0 and 4Cfi differ in their pattern of projections to the superficial layers of striate cortex. Axons from neurons in lamina 4C/3 ascend through lamina 48 without giving off collaterals and terminate in lamina 4A and in the base of lamina 3. By contrast, axons from neurons in lamina 4Ccu terminate in lamina 48 and less densely in the 4A/3B region.The projection from lamina 4Cp to lamina 4A is particularly dense and is distributed in a patchy fashion immediately above each injection site. The projection from lamina 4Cp to lamina 38 appears less dense and more widespread; we estimate that individual 4Cj3 axons may spread laterally for more than 400 pm. Furthermore, the pattern of HRP-labeled cell bodies in lamina 4Cj3 following injections into laminae 4A and 3B provides evidence for a subdivision within SC& These injections always produce a large number of labeled neurons in the upper part of lamina 4C& whereas the lower portion contains few labeled neurons that are located immediately under the center of the injection site.Both lamina 4& and lamina 4Cp also contribute less dense projections to the deeper layers of cortex. Lamina 4Cj3 projects mainly to lamina 6, whereas lamina 4Ca contributes axon terminals to both lamina 5A and lamina 6.Neurons in lamina 6 provide the bulk of the intracortical projections to lamina 4C. These results confirm or refine many conclusions about intrinsic connections of striate cortex drawn from Golgi material and suggest new patterns of connections not suspected from previous work.The key to understanding cortical function lies in establishing the way in which inputs from the thalamus and other brainstem regions are transformed into the response properties of output neurons. Although we are still far from understanding the nature of this complex process, it is clear that the achievement of this objective will require a detailed knowledge of intracortical circuitry and the relation of this circuitry to afferent and efferent cell groups.The macaque striate cortex provides an excellent system for the study of intracortical circuitry because of the remarkable degree of lamlnar segregation of different afferent and efferent pathways. For example, inputs from the magnocellular and parvocellular laminae of the lateral geniculate nucleus (LGN) terminate in separate and largely nonoverlaping tiers within lamina 4C with magnocellular afferents occupying a more superficial position (lamina 4Ca) than parvocellular ones (lamina 4Cp) (Hubel and Wiesel, 1972; Hendrickson et al., 1978). Likewise, the...

Differential images of ocular dominance, acquired by comparing responses to the two eyes, reveal dark and light bands where cortical cells are dominated by the right and left eyes. These include most (but not all) histochemically stained cytochrome oxidase blobs in their centers. Differential images of orientation, acquired by comparing responses to orthogonal orientations, reveal dark and light bands that are reminiscent of the "orientation columns" reported earlier, on the basis of 2-deoxyglucose (2DG) autoradiograms (Hubel et al., 1978). However, they are shorter and more fragmented because they do not include regions lacking selectivity for orientation. Even though these "bands" derive from orientation-selective areas, comparisons with differential images of other orientations reveal that regions along their centers prefer different orientations. Hence, the orientation preferences inferred from "bands" in single differential images, or single 2DG autoradiograms, are not necessarily incorrect. Interactions between ocular dominance and orientation were investigated by comparing differential images of orientation obtained with binocular and monocular stimulation, as well as by comparing differential images of ocular dominance obtained with different orientations. In both cases, the elicited interactions were minimal, indicating a remarkable and unexpected independence that subsequent experiments revealed arises, at least in part, from a lateral segregation of regions most selective for one eye and regions most selective for one orientation, in the centers and edges of ocular dominance columns. Since this can also be viewed as a lateral correlation between binocularity and orientation selectivity, it fits with the simultaneous emergence of these properties in layers receiving input from layer 4c, and suggests that each of these properties requires the other.