Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys.

When viewing a stationary object, we unconsciously make small, involuntary eye movements or 'microsaccades'. If displacements of the retinal image are prevented, the image quickly fades from perception. To understand how microsaccades sustain perception, we studied their relationship to the firing of cells in primary visual cortex (V1). We tracked eye movements and recorded from V1 cells as macaque monkeys fixated. When an optimally oriented line was centered over a cell's receptive field, activity increased after microsaccades. Moreover, microsaccades were better correlated with bursts of spikes than with either single spikes or instantaneous firing rate. These findings may help explain maintenance of perception during normal visual fixation.

Stereopsis and binocularity in the squirrel monkey.

The squirrel monkey lacks anatomically demonstrable ocular dominance columns, and physiologically it has an ocular dominance distribution in V1 that is very different from that of macaques, with far fewer cells that strongly favor one eye over the other. We tested an alert squirrel monkey for physiological responses to stereoscopic stimuli by measuring evoked potentials in response to cytclopean patterns generated in dynamic random-dot stereograms. The monkey showed evoked responses both to changes in disparity and to shifts between correlation and uncorrelation between the two eyes. This result strongly suggests that the squirrel monkey can detect stereoscopic depth, which in turn casts some doubt on the assumption that ocular dominance columns bear an important relation to stereopsis.

Stereopsis and positional acuity under dark adaptation.

Though experience tells us we can perceive depth in dim light, it is not so obvious that one of the chief mechanisms for depth perception, stereopsis, is possible under scotopic conditions. The only studies on human stereopsis in the dark adapted state seem to be those of Nagel [(1902) Zeitschrift für Psychologie, 27, 264-266] and Mueller and Lloyd [(1948) Proceedings of the National Academy of Science, U.S.A., 34, 223-227], both of which used real objects or line stereograms. We tested stereopsis using both random-dot and line stereograms and, in agreement with these studies, found that stereopsis is indeed possible in dark adaptation. We also measured stereo acuity and positional acuity (both of which are examples of hyperacuity) and compared these with grating acuity at several levels of light and dark adaptation. At all illumination levels tested, acuities for stereopsis and relative line position were both higher than for grating acuity. As light levels decreased, positional and grating acuity declined in parallel fashion, whereas stereoacuity declined more steeply.

Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey.

We tested color and contrast sensitivity in the magnocellular and parvocellular subdivisions of the lateral geniculate body and in layers 2, 3, 4B, and 4C alpha of visual area 1 to obtain physiological data on the degree of segregation of the 2 pathways and on the fate of the color and contrast information as it is transmitted from the geniculate to the cortex. On average, magnocellular geniculate cells were much less responsive than parvocellular cells to shifts between 2 equiluminant colors. Nevertheless, many magnocellular cells (though not all) continued to give some response at equiluminance. As expected from previous studies, luminance contrast sensitivity differed markedly between magnocellular and parvocellular layers. In V-1, the properties of cells in the magnorecipient layers 4C alpha and 4B faithfully reflected the properties of magnocellular geniculate cells, showing no evidence of any parvocellular input. Like magnocellular geniculate cells, they showed high contrast sensitivity, and with color contrast stimuli they showed large response decrements at equiluminance. In the interblob regions of cortical layers 2 and 3, which anatomically appear to receive most of their inputs from parvorecipient layer 4C beta, contrast sensitivities of some of the cells were compatible with a predominantly parvocellular input. Other interblob cells had sensitivities intermediate between magno- and parvocellular geniculate cells, suggesting a possible contribution from the magnocellular system. Many cells in cortical layers 2 and 3 responded to color-contrast borders equally well at all relative brightnesses of the 2 colors, including equiluminance. We recorded from many direction- and disparity-selective cells in V-1: most of the direction-selective and all of the clearly stereo-selective cells were located in layer 4B.

Do the relative mapping densities of the magno- and parvocellular systems vary with eccentricity?

Two recent papers on the macaque visual system have concluded that in the lateral geniculate body the ratio of the number of cells in the magnocellular system to the number in the parvocellular system representing the same area of visual field increases by a factor of 20 between the fovea and the far periphery. In the primary visual cortex the relative cell densities of the 2 systems change little with eccentricity. These calculations therefore predict a 20-fold change in the relative densities of the inputs to the visual cortex from the 2 subdivisions of the lateral geniculate body. To test this prediction, we asked if the following vary with eccentricity: (1) the ratio of the number of magnocellular to parvocellular neurons innervating a given area of striate cortex and (2) the relative density, in the magno- and parvo-recipient sublaminae of layer 4C, of radioactivity transported from the eye to the cortex. Neither of these ratios showed any significant variation with eccentricity. These results seem to throw doubt on the contention that the ratio between the magnocellular and parvocellular layers of the number of cells per degree2 of visual field varies significantly with eccentricity.

Connections between layer 4B of area 17 and the thick cytochrome oxidase stripes of area 18 in the squirrel monkey.

In area 18 of the primate visual cortex, staining for the mitochondrial enzyme cytochrome oxidase reveals 3 types of stripelike subdivisions running perpendicular to the 17/18 border: thick, thin, and pale stripes. In a previous paper (Livingstone and Hubel, 1984), we described the anatomical connections with area 17 of 2 of these 3 subdivisions, but we did not have any conclusive information on the third subdivision, the thick stripes. Here we report that, in the squirrel monkey, the main input to the thick stripes from area 17 arises from layer 4B. Layer 4B receives its input from the magnocellular division of the lateral geniculate body by way of layer 4C alpha; the thick stripes therefore probably belong to the magnocellular subdivision of the visual pathway.

Segregation of form, color, and stereopsis in primate area 18.

Primate visual cortical area 18 (visual area 2), when stained for the enzyme cytochrome oxidase, shows a pattern of alternating dark and light stripes; in squirrel monkeys, the dark stripes are clearly of 2 alternating types, thick and thin. We have recorded from these 3 subdivisions in macaques and squirrel monkeys, and find that each has distinctive physiological properties: (1) Cells in one set of dark stripes, in squirrel monkeys the thin stripes, are not orientation-selective; a high proportion show color-opponency. (2) Cells in the other set of dark stripes (thick stripes) are orientation-selective; most of them are also selective for binocular disparity, suggesting that they are concerned with stereoscopic depth. (3) Cells in the pale stripes are also orientation-selective and more than half of them are end-stopped. Each of the 3 subdivisions receives a different input from area 17: the thin stripes from the blobs, the pale stripes from the interblobs, the thick stripes from layer 4B. The pale stripes are thus part of the parvocellular system, and the thick stripes part of the magnocellular system. The physiological properties of the cells in the thin and pale stripes reflect the properties of their antecedent cells in 17, but nevertheless exhibit differences that suggest the kinds of processing that might occur at this stage.

Psychophysical evidence for separate channels for the perception of form, color, movement, and depth.

Physiological and anatomical findings in the primate visual system, as well as clinical evidence in humans, suggest that different components of visual information processing are segregated into largely independent parallel pathways. Such a segregation leads to certain predictions about human vision. In this paper we describe psychophysical experiments on the interactions of color, form, depth, and movement in human perception, and we attempt to correlate these aspects of visual perception with the different subdivisions of the visual system.

Effects of monocular exposure to oriented lines on monkey striate cortex.

This study examines the extent to which the restriction of visual experience to lines of a single orientation influences the organization of the striate cortex in infant monkeys (Macaca mulatta). Previous studies of kittens raised with monocular exposure to a single line orientation have consistently shown the response preference of cells driven by that eye to be biased towards the experienced orientation. Studies of binocular exposure to restricted orientations have been equivocal. In the infant monkey cortex responses to oriented lines have virtually all the specificity of responses seen in the adult animal. In an effort to clarify the phenomenon and the mechanism by which orientation bias might be obtained, we examined the effects of monocular exposure to a restricted orientation in infant macaques. Three monkeys were used. Each monkey was raised with one open eye exposed to lines of a single orientation and one eye occluded by lid suture. As in other cases of monocular deprivation in either cat or monkey, few binocularly driven cells were recorded and the majority of cells were dominated by the open eye. Cells driven by the open eye had normal representation of all orientation preferences and there was no overall increase in the number of cells preferring the orientation to which the eye had been exposed. The cells dominated by the occluded eye, however, showed a lack of cells responding to orientations to which the open eye had been exposed. These findings suggest that a competitive mechanism operates between the two eyes to provide an orientation selective advantage to the open eye.

Complex-unoriented cells in a subregion of primate area 18.

In primates, both the primary and secondary visual cortical areas can be subdivided histologically by staining for the mitochondrial enzyme cytochrome oxidase. In the primary visual cortex (area 17, the first cortical receiving area for visual information) these histological differences correspond to functional subdivisions, cytochrome-dark regions being concerned with information about colour and cytochrome-light regions concerned with form. Here we report that the second visual area, area 18, which receives its main cortical input from area 17 (refs 7,8), similarly has functional subdivisions that correspond to the cytochrome oxidase staining pattern. In area 18 the segregation between form and colour is maintained, reinforcing our notion that form and colour information follow parallel pathways. The specific differences between cells in areas 17 and 18 suggest that a possible step in hierarchical information processing is spatial generalization, analogous to the difference between simple and complex cells.