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R B Tootell

Publications and source records attributed to R B Tootell.

At least 19 recordsLinked to original sources

Segregation of global and local motion processing in primate middle temporal visual area.

The early stages of primate visual processing appear to be divided up into several component parts so that, for example, colour, form and motion are analysed by anatomically distinct streams. We have found that further subspecialization occurs within the motion processing stream. Neurons representing two different kinds of information about visual motion are segregated in columnar fashion within the middle temporal area of the owl monkey. These columns can be distinguished by labelling with 2-deoxyglucose in response to large-field random-dot patterns. Neurons in lightly labelled interbands have receptive fields with antagonistic surrounds: the response to a centrally placed moving stimulus is suppressed by motion in the surround. Neurons in more densely labelled bands have surrounds that reinforce the centre response so that they integrate motion cues over large areas of the visual field. Interband cells carry information about local motion contrast that may be used to detect motion boundaries or to indicate retinal slip during visual tracking. Band cells encode information about global motion that might be useful for orienting the animal in its environment.

Animals

Magnetic resonance imaging mapping of brain function. Human visual cortex.

Magnetic resonance imaging (MRI) studies of human brain activity are described. Task-induced changes in brain cognitive state were measured using high-speed MRI techniques sensitive to changes in cerebral blood volume (CBV), blood flow (CBF), and blood oxygenation. These techniques were used to generate the first functional MRI maps of human task activation, by using a visual stimulus paradigm. The methodology of MRI brain mapping and results from the investigation of the functional organization and frequency response of human primary visual cortex (V1) are presented.

Brain Mapping

Spatial frequency tuning of single units in macaque supragranular striate cortex.

2-Deoxyglucose experiments have raised the possibility of a functional organization for spatial frequency in macaque striate cortex. To analyze this possibility with better spatial resolution, we made tangential microelectrode penetrations at constant eccentricity through supragranular striate cortex in 7 anesthetized, paralyzed macaque monkeys. We recorded from 121 single units. The data fell into two distinct populations with respect to mean preferred spatial frequency: (i) interblob cells (3.8 +/- 2.0 cycles/degree, n = 83) and (ii) blob cells (1.1 +/- 0.8 cycles/degree, n = 38; P less than 0.001). Beyond this, we found no evidence for an orderly mapping of spatial frequency optima. At blob-interblob borders, we observed abrupt shifts from low, relatively uniform spatial frequency optima (blobs) to higher optima that varied unsystematically (interblobs). The spatial frequency optima (low vs. high) and nature of the tuning curves (low-pass vs. band-pass) in blob vs. interblob cells correlate well with psychophysical measures of the same differences for the chrominance vs. luminance channels. These data are consistent with a functional subdivision of striate cortex in which blob cells carry information concerned predominantly with color and interblob neurons carry information important for form analysis.

Animals

Single-unit and 2-deoxyglucose studies of side inhibition in macaque striate cortex.

In the course of studies to map spatial frequency tuning of neurons in layers 2 and 3 of macaque striate cortex, we found that a high proportion (70%) of cells in the interblob regions responded poorly to full-field gratings, compared with responses to single bars, edges, or delimited gratings. This was most often due to side inhibition, in which increasing the number of cycles of a grating placed within the cell's receptive field causes progressive inhibition of response. Quantitative receptive-field mappings showed, however, that the inhibition can occur within the region activated by a bar, as well as beyond it. The inhibition appears to be orientation-selective, in that a surround grating was more effective at inhibiting the response to a center grating patch if it was of similar orientation. 2-Deoxyglucose experiments confirmed that side inhibition is very widespread in the interblobs of layers 2 and 3 and suggested that it is reduced or lacking in layers 4A through 6. Since layers 2 and 3 of striate cortex are the major source of cortical projections to area V2 and beyond, the prevalence of side stopping in these laminae has implications for theories of cortical visual function. Side-stopped interblob cells may be acting as "contour-pass filters" that filter out redundant information in textured or noisy surfaces, focusing subsequent form processing on contrasts corresponding to object boundaries.

Animals

Molecular differences among neurons reveal an organization of human visual cortex.

Monoclonal antibody Cat-301 recognizes a cell-surface proteoglycan on subsets of neurons in several areas of the cat and macaque monkey central nervous system. In striate and extrastriate visual cortex of the macaque, the distribution of Cat-301-positive neurons demonstrates features of cellular organization that correlate with previously described functional subdivisions. Here we show that Cat-301 recognizes an antigen in human cortex that is closely related, if not identical, to the antigen in laboratory animals. Further, we use Cat-301 to demonstrate an organization of molecularly defined neurons in primary and secondary visual cortex (cortical areas V1 and V2) of the human. The organization demonstrated with Cat-301 in human area V1 correlates with the organization of ocular dominance columns demonstrated by cytochrome oxidase histochemistry. The organization demonstrated with Cat-301 in human area V2 correlates with the thick stripes of the cytochrome oxidase pattern. The present observations provide evidence for a visual pathway in human cortex homologous to the magnocellular pathway in macaque, a pathway involved in processing the low-contrast, achromatic, and moving components of visual stimuli.

Animals

Functional anatomy of the second visual area (V2) in the macaque.

To study the functional organization of secondary visual cortex (V2) in the primate, 14C-2-deoxy-d-glucose (DG) was injected while macaque monkeys were shown specific visual stimuli. Wherever possible, patterns of DG uptake were compared with the position of dark and light cytochrome oxidase (cytox) stripes (Tootell et al., 1983). Often, the DG effects of 2 different stimuli were compared in the same hemisphere to eliminate ambiguities inherent in between-animal comparisons. Data were obtained from a large number of animals in conjunction with related DG studies in area V1 (primary visual or striate cortex). The following conclusions were reached: (1) in some macaque monkeys, dark cytox stripes were faint or absent. Although this could conceivably be due to poor staining technique, some evidence suggests that the lack of enzyme stripe pattern is real. In all animals, including those that showed poor or no cytox staining evidence for stripes, the functional architecture revealed by the DG was consistently present and robust. (2) Uniform gray stimuli produce a relatively uniform pattern and minimal stimulus-related DG uptake. (3) Eye movements per se produce some uptake in the V2 stripes. (4) Very generalized visual stimulation conditions (e.g., binocular stimulation with a grating of varied orientation and varied spatial frequency) produced a pattern of uptake that is greatest in both sets of dark cytox stripes and lighter in the light cytochrome stripes. (5) In both the DG and cytox results, the V2 "stripes" are more accurately described as stripe-shaped collections of patches. (6) In almost all cases, DG patterns were columnar in shape, extending from white matter to cortical surface. The boundaries of the columns were most sharply defined, and the contrast was highest, in layers 3B/4, becoming slightly more blurry and lower in contrast in other layers. Laminar differences between DG patterns in V2 were almost negligible, compared with the profound laminar differences in macaque V1. (7) There is no DG evidence for, and much against, the possibility of an ocular dominance architecture in V2. (8) There are orientation columns in macaque V2. DG-labeled orientation columns are spaced further apart than those in V1, by a factor of about 1.6, but the columns are not correspondingly wider. (9) Spatially diffuse variations in color produce high uptake confined, at least largely, to the thin cytox stripes. (10) There is evidence for spatially antagonistic color surrounds in color cells in the thin stripes.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

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

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.

Animals

Functional anatomy of macaque striate cortex. II. Retinotopic organization.

Macaque monkeys were shown retinotopically-specific visual stimuli during 14C-2-deoxy-d-glucose (DG) infusion in a study of the retinotopic organization of primary visual cortex (V1). In the central half of V1, the cortical magnification was found to be greater along the vertical than along the horizontal meridian, and overall magnification factors appeared to be scaled proportionate to brain size across different species. The cortical magnification factor (CMF) was found to reach a maximum of about 15 mm/deg at the representation of the fovea, at a point of acute curvature in the V1-V2 border. We find neither a duplication nor an overrepresentation of the vertical meridian. The magnification factor did not appear to be doubled in a direction perpendicular to the ocular dominance strips; it may not be increased at all. The DG borders in parvorecipient layer 4Cb were found to be as sharp as 140 micron (half-amplitude, half width), corresponding to a visual angle of less than 2' of arc at the eccentricity measured. In other layers (including magnorecipient layer 4Ca), the retinotopic borders are broader. The retinotopic spread of activity is greater when produced by a low-spatial-frequency grating than when produced by a high-spatial-frequency grating. Orientation-specific stimuli produced a pattern of activation that spread further than 1 mm across cortex in some layers. Some DG evidence suggests that the spread of functional activity is greater near the foveal representation than near 5 degrees eccentricity.

Animals

Functional anatomy of macaque striate cortex. III. Color.

Using spatially diffuse stimuli (or sinusoidal gratings of very low spatial frequency), levels of 14C-2-deoxy-d-glucose (DG) uptake produced by color-varying stimuli are much greater than those produced by luminance-varying stimuli in macaque striate cortex. Such a difference in DG results is consistent with previous psychophysical and electrophysiological results from man and monkey. In DG experiments with color-varying gratings of low and middle spatial frequencies, or with spatially diffuse color variations, DG uptake was highest in the cytochrome oxidase blobs, as was also seen with low-spatial-frequency luminance gratings. High-spatial-frequency, color-varying uptake patterns were shifted to cover both blob and interblob regions in a manner similar to that of the patterns obtained with middle-spatial-frequency luminance stimuli. However, in no instance did chromatic gratings produce uptake restricted to the interblob regions, as with the pattern seen with the highest-spatial-frequency luminance gratings. Thus, DG uptake is relatively higher in the interblob regions when comparing luminance with color-varying gratings that are otherwise similar. It was also possible to show DG evidence for receptive-field double-opponency in the upper-layer blobs, but color sensitivity in layer 4Cb appears single-opponent. The DG results suggest that color sensitivity is also high in the lower-layer (layers 5 + 6) blobs, and that many layer 5 receptive fields are double-opponent. Striate layers 4Ca and 4B-appeared color-insensitive in a wide variety of DG tests; this supports the idea of a color-insensitive stream running from the magnocellular LGN layers through striate layers 4Ca and 4B to extrastriate areas MT and V3. There was also a major effect due to wavelength: long and short wavelengths produced much more uptake than did middle wavelengths, even when all colors were equated for luminance and saturation. No variation with eccentricity was seen in cortical color sensitivity, at least between 0 degrees and 10 degrees.

Animals

Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams.

Macaque monkeys were shown achromatic gratings of various contrasts during 14C-2-deoxy-d-glucose (DG) infusion in order to measure the contrast sensitivity of different subdivisions of primary visual cortex. DG uptake is essentially saturated at stimulus contrasts of 50% and above, although the saturation contrast varies with layer and with different criteria. Following visual stimulation with gratings of 8% contrast, stimulus-driven uptake was relatively high in striate layer 4Ca (which receives primary input from the magnocellular LGN layers), but was absent in layer 4Cb (which receives primary input from the parvocellular layers). In this same (magnocellular-specific) stimulation condition, striate layers 4B, 4Ca, and 6 showed strong stimulus-induced DG uptake, and layers 2, 3, 4A, and 5 showed only light or negligible uptake. By comparison to other cases that were shown stimuli of systematically higher contrast, and to a wide variety of DG cases shown very different stimuli, it is evident that information derived from the magnocellular and parvocellular layers in the LGN remains partially, or largely, segregated in its passage through striate cortex, and projects in a still somewhat segregated fashion to different extrastriate areas. The sum of all available evidence suggests that the magnocellular information projects strongly through striate layers 4Ca, 4B, and 6, with moderate input into the blobs in layers 2 + 3, and to blob-aligned portions of layer 4A. Parvocellular-dominated regions of striate cortex include both the blob and interblob portions of layers 2 + 3, 4A, 4Cb, and 5. Because the major striate input to V2 arrives from striate layers 2 + 3, and because the major striate input to MT originates in layer 4B and 6, it appears that area V2 receives information derived largely from the parvocellular LGN layers, and that area MT receives information derived mainly from the magnocellular layers.

Animals

Functional anatomy of macaque striate cortex. V. Spatial frequency.

When macaque monkeys view achromatic, sinusoidal gratings of a single spatial frequency, the pattern of 14C-2-deoxy-d-glucose (DG) uptake produced by the gratings is shown to depend on the spatial frequency chosen. When a relatively high (5-7 cycles/deg) spatial frequency is shown binocularly at systematically varied orientations, uptake in parafoveal striate cortex is highest between the cytochrome oxidase blobs (that is, in the interblobs) in layers 1, 2, and 3. In layers 4B, 5, and 6, where the cytochrome oxidase blobs are faint or absent, DG uptake is highest in a periodic pattern that lies in register with the interblobs of layers 2 + 3. When the grating is, instead, of relatively low (1-1.5 cycles/deg) spatial frequency, DG uptake is highest in the blobs, in the blob-aligned portions of layers 1-4B, and in the lower-layer blobs as well. These variations in DG topography are confirmed in stimulus comparisons within a single hemisphere. Presumably, this shift in functional topography within the extra-granular layer is the primate homolog of "spatial frequency columns" shown earlier in the cat (Tootell et al., 1981; Silverman, 1984). In the well-differentiated architecture of primate striate cortex, laminar differences produced by high- versus low-spatial-frequency gratings are visible as well. Gratings of very high spatial frequency produce much higher uptake in 4Cb (which receives input from the parvocellular LGN layers) than in 4Ca (which gets its input from the magnocellular LGN layers). Gratings of low spatial frequency produce the converse result. Presumably, cells in the magnocellular LGN layers and/or in the magnocellular-dominated layer 4Ca have lower average spatial frequency tuning (larger receptive fields) than their counterparts in the parvocellular LGN and/or in striate layer 4Cb. The DG patterns produced by various spatial frequencies also vary with eccentricity, in a manner consistent with known, eccentricity-dependent variations of receptive-field size and spatial frequency tuning. Thus, gratings of a "middle"-spatial-frequency range (4-5 cycles/deg) produce high uptake in the blobs near the foveal representation and high uptake in the interblobs at more peripheral eccentricities, including 5 degrees. This shift in DG topography also includes the transition zone near 3 degrees, where the level of stimulus-driven uptake is as high in the blob regions as it is in interblob regions. Variations in uptake between layers 4Ca and 4Cb, as a function of eccentricity, shift in parallel with the changes in the upper-layer topography.

Animals

Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with 2-deoxyglucose autoradiography.

Staining the brain for cytochrome oxidase (CO) produces patterns which can resemble the patterns produced by 2-deoxyglucose (2-DG) autoradiography. In order to assess the differences between CO patterns of long-term metabolic activity and 2-DG patterns of short-term activity, comparisons should, ideally, be made on the same section. Consequently, we have made certain modifications in the standard CO histologic procedure which improve the stain and allow both 2-DG autoradiography and CO staining on the same section.

Animals

Picture processing techniques applied to autoradiographic studies of visual cortex.

Picture processing techniques are applied to 2-deoxyglucose autoradiographs of sections from striate cortex and to patterns resulting from staining these sections for cytochrome oxidase. This procedure allows computer identification of deoxyglucose active and inactive regions in the autoradiographs and cytochrome active and inactive regions in the stain patterns. Subsequently, the topographical relationship between these patterns can be quantitatively analyzed by means of overlap and density distribution measures and can be displayed using color enhanced graphics. The processing techniques have been applied in studies of the functional organization of visual cortex in primates. Computer graphic techniques have allowed implementation of split-field presentations of stimuli in deoxyglucose experiments. An application of this split-field technique for presenting multiple-stimuli to distinct parts of the visual field is described and an autoradiograph from a split-field experiment is shown.

Animals

Topography of cytochrome oxidase activity in owl monkey cortex.

In primate cortical tissue which has been stained for the mitochondrial enzyme cytochrome oxidase, a topographical pattern of regularly spaced blobs has been demonstrated in primary visual cortex (Hendrickson, A. E., S. P. Hunt, and J. -Y. Wu (1981) Nature 292: 605-607; Horton, J. C., and D. H. Hubel (1981) Nature 292: 762-764), and a pattern of stripes has been shown in secondary visual cortex (V2) as well (Livingstone, M. S., and D. H. Hubel (1982) Proc. Natl. Acad. Sci. U. S. A. 79: 6098-6101; Tootell, R. B. H., M. S. Silverman, E. Switkes, and R. L. De Valois (1982) Soc. Neurosci. Abstr. 8: 707). These regular cytoarchitectonic landmarks have proven extremely useful in parsing the functional and anatomical architecture of these two cortical areas. In order to look for similar landmarks in other cortical areas of a primate, we completely unfolded the cortical gray matter in the owl monkey (Aotus trivirgatus), sectioned it parallel with the flattened cortical surface, and stained the tissue for cytochrome oxidase. Distinctive cytochrome oxidase topographies were found in about seven different cortical areas. As in other primates, area V1 is characterized by blobs and area V2 is characterized by strips. In the owl monkey, area MT is characterized by an elaborate topography of dark staining in layers 1 to 4, interspersed with light blob-shaped regions, and partially surrounded by a dark ring. Many of these topographic inhomogeneities are also reflected in the lower layer myelination topography in MT. Visual area(s) VP/VA is characterized by an irregular or strip-like topography. In some animals, a distinctive topography can be seen in area DX, which is presumably equivalent to either area DM or DI. Primary auditory cortex stains very darkly, but the overall shape of area A is quite variable and the borders are indistinct. Somatosensory area 3B stains quite darkly with sharp borders, but again the overall shape of area 3B is different from that previously described.

Animals

Visual capacities of the owl monkey (Aotus trivirgatus): temporal contrast sensitivity.

Aotus monkeys were tested in a forced-choice discrimination task to determine their ability to discriminate sinusoidally flickering lights varying in temporal frequency and luminance contrast. Under conditions of moderate light adaptation this primate is maximally sensitive to lights flickering at 10 Hz while the highest frequency they can discriminate is about 42 Hz. At very low light levels (10(-5) ft L) maximum sensitivity is for 2.2--5 Hz flicker. The highest flicker rate that could be discriminated under these conditons was about 29 Hz. In comparison to humans tested in the same situation. Aotus monkeys show relatively lower sensitivity to temporal flicker under conditions of light adaptation but relatively higher sensitivity at very low light levels.

Adaptation, Ocular