Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions

Abstract

A series of experiments was carried out using 14C-2-deoxy-d-glucose (DG) in order to examine the functional architecture of macaque striate (primary visual) cortex. This paper describes the results of experiments on uptake during various baseline (or reference) conditions of visual stimulation (described below), and on differences in the functional architecture following monocular versus binocular viewing conditions. In binocular “baseline” experiments, monkeys were stimulated either (1) in the dark, (2) with a diffuse gray screen, or (3) with a very general visual stimulus composed of gratings of varied orientation and spatial frequency. In all of these conditions, DG uptake was found to be topographically uniform within all layers of parafoveal striate cortex. In monocular experiments that were otherwise similar, uptake was topographically uniform within the full extent of the eye dominance strip, in all layers. Certain other visual stimuli produce high uptake in the blobs, and still another set of visual stimuli (including high-spatial-frequency gratings) produce highest uptake between the blobs at parafoveal eccentricities, even in an unanesthetized, unparalyzed monkey. Eye movements per se had no obvious effect on striate DG uptake. Endogenous uptake in the blobs (relative to that in the interblobs) appears higher in the squirrel monkey than in the macaque. The pattern of DG uptake produced by binocular viewing was found to deviate in a number of ways from that expected by linearly summing the component monocular DG patterns. One of the most interesting deviations was an enhancement of the representation of visual field borders between stimuli differing from each other in texture, orientation, direction, etc. This “border enhancement” was confined to striate layers 1–3 (not appearing in any of the striate input layers), and it only appeared following binocular, but not monocular, viewing conditions. The border enhancement may be related to a suppression of DG uptake that occurs during binocular viewing conditions in layers 2 + 3 (and perhaps layers 1 and 4B), but not in layers 4Ca, 4Cb, 5 or 6. Another major class of binocular interaction was a spread of neural activity into the “unstimulated” ocular dominance strips following monocular stimulation. Such an effect was prominent in striate layer 4Ca, but it did not occur in layer 4Cb. This “binocular” spread of DG uptake into the inappropriate eye dominance strip in 4Ca may be related to the appearance of orientation tuning and orientation columns in that layer. No DG effects were seen that depended on the absolute disparity of visual stimuli in macaque striate cortex.

High-field fMRI unveils orientation columns in humans

“…Similar to the ODC maps in the monkey (26,33,34) and previous human anatomical (16,35) and functional (19,21) studies, preferences to right vs. left eye stimulation were observed as parallel bands modulating in 2-mm cycles (21). We have also demonstrated that such ODC maps are reproducible over days (21).…”

Coupling between neuronal activity and microcirculation: Implications for functional brain imaging

“…Moreover, those metabolic responses (here, glucose consumption) and neuronal activity were tightly co-localized (Sokoloff, 1981), as demonstrated by the high resolution of functional maps obtained in cat and monkey using the 2DG method (Kennedy et al, 1976;Tootell et al, 1981Tootell et al, , 1982Tootell et al, , 1988, as well as by staining selec- Figure 1. High-resolution functional optical imaging reveals the relationship between pinwheels "detection of orientated edges, shape processing…, ocular dominance columns "stereo vision, depth processing…, and cytochrome oxidase blobs "color vision… in the primary visual cortex of the macaque monkey.…”

“…Each module contains a complete set of about 60,000 neurons, processing the three features of orientation, depth, and color. ͑Modified from Bartfeld and Grinvald, 1992.͒ tively for cytochrome oxidase (Tootell et al, 1983(Tootell et al, , 1988, an enzyme that participates in the mitochondrial respiratory chain and thus accumulates in loci of increased metabolic activity. Spatial resolution of those methods easily attains the sub-millimeter scale, allowing the abovementioned cortical columns to be clearly visualized.…”

Curvature-processing network in macaque visual cortex

“…Familiar examples include the ocular dominance (39,40) and orientation columns in V1 (41), orientation-and colorsegregated columnar stripes in V2 (42,43), columns for direction of motion in MT/V5 (44), and subregions for object-related properties and face selectivity in the inferior temporal (IT) cortex (12,27,45). Presumably, columns/patches arise because such an architecture allows shorter axonal connections between neurons that require a great deal of interaction-i.e., functionally similar neurons.…”