Striate Cortex Of Macaque Monkey Research Articles

Neuronal Selectivity and Local Map Structure in Visual Cortex

The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development.

Effects of experimental strabismus on the architecture of macaque monkey striate cortex.

Strabismus, a misalignment of the eyes, results in a loss of binocular visual function in humans. The effects are similar in monkeys, where a loss of binocular convergence onto single cortical neurons is always found. Changes in the anatomical organization of primary visual cortex (V1) may be associated with these physiological deficits, yet few have been reported. We examined the distributions of several anatomical markers in V1 of two experimentally strabismic Macaca nemestrina monkeys. Staining patterns in tangential sections were related to the ocular dominance (OD) column structure as deduced from cytochrome oxidase (CO) staining. CO staining appears roughly normal in the superficial layers, but in layer 4C, one eye's columns were pale. Thin, dark stripes falling near OD column borders are evident in Nissl-stained sections in all layers and in immunoreactivity for calbindin, especially in layers 3 and 4B. The monoclonal antibody SMI32, which labels a neurofilament protein found in pyramidal cells, is reduced in one eye's columns and absent at OD column borders. The pale SMI32 columns are those that are dark with CO in layer 4. Gallyas staining for myelin reveals thin stripes through layers 2-5; the dark stripes fall at OD column centers. All these changes appear to be related to the loss of binocularity in cortical neurons, which has its most profound effects near OD column borders.

Termination of the geniculocortical projection in the striate cortex of macaque monkey: A quantitative immunoelectron microscopic study

The goal of this present study was to derive a new estimate of the synaptic contribution of the dorsal lateral geniculate nucleus (dLGN) to the subdivisions of its main recipient layer, layer 4C, of striate cortex of macaque monkey. The projection from the dLGN and its terminal boutons within layer 4C were visualized by immunodetection of the calcium binding protein, parvalbumin (PV), which is expressed in relay cells of the dLGN. The proportion of asymmetric synapses formed by PV-positive boutons within the alpha and beta sublayers of 4C was estimated by using a nonbiased stereological counting method. The proportion of asymmetric synapses contributed by the PV-positive boutons to layer 4Calpha is 8.7%; to 4Cbeta is 6.9%. Assuming all the PV-positive asymmetric synapses derive from the dLGN relay cells, this gives a ratio of dLGN synapses per neuron of 192 in layer 4Calpha and 128 in layer 4Cbeta. Thus, the recurrent excitatory input from neighboring cortical neurons must play an important part in responses of the neurons lying at the input stage of the cortical circuit.

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

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

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.

The temporal correlation hypothesis of visual feature integration: still alive and well.

The temporal correlation hypothesis of visual feature integration: still alive and well.

Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex.

To help understand the role of long-range, clustered lateral connections in the superficial layers of macaque striate cortex (area V1), we have examined the relationship of the patterns of intrinsic connections to cytochrome oxidase (CO) blobs, interblobs, and ocular dominance (OD) bands, using biocytin based neuroanatomical tracing, CO histochemistry, and optical imaging. Microinjections of biocytin in layer 3 resulted in an asymmetric field (average anisotropy of 1.8; maximum spread--3.7 mm) of labeled axon terminal clusters in layers 1-3, with the longer axis of the label spread oriented orthogonal to the rows of blobs and imaged OD stripes, parallel to the V1/V2 border. These labeled terminal patches (n = 186) from either blob or interblob injections (n = 20) revealed a 71% (132 out of 186) commitment of patches to the same compartment as the injection site; 11% (20 out of 186) to the opposite compartment, and 18% (34 out of 186) to borders of blob-interblob compartments, indicating that the connectivity pattern is not strictly blob to blob, or interblob to interblob (p < 0.005; chi(2)). In injections placed within single OD domains (n = 11), 54% of the resulting labeled terminal patches (43 out of 79) fell into the same OD territories as the injection sites, 28% (22 out of 79) into the opposite OD regions, and 18% (14 out of 79) on borders, showing some connectional bias toward same-eye compartments (p < 0.02; ANOVA). Individual injection cases, however, varied in the degree (50-100% for CO patterns, 22-100% for OD patterns) to which they showed same-compartment connectivity. These results reveal that while connectivity between similar compartments predominates (e.g., blob to blob, right eye column to right eye column), interactions do occur between functionally different regions.

Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs

The striate cortex of macaque monkeys contains an array of patches which stain heavily for the enzyme cytochrome oxidase (CO blobs). Cells inside and outside these blobs are often described as belonging to two distinct populations or streams. In order to better understand the function of the CO blobs, we measured the contrast sensitivity and spatial frequency response of single neurons in and around the CO blobs. Density profiles of each blob were assessed using a new quantitative method, and correlations of local CO density with the physiology were noted. We found that the CO density dropped off gradually with distance from blob centers: in a typical blob the CO density dropped from 75% to 25% over 100 μm. Recordings were confined to cortical layers 2/3. Most neurons in these layers have poor contrast sensitivity, similar to that of the parvocellular neurons in the lateral geniculate nucleus. However, in a small proportion of layers 2/3 neurons we found higher contrast sensitivity, similar to that of the magnocellular neurons. These neurons were found to cluster near blob centers. This finding is consistent with (indirect) parvocellular input spread uniformly throughout layers 2/3, and (indirect) magnocellular input focused on CO blobs. We also measured spatial tuning curves for both single units and multiple unit activity. In agreement with other workers we found that the optimal spatial frequencies of cells near blob centers were low (median 2.8 c/deg), while the optimal frequencies of cells in the interblob regions were spread over a wide range of spatial frequencies. The high cut-off spatial frequency of multi-unit activity increased with distance from blob centers. We found no correlation between spatial bandwidth and distance from blob centers. All measured physiological properties varied gradually with distance from CO blob centers. This suggests that the view of blob cells subserving visual functions which are entirely distinct from non-blob cells may have to be reevaluated.

Visual response latencies in striate cortex of the macaque monkey.

1. Many lines of evidence suggest that signals relayed by the magnocellular and parvocellular subdivisions of the primate lateral geniculate nucleus (LGN) maintain their segregation in cortical processing. We have examined two response properties of units in the striate cortex of macaque monkeys, latency and transience, with the goal of assessing whether they might be used to infer specific geniculate contributions. Recordings were made from 298 isolated units and 1,129 multiunit sites in the striate cortex in four monkeys. Excitotoxin lesions that selectively affected one or the other LGN subdivision were made in three animals to demonstrate directly the magnocellular and parvocellular contributions. An additional 435 single units and 551 multiunit sites were recorded after the ablations. 2. Most units in striate cortex had visual response latencies in the range of 30-50 ms under the stimulus conditions used. The earliest neuronal responses in striate cortex differed appreciably between individuals. The shortest latency recorded in the four animals ranged from 20 to 31 ms. Comparable values were obtained from both single unit and multiunit sites. After lesions were made in the magnocellular subdivision of the LGN in two animals, the shortest response latencies were 7 and 10 ms later than before the ablations. A larger lesion in the parvocellular subdivision of another animal produced no such shift. Thus it appears that the first 7-10 ms of cortical activation can be attributed to activation relayed by the magnocellular layers of the LGN. 3. The units with the shortest latencies were all found in layers 4C or 6 and their responses were among the most transient in striate cortex. Furthermore, their responses all showed a pronounced periodicity at a frequency of 50-100 Hz. This periodicity was stimulus locked, and the responses of all short-latency units oscillated in phase. 4. An index of response transience was computed for the units recorded in striate cortex. The distribution of this index was unimodal and gave no suggestion of distinct contributions from the geniculate subdivisions. Magnocellular and the parvocellular lesions affected the overall transience of responses in striate cortex. The changes, however, were very small; extremely transient responses and extremely sustained responses survived both types of lesions. 5. A characteristic profile was observed in the response latencies in superficial layers. Latencies appeared to increase monotonically from layer 4 toward the surface of cortex, with the most superficial neurons not becoming active until 15 ms after responses were observed in layer 4C.(ABSTRACT TRUNCATED AT 400 WORDS)

Development of synapses in macaque monkey striate cortex

A quantitative electron-microscopic (EM) analysis of the development of synaptic density (number of synapses/100 microns2 neuropil) has been done in primary visual cortex (striate, area 17) of the Old World monkey Macaca nemestrina. A comparative EM morphological study of developing synaptic contacts also was done in the same tissue. We find that a few immature synaptic contacts are present at fetal (F) 75 days either in the marginal zone, which becomes layer 1, or in the deepest portion of the cortical plate, the future layer 6. At F90-140 days synaptic contacts are found throughout the cortical plate, but their density remains higher in lower cortical layers. By F140 days synaptic density averaged for all layers (10.9) is three times higher than at F90 days. Just before and after birth, synaptic density rises very rapidly to peak at postnatal (P) 12 weeks (63) and then declines slowly to reach adult values (37.7) between 2-6 years. This pattern was further tested by comparing synaptic density in layer 2 which contains the last cells generated in the striate cortex to that in layer 6 which contains the first cells generated in the striate cortex. Layer 6 contained the first synapses, and had a higher density up to F140 days (an "inside-to-outside" distribution). Synaptic density was equal in the two layers at F152 days and P2 days, but by P12 weeks synaptic density in layer 2 was 27% higher than that in layer 6 (an "outside-to-inside" distribution). After P12 weeks, the synaptic density declined 51% in layer 2 and 21% in layer 6 so that both layers achieved similar densities by P6 years. A light and EM comparison of neuropil and synaptic contact morphology finds that, at each age up to birth, synapses in layer 2 are generally less mature than those in layer 6, but these differences disappear shortly after birth. Between P6-24 weeks, synaptic contacts throughout the cortex acquire a mature morphology that clearly differentiates between asymmetric and symmetric types, although asymmetric contacts continue to acquire more postsynaptic density until adulthood. This complex developmental pattern suggests a sequence for synaptic developments which is more related to neuron birthdate than to the arrival of extrinsic pathways or developmental events occurring in specific laminae.

Coverage and the design of striate cortex

Hubel and Wiesel (1977) suggested that ocular dominance and orientation columns in the macaque monkey striate cortex might be bands of uniform width that intersected orthogonally. They pointed out that if this were the case, there would be an equal allocation of cells of different orientation preference to each eye and to each point in visual space. However, orientation and ocular dominance columns have a more complex structural organization than is implied by this model: for example, iso-orientation domains do not intersect ocular dominance stripes at right angles and the two columnar systems have different periodicities. This raises the question as to how well the striate cortex manages to allocate equal numbers of neurons of different orientation preference to each eye and to each region of visual space, a factor referred to here as coverage. This paper defines a measure of uniformity of coverage, c', and investigates its dependence on several different parameters of columnar organisation. Calculations were done first using a simplified one-dimensional model of orientation and ocular dominance columns and were then repeated using more realistic two-dimensional models, generated with the algorithms described in the preceding paper (Swindale 1991). Factors investigated include the relative periodicities of the two columnar systems, the size of the cortical point image, the width of orientation tuning curves, whether columns are spatially anisotropic or not, and the role of the structural relationships between columns described by Blasdel and Salama (1986). The results demonstrate that coverage is most uniform when orientation hypercolumns are about half the size of ocular dominance hypercolumns. Coverage is most uneven when the hypercolumns are the same size, unless they are related in the way described by Blasdel and Salama, in which case coverage gets only slightly worse as the size ratio (ori/od) increases above 0.5. The minimum diameter of cortical point image that ensures reasonably uniform coverage is about twice the size of an ocular dominance hypercolumn i.e. about 1.5-2.0 mm.

Contrast adaptation in striate cortex of macaque

We have characterized the contrast-response relationships for simple and complex cells in striate cortex of macaque monkey, before and during adaptation to high-contrast sinusoidal gratings of the optimal spatial-frequency and orientation. Adaptation brings about systematic changes in the steepness of contrast-response curves and in the effective contrast of stimuli. Adaptation reduces the detectability of low-contrast gratings by almost a factor of three, but by extending the operating range of most cells it appears to improve the discriminability of high-contrast stimuli that previously gave rise to responses of saturating amplitude.

Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey

We have used 2-deoxy-D-[14C]glucose (2-DG) autoradiography and cytochrome oxidase histochemistry to examine background and stimulus-induced patterns of metabolic activity in monkey striate cortex. In squirrel monkeys (Saimiri sciureus) that binocularly or monocularly viewed diffuse white light or binocularly viewed bars of many orientations and spatial frequencies, 2-DG consumption was not uniform across the cortex but consisted of regularly spaced radial zones of high uptake. The zones extended through all laminae except IVc beta and, when viewed tangentially, formed separate patches 500 microns apart. The cytochrome oxidase stain in these animals also revealed patches of high metabolism which coincided with the 2-DG patches. Squirrel monkeys binocularly viewing vertical stripes showed parallel bands of increased 2-DG uptake in the cortex, while the cytochrome label in these animals remained patchy. When monkeys were kept in the dark during 2-DG exposure, 2-DG-labeled patches were not seen but cytochrome oxidase-positive patches remained. In macaque (Macaca nemestrina) monkeys, binocular stimulation with many orientations and spatial frequencies produced radial zones of high 2-DG uptake in layers I to IVa and VI. When viewed tangentially, these zones formed a dots-in-rows pattern with a spacing of 350 X 500 microns; cytochrome oxidase staining produced an identical pattern. Macaca differed from Saimiri in that monocular stimulation labeled alternate rows. These results indicate that there are radial zones of high background metabolism across squirrel and macaque monkey striate cortex. In Saimiri these zones do not appear to be related to an eye dominance system, while in Macaca they do. The presence of these zones of high metabolism may complicate the interpretation of 2-DG autoradiographs that result from specific visual stimuli.

Structure of columns in monkey striate cortex induced by luminant-contrast and color-contrast stimulation.

Color and black and white line stimulation produce qualitatively and quantitatively different 2-deoxy[14C]glucose column patterns in the striate cortex of macaque monkeys. Microdensitometry of these stimulus-dependent columns reveals interlaminar density differences that serve as a signature for the stimulus conditions which produced them. Such columns are individually distinct and form a three-dimensional mosaic throughout striate cortex.

Postnatal changes in the number of astrocytes, oligodendrocytes, and microglia in the visual cortex (area 17) of the macaque monkey: a stereological analysis in normal and monocularly deprived animals.

The numerical densities (Nv) of astrocytes, oligodendrocytes, and microglia were measured in individual laminae of the striate cortex of macaque monkeys ranging in age from newborn to adult. Using measurements of cortical thickness and surface area, the total number of cells in the striate cortex of one hemisphere was derived for each glial cell type. Normal monkeys were compared at 3 months and 6 months of age to animals reared from birth with a monocular eyelid suture. No significant differences were observed between normal and monocularly deprived monkeys. The combined data from these groups, however, demonstrated several significant developmental changes. The Nv of astrocytes decreased from birth to 6 months of age and subsequently increased in the adult. The greatest changes were seen in the more superficial laminae. These changes, however, were only a response to a substantial overshoot in cortical volume at six months: the total number of astrocytes in the striate cortex did not change. There was a tenfold increase in both the Nv and the total number of oligodendrocytes from birth to maturity with a corresponding increase in the density of myelinated axons. The greatest changes were observed in the deeper laminae. The total number of microglia remained relatively constant from birth to 6 months of age. There was a 55% reduction in the number of microglia in the adult, although statistical analysis indicated that this decrease was only of borderline significance. The possible relationships between these postnatal changes in glial cell numbers and the development of neuronal connectivity are discussed.

The orientation and direction selectivity of cells in macaque visual cortex

Quantitative data are presented on the orientation and direction specificity of the responses of cells in macaque monkey striate cortex. There is a bimodal distribution of direction-specific and nondirection-specific cells, with similar orientation tuning in each class. Cells range in orientation bandwidth at half amplitude from 6° to 360° (i.e. no orientation tuning), with a median near 40°. Fovealparafoveal and simple-complex subsamples show similar ranges of orientation bandwidths as well as similar medians (the bandwidths being somewhat broader than those found in cat cortex). The foveal subsample and a high-spatial-frequency subsample have more horizontal and vertical optimal orientations than oblique ones. Most cells show inhibition to some orientations, as well as excitation to others. Minimum-response orientations are generally less than 90° from the optimal orientation—indicating maximum inhibition adjacent to the excitatory orientations. Three simple receptive field models are shown to differ in their abilities to account for these results.

A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys.

In a previous Golgi study (Lund et al., '77) which examined the development of the macaque monkey striate cortex (area 17) it was observed that the dendrites of neurons within the visual cortex show a marked increase in the number of spines on their surface during the first eight weeks of postnatal life. The qualitative observation was also made that all neurons then showed a marked decrease in spine numbers by the time the animal was adult. Since these spines are known to be sites of synaptic contact, changes in their numbers may reflect changes in synapse populations on these neurons. This study examines quantitatively spine frequency and total dendritic development of Golgi impregnated neurons in monkeys ranging in age from 145 days gestation to adult. Four cell types were studied: spiny stellate neurons from laminae IVCalpha and IVCbeta and pyramidal neurons with soma in either lamina IIIB or upper lamina VI. After consideration of possible sources of variation in spine numbers several conclusions are made: (1) Dendritic spine development appears to be a tightly controlled process both in terms of actual numbers of spines on a neuron at any one age and in the rate of change of spine frequency. (2) The neurons populations examined all show a gradual increase in spine numbers up to eight weeks of age. (3) At least two different trends are found in spine population maturation after the eight week point: (A)-the spine population may remain constant at the eight week level for same period of time or (B)-there may be a rapid decline in spine numbers following the eight week peak. (4) There is a suggestion that those neurons associated with direct input, or early stages in the relays, from the parvocellular geniculate laminae show trend B, while those associated with magnocellular input, or later order combined relays within the cortex, show trend A. (5) Different parts of a single pyramidal neuron dendrite may show either trend A or trend B, depending on the lamina location of the dendritic segment considered. (6) All neurons show spine population decreases between nine months of age and adult (5-7 years) suggesting continuing long term maturational changes.