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Biomedical subjects

M S Livingstone

Publications and source records attributed to M S Livingstone.

At least 19 recordsLinked to original sources

Receptive fields of disparity-selective neurons in macaque striate cortex.

To identify neuronal mechanisms underlying stereopsis, we characterized interactions between inputs from the two eyes in disparity-selective neurons in macaque V1. All disparity-selective cells showed suppressive interactions between the right and left eyes, and some showed facilitatory interactions. Disparity selectivity was narrower than the receptive-field width and was constant across the receptive field. Such position-invariant disparity selectivity is also found in anesthetized cat V1. Complex cells have been suggested to inherit their disparity selectivity from simple cells with receptive fields mismatched between the two eyes. However, we found no such antecedent disparity-tuned simple cells. We did find disparity-selective cells with some simple-cell characteristics, but surprisingly, they also showed position-invariant disparity selectivity rather than simple linear binocular interactions.

Animals

Mechanisms of direction selectivity in macaque V1.

Mechanisms underlying direction selectivity were studied in V1 of alert fixating macaque monkeys. Some direction-selective cells showed delayed asymmetric inhibition, some showed a shifting excitatory time course across the receptive field, and some showed both. Both the direction of the spatial offset of the inhibition and the direction of the shift in excitatory response time course correlated with the cells' preferred directionality. The delayed asymmetric inhibition may contribute to the shifting response time course. The data suggest that asymmetric inhibition is the major determinant for directionality in these cells, though both mechanisms could contribute. Based on this physiology, a simple, single-cell model is proposed, consistent with the known anatomy of some direction-selective cells.

Animals

Neuronal correlates of visibility and invisibility in the primate visual system.

A brief visual target stimulus may be rendered invisible if it is immediately preceded or followed by another stimulus. This class of illusions, known as visual masking, may allow insights into the neural mechanisms that underlie visual perception. We have therefore explored the temporal characteristics of masking illusions in humans, and compared them with corresponding neuronal responses in the primary visual cortex of awake and anesthetized monkeys. Stimulus parameters that in humans produce forward masking (in which the mask precedes the target) suppress the transient on-response to the target in monkey visual cortex. Those that produce backward masking (in which the mask comes after the target) inhibit the transient after-discharge, the excitatory response that occurs just after the disappearance of the target. These results suggest that, for targets that can be masked (those of short duration), the transient neuronal responses associated with onset and turning off of the target may be important in its visibility.

Animals

Ocular dominance columns in New World monkeys.

Squirrel monkeys normally lack ocular dominance columns in V1. This study shows that squirrel monkeys can exhibit clear ocular dominance columns if they are made strabismic within a few weeks of birth. Columns were seen only in layer 4C beta and were coarser than the overlying blob pattern in the same animal. In physiological recordings from layer 4C of a normal squirrel monkey, single units were mostly monocular, but units driven by the two eyes were intermixed. These results suggest that in squirrel monkeys activity-dependent mechanisms do normally segregate geniculate inputs from the two eyes, but on a much finer scale than in Old World primates. Strabismic owl monkeys also showed ocular dominance columns; normal owl monkeys showed variable expression. Because ocular dominance columns, when present in New World monkeys, tend to occur in later-maturing parts of layer 4C, I hypothesize that a difference in the relative timing of the maturation of geniculocortical inputs and intracortical lateral connectivity explains the variability of ocular dominance column expression in New World monkeys.

Animals

Differences between stereopsis, interocular correlation and binocularity.

In normal human subjects, evoked potentials in response to depth reversing two-color dynamic random-dot stereograms disappeared or were greatly reduced at equiluminance, whereas responses to shifts between patterns that were correlated and anticorrelated (for the two eyes) were, for most subjects, actually larger at equiluminance than at non-equiluminance. Responses were only slightly diminished at equiluminance to similar texture-shifting patterns that were identical to the two eyes. These results suggest that a significant fraction of cells with input from both eyes can respond to correlation/anticorrelation shifts, yet are not involved in stereopsis. Also, binocular rivalry may gate the responses of these binocular-nonstereoscopic units.

Depth Perception

Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex.

1. This work explores a mechanism that the brain may use for linking related percepts. It has been proposed that temporal relationships in the firing of neurons may be important in indicating how the stimuli that activate those neurons are related in the external world. Such temporal relationships cannot be seen with conventional receptive field mapping but require cross-correlation and auto-correlation analysis. 2. In the cat and the macaque monkey, cells with similar receptive field properties show correlated firing even when their receptive fields do not overlap. Here I report that in the squirrel monkey, as in the cat, pairs of cells < or = 5 mm apart can show correlated firing, and these correlations between pairs of cells are often stronger when they are stimulated by a single contour. This suggests that the correlations reflect not only permanent connections between cells with similar receptive fields, but in addition may encode information that the activating stimuli are continuous or part of a single object. I also find that, as in the cat, and contrary to some other reports on experiments in monkeys, the correlated firing is often rhythmic. These recordings further indicate that periods of rhythmicity are associated with stronger interneuronal synchrony, which is consistent with the hypothesis that recurrent feedback loops are involved in generating both. 3. Pairs of cells in the same cortical column, but at different depths also showed correlated firing, but with several milliseconds difference in timing between layers. This was true for cells at different depths within layer 2/3 and for pairs of cells in different layers (2/3 vs. 4B or 4C alpha), providing evidence for cross-talk between the magno- and parvocellular streams.

Anesthesia

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.

Animals

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.

Dark Adaptation

Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia.

Several behavioral studies have shown that developmental dyslexics do poorly in tests requiring rapid visual processing. In primates fast, low-contrast visual information is carried by the magnocellular subdivision of the visual pathway, and slow, high-contrast information is carried by the parvocellular division. In this study, we found that dyslexic subjects showed diminished visually evoked potentials to rapid, low-contrast stimuli but normal responses to slow or high-contrast stimuli. The abnormalities in the dyslexic subjects' evoked potentials were consistent with a defect in the magnocellular pathway at the level of visual area 1 or earlier. We then compared the lateral geniculate nuclei from five dyslexic brains to five control brains and found abnormalities in the magnocellular, but not the parvocellular, layers. Studies using auditory and somatosensory tests have shown that dyslexics do poorly in these modalities only when the tests require rapid discriminations. We therefore hypothesize that many cortical systems are similarly divided into a fast and a slow subdivision and that dyslexia specifically affects the fast subdivisions.

Adult

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.

Animals

Art, illusion and the visual system.

The verve of op art, the serenity of a pointillist painting and the 3-D puzzlement of an Escher print derive from the interplay of the art with the anatomy of the visual system. Color, shape and movement are each processed separately by different structures in the eye and brain and then are combined to produce the experience we call perception.

Art

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.

Animals

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.

Animals

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.

Animals

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.

Color Perception

Genetic dissection of Drosophila adenylate cyclase.

The Drosophila learning mutant rutabaga is missing calcium/calmodulin activation of adenylate cyclase (EC4.6.1.1). The mutation was mapped at a finer resolution to X chromosome bands 12F5-7. By comparing wild-type and mutant cyclase activities, the relative responsiveness of the calcium-sensitive and calcium-insensitive components to different ligands could be determined; the calcium-sensitive fraction of the total cyclase activity was significantly less responsive to guanyl nucleotides and monoamines. The results suggest that the component of cyclase activity that is stimulated by calcium/calmodulin, possibly a genetically distinct catalytic subunit, is not coupled to the G subunit or the G subunit/monoamine receptor complex.

Adenylyl Cyclases