Laminar,columnar and topographic aspects of ocular dominance in the primary visual cortex ofCebus monkeys

Summary The representation of the two eyes in striate cortex (V1) ofCebus monkeys was studied by electrophysiological single-unit recordings in normal animals and by morphometric analysis of the pattern of ocular dominance (OD) stripes, as revealed by cytochrome oxidase histochemistry in V1 flat-mounts of enucleated animals. Single-unit recordings revealed that the large majority of V1 neurons respond to the stimulation of either eye but are more strongly activated by one of them. As in other species of monkey, neurons with preference for the stimulation of the same eye are grouped in columns 300–400 µm wide, spanning all cortical layers. Monocular neurons are clustered in layer IVc, specially in its deeper half (IVc-beta), and constitute less than 10% of the population of other layers. Neurons with equal responses to each eye are more commonly found in layer V than elsewhere in V1. In the supragranular layers and in granular layer IVc-alpha neurons strongly dominated by one of the eyes tend to be broadly tuned for orientation, while binocularly balanced neurons tend to be sharply tuned for this parameter. No such correlation was detected in the infragranular layers, and most neurons in layer IVc-beta responded regardless of stimulus orientation. Ocular dominance stripes are present throughout most of V1 as long, parallel or bifurcating bands alternately dominated by the ipsi- or the contralateral eye. They are absent from the cortical representations of the blind spot and the monocular crescent. The domains of each eye occupy nearly equal portions of the surface of binocular V1, except for the representation of the periphery, where the contralateral eye has a larger domain, and a narrow strip along the border of V1 with V2, where either eye may predominate. The orderliness of the pattern of stripes and the relationship between stripe arrangement and the representation of the visual meridians vary with eccentricity and polar angle but follow the same rules in different animals. These results demonstrate that the laminar, columnar and topographic distribution of neurons with different degrees of OD in V1 is qualitatively similar in New- and Old World monkeys of similar sizes and suggest that common ancestry, rather than parallel evolution, may account for the OD phenotypes of contemporaneous simians.     

A quantitative study of the classification and stability of ocular dominance in the cat's visual cortex

Summary We recorded from single cells in the cat's visual cortex to quantitatively evaluate (1) the reliability of subjective assessments of ocular dominance (101 cells) and (2) the stability of ocular dominance over time (25 cells). We found that the correlation between subjective and objective measures of this variable was poorer than expected, and was worst for cells with low overall response strengths. This result appears to reflect variability in the subjective assessment procedure. For the second part of the study, we recorded from single cortical cells of 5-week-old kittens, and made repeated objective measurements of ocular dominance over time. Twenty-four of the twenty-five cells examined were quite stable in ocular dominance for periods so long as 8 h. One unit was encountered which showed substantial progressive shifts in ocular dominance over time.Supported by grant EY01175 and Research Career Development Award EY00029 from the US National Eye Institute to R.D. Freeman     

Complete pattern of ocular dominance stripes in V1 of a New World monkey,Cebus apella

Summary The presence of ocular dominance (OD) stripes in layer IVc of striate cortex (V1) is characteristic of all Old World simians so far studied. In contrast, some species of New World monkeys do not have ocular dominance stripes, and in those that do, the pattern of stripes may be different from that shown in Old World monkeys. This difference has led to the suggestion that OD stripes evolved independently in both groups. We have mapped the entire system of OD stripes in the New World monkey Cebus, by means of cytochrome oxidase histochemistry after monocular enucleation. A striking similarity was found between the patterns in Cebus and Macaca, which is suggestive of common ancestry, rather than parallel evolution.     

Cortical activity blockade prevents ocular dominance plasticity in the kitten visual cortex

Summary Recordings from single units in kitten primary visual cortex show that a reversible blockade of the discharge activities of cortical neurons and geniculocortical afferent terminals by intracortical infusion of the sodium channel blocker tetrodotoxin (TTX) completely prevented the ocular dominance shift that would normally be seen after monocular deprivation. The blockade of cortical plasticity, like the blockade of discharge activity, was reversible, and plasticity was restored following recovery from the effects of TTX. These results extend previous work suggesting involvement of electrical activity at the level of the cortex in the phenomenon of cortical plasticity by demonstrating an absolute requirement for discharge activities in the primary visual cortex.This work was supported by the NIH (EY02874 and EY00213) and by grants from the March of Dimes Birth Defects Foundation and the University of California Academic Senate     

Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys

Summary Density of cones and ganglion cells was studied in horizontal sections of retina in the rhesus monkey (Macaca, mulatta) and the squirrel monkey (Saimiri sciureus). The lower angular density of cones in the fovea of Saimiri correlates with its visual acuity, which is poorer than that of Macaca (0.74 and 0.65 min of arc respectively). Cone density falls more steeply with angular eccentricity from the fovea in Saimiri, in accordance with its relatively poorer peripheral acuity. Comparable results were obtained with retinal ganglion cells, but the comparisons at the fovea itself are more difficult because of the lateral displacement of these elements in the foveal region.The cortical magnification of the visual field (that is, the number of mm of cortex per degree of visual field) is lower for both the foveal and parafoveal representations at the striate cortex in Saimiri. This was correlated with its poorer foveal and parafoveal acuity. It was shown that with increasing eccentricity from the fovea, the fall in the magnification of the visual field at the striate cortex is approximately proportional to the decrease in ganglion cell density at the retina. The results of this study, in which acuity and topography of the visual system are compared in two species of monkey, are consistent with the view that both retinal topography, and the cortical magnification of the visual field, are closely related to visual acuity.This work was supported by Medical Research Council Grant G.967/2/B. We wish to thank Mrs L. Bowman and Mr D. Canwell for their help in preparing histological material.     

Stimulus dependence of ocular dominance of complex cells in area 17 of the feline visual cortex

Summary Stimulus dependence of ocular dominance of 31 deep-layer complex cells was assessed from detailed monocular directional tuning curves for motion of bar stimuli or fields of static visual noise, in area 17 of normal adult cats, lightly anaesthetised with N₂O/O₂ supplemented with pentobarbitone. Virtually all cells were binocularly driven, with the anticipated ocular dominance distribution. Interocular differences in directional bias and sharpness of directional tuning for noise were observed in eleven cells, whereas preferred direction and sharpness of tuning for bar stimuli were similar for each eye. In the majority of cells (20/31), any differences between noise and bar tuning in one eye were replicated in the other. Ocular dominance of about half the cells (17/31) for noise and for bar motion was similar, or marginally shifted by up to one ocular dominance group. Substantial shifts in ocular dominance were seen in 14 cells — by up to two ocular dominance groups in 12 cells and by up to three ocular dominance groups in two cells. In three cases these shifts involved a reversal of eye dominance. Notwithstanding these changes, there were no obvious trends in shifts of ocular dominance in favour of the ipsilateral or contralateral eye, nor was there any tendency towards increased binocularity for noise.     

Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis

The representation of the visual field in the primate lateral intraparietal area (LIP) was examined, using a rapid, computer-driven receptive field (RF) mapping procedure. RF characteristics of single LIP neurons could thus be measured repeatedly under different behavioral conditions. Here we report data obtained using a standard ocular fixation task during which the animals were required to monitor small changes in color of the fixated target. In a first step, statistical analyses were conducted in order to establish the experimental limits of the mapping procedure on 171 LIP neurons recorded from three hemispheres of two macaque monkeys. The characteristics of the receptive fields of LIP neurons were analyzed at the single cell and at the population level. Although for many neurons the assumption of a simple two-dimensional gaussian profile with a central area of maximal excitability at the center and progressively decreasing response strength at the periphery can represent relatively accurately the spatial structure of the RF, about 19% of the cells had a markedly asymmetrical shape. At the population level, we observed, in agreement with prior studies, a systematic relation between RF size and eccentricity. However, we also found a more accentuated overrepresentation of the central visual field than had been previously reported and no marked differences between the upper and lower visual representation of space. This observation correlates with an extension of the definition of LIP from the posterior third of the lateral intraparietal sulcus to most of the middle and posterior thirds. Detailed histological analyses of the recorded hemispheres suggest that there exists, in this newly defined unitary functional cortical area, a coarse but systematic topographical organization in area LIP that supports the distinction between its dorsal and ventral regions, LIPd and LIPv, respectively. Paralleling the physiological data, the central visual field is mostly represented in the middle dorsal region and the visual periphery more ventral and posterior. An anteroposterior gradient from the lower to the upper visual field representations can also be identified. In conclusion, this study provides the basis for a reliable mapping method in awake monkeys and a reference for the organization of the properties of the visual space representation in an area LIP extended with respect to the previously described LIP and showing a relative emphasis of central visual field. Electronic Publication     

Ocular dominance in striate cortex is altered by neonatal section of the posterior corpus callosum in the cat

Summary In adult cats that had previously undergone surgical section of the posterior corpus callosum at 13–18 days after birth, the striate cortex was examined using extracellular single unit recordings. The receptive fields of the cells examined were located from the vertical meridian to 39 ° peripherally, and ranged from above to below the horizontal meridian. Cells were classified according to type (simple, complex), ocular dominance, receptive field size and location. Callosum sectioned cats had 53% of striate cells activated monocularly as compared to 25% for control cats. This increase in monocularly activated units primarily occurred for receptive fields in the paracentral region of the visual field, from 4–39 °. The age at which the neonatal surgery had occurred was correlated with the individual cat's proportion of monocularly activated cells.Therefore, the increase in monocular activation of striate units occurred within a large portion of the normal binocular visual field. This physiological change was partially predicted by a previous behavioral study showing a substantial loss in the extent of the binocular visual field following neonatal corpus callosum section (Elberger 1979).Support for this research was received from Training Grant No. T-32 EY 07035-02 awarded to the University of Pennsylvania. Additional support was provided by the Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, No. 1-11321-215001-10     

Development of the rabbit visual cortex: A quantitative Golgi analysis

Summary The horizontal and vertical components of the positions of both eyes of rhesus monkeys were measured during periods of binocularly stable eye positions (eye pauses) while the animals fixated a small target. Differences between monocular and binocular viewing, as well as effects of target size and background illumination, were assessed and found to be comparable to similar measures for humans. The scatter of eye position for either eye during binocular viewing had a standard deviation of 6–8 min arc in the horizontal and 7–13 min arc in the vertical meridia. Measurements of vergence and vertical misalignment, taken from binocular positional disparity, showed that for nearly 60% of eye pause time the eyes were misaligned on the fixation target by more than 7 min arc along both horizontal and vertical axes. In addition, the line of gaze during the trial was found to follow certain idiosyncratic tendencies for each monkey, although the positional variability remained relatively constant throughout the fixation trial. These observations suggest that during binocular fusion and stereopsis a mechanism exists that dynamically compensates for the relatively large shifts in retinal image position during fixation.Supported by NIH Grant EY02966     

The pattern of ocular dominance columns in flat-mounts of the cat visual cortex

Summary Ocular dominance (OD) columns in the cat visual cortex were visualized with autoradiography after intravitreal injection of (³H)proline. Extending previous studies, a flat-mount technique was applied that enabled the analysis of the distribution of label throughout extensive regions of the visual cortex without requiring reconstructions from serial sections. OD-columns were confined to layer IV and consisted of isolated patches and short bands. The latter were parallel to each other and regularly spaced, the main trajectory being orthogonal to the 17/18 border. This pattern of the geniculo-cortical terminals was similar in the hemispheres ipsi- and contralateral to the injected eye. The mean periodicities of the OD-bands were virtually identical in the two hemispheres of the same animal: 850 m and 830 m in cat D1 and 770 m and 800 m in cat D2. However, the ipsilateral OD-columns appeared smaller, more heavily labeled and more sharply delineated than the contralateral columns.     

Serotonin nerve fibers in the primary visual cortex of the monkey. Quantitative and immunoelectronmicroscopical analysis

Summary A quantitative and immunoelectronmicroscopical analysis of serotonin nerve fibers in the primary visual cortex of the monkey (Macaca fuscata) was made using a sensitive immunoperoxidase method for serotonin. The overall numerical density of serotonin-containing varicosities in the primate striate cortex was approximately 770,000/mm³ and the highest concentration of immunore-active varicosities (ca. 1,400,000/mm³) was observed in the upper portion of layer IVc, the next highest concentration being in layer IVb (ca. 1,180,000/mm³). At the ultrastructural level, the electron dense immunoreactive products were observed in the small granules (10–65 nm in diameter). The varicosities were usually small (0.5–1.0 m in diameter) and made contact with both stellate and pyramidal cells. Serotonin fibers were often in close apposition to the poorly myelinated axons in layers IVb, V, and VI, and they rarely formed distinct synaptic structures with unlabelled neuronal elements.Supported by grant (No. 57214028) from the Ministry of Education, Science and Culture, Japan     

Reduced binocularity in the noradrenaline-infused striate cortex of acutely anesthetized and paralyzed,otherwise normal cats

Summary In anesthetized and paralyzed cats, the normal alignment of the visual axes is disturbed by paralysis of the eye muscles. Thus, the separation between paired receptive fields of binocular cells in visual cortex is increased (paralysis squint). This increased separation is normally tolerated by the majority of visuocortical cells, about 80% of them being binocularly driven (Hubel and Wiesel 1962). It was shown previously that neuronal plasticity in visual cortex can be enhanced in both normal adult cats (Kasamatsu et al. 1979) and kittens (Kuppermann and Kasamatsu 1984) by intracortical microinfusion of noradrenaline (NA). In the present study we tested whether the usual range of disparity produced by the paralysis squint is sufficient to induce ocular dominance changes in visual cortex of adult cats when the neuronal plasticity is enhanced by NA. NA was continuously infused into visual cortex throughout the experiments. The period of the paralysis squint varied from experiment to experiment between 9 and 47 h. We found: (1) These short periods were sufficient to produce a marked reduction in the proportion of binocular cells. (2) The proportion decreased linearly with increasing the duration of the squint period at a rate of 0.17 per 10 h up to about 22 h. (3) At longer durations the average binocularity remained at about 0.30 and could not be further reduced in the present paradigm. (4) The binocularity seemed to decrease with increasing separation of paired receptive fields. (5) Binocularity increased again toward the normal value after optical correction of the squint. (6) The amount of increased binocularity was linearly correlated with the duration of the period after the squint correction. (7) The binocularity increased at a rate of 0.18 per 10 h, reaching the normal value in less than 30 h. We thus concluded that if visuocortical plasticity is maintained at a high level through the continuous infusion of NA it is possible to change the ocular dominance distribution in the mature visual cortex by manipulations of the alignment of the visual axes even in the acutely anesthetized and paralyzed condition.     

Effects of neonatal monocular enucleation on the number of GAD-positive puncta in rat visual cortex

Summary Rats that had one eye removed on the day of birth were examined at various postnatal ages with immunocytochemical methods to determine the effect on the development of the GABAergic axonal plexus in the visual cortex. The monocular segment of visual cortex contralateral to the enucleated orbit had 20–30% fewer GABAergic axon terminals than the monocular segment of visual cortex contralateral to the normal eye. Other cortical areas did not show any significant changes. These findings suggest that sensory deprivation of the visual cortex interferes with the normal development of GABAergic neurons.     

Ocular dominance and disparity-sensitivity: why there are cells in the visual cortex driven unequally by the two eyes

Summary Tuning curves for stimulus disparity were constructed for units in area 18 and along the 17/18 border of the cat visual cortex (N=248). Units were activated with stimuli moving in the same (in-phase motion) or in the opposite direction (antiphase motion) across the two retinae. Over 70% of the units encountered showed sensitivity to stimulus disparity. A clear relationship was found between disparity-sensitivity and unit ocular dominance (OD). Contrary to what might have been expected, large binocular interactions were correlated with unilateral OD. Units highly sensitive to stimulus disparity generally showed strong dominance by one eye (OD groups 1, 2, 6 and 7), or responded well only to binocular stimulation, and weakly or not at all through each eye separately (“binocular-only”). Units unselective for stimulus disparity were usually driven well through either eye (OD groups 3, 4 and 5). High disparity-sensitivity was due to both strong binocular inhibition and strong binocular facilitation in units of extreme unilateral OD. Nearly all units of OD groups 1 and 7 showed clear binocular interactions, indicating that there are few “truly monocular” cells in the cat visual cortex.     

Immunocytochemical localization of calcineurin in the adult and developing primary visual cortex of cats

An immunocytochemical method was used to localize calcineurin, a calcium-dependent calmodulinstimulated protein phosphatase, in the primary visual cortex of developing and adult cats. In the adult calcineurin immunoreactivity exhibits a laminar distribution with dense labeling in the upper half of layers II/III and two lightly labeled bands in lower layer IV and in layer VI. Most of the immunoreactive neurons are pyramidal in shape and appear to form a subpopulation of cortical neurons, but non-pyramidal neurons were also labeled, especially during early stages of postnatal development. The distribution pattern of calcineurin immunoreactivity showed developmental changes until at least 3 months of age. The number of calcineurin-positive cells abruptly increased at 3 weeks, and heavily labeled neurons appeared in a well-delineated band in layer IV between 3 and 5 weeks of age. At 6 to 10 weeks, neurons in layers II/III also became strongly immunoreactive. At this developmental stage intensely stained cells were thus distributed throughout layers II to IV. Thereafter, there was a marked decrease in the number of immunoreactive cells in layer IV and beyond 12 weeks the distribution pattern of calcineurin immunoreactivity became similar to that of adult animals. These changes of calcineurin expression show some relation with the inside-out pattern of cortical maturation and with the time course and the laminar selectivity of use-dependent malleability. Therefore, we suggest that calcineurin may be involved in processes of neuronal differentiation and experience-dependent plasticity.     

Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult macaque monkey

Summary The laminar location of cytochrome oxidase staining has been compared in the lateral geniculate nucleus and area 17 in newborn and adult macaque monkeys. In area 17 of the adult, the distribution of cytochrome oxidase activity confirmed published findings. In the newborn animals, the tissue reacted as strongly for cytochrome oxidase as in the adult but the pattern of labelling was different in two respects. Firstly in layer 1 activity was stronger and occupied a wider portion of this layer. Secondly, cytochrome oxidase staining in layer 4C occupied two separate bands, a small narrow band at the bottom of 4C and a wider one occupying the full width of 4C and spilling over into 4B. The pattern of cytochrome oxidase activity did not appear to be influenced by eccentricity in the newborn whereas, in the adult, label in 4C was more intense in cortex subserving central vision. In the lateral geniculate nucleus of the adult, the magnocellular layers and the most dorsal parvocellular layer reacted most strongly for cytochrome oxidase. In the newborn, parvocellular layers were more uniformly labelled and the difference between parvo and magnocellular layers more pronounced. These results are discussed in relationship to the development of thalamo-cortical projections in the monkey.     

Age dependence of the effect of squint on cells in Kittens' visual cortex

Summary The period of susceptibility of the visual cortex of kittens to the effect of squint is limited to the first three postnatal months. The reduction of binocularity found in these kittens as reflected by the distribution of neurons according to their ocular dominance is especially emphasized in animals operated on between the ages of 4–7 weeks in comparison to animals operated on between the ages of 8–11 weeks. The proportion of monocularly dominated neurons within the first three postnatal months is significantly (0.05 > p > 0.025) reduced with age. Similar effect on cortical neurons was found for animals who were under the influence of squint for 6 weeks or 15 months and for animals with wide range of deviation angles.     

Inverted vision surgically induced in experienced cats: Physiology of the primary cortex

Summary The physiological effects of inversion of vision were studied in the visual cortex of five adult cats following 180 ° surgical rotation of one eye for 2–3 months. The other eye was closed in order to prevent binocular conflicting visual input in the period between eye inversion and unit recording.The distribution of neurons according to their ocular dominance was very slightly different from that of normal cats. The retinotopic map was stable in that respect that receptive fields were spatially located in their expected position in accordance with the inversion induced; they reversed positions when maps of the two eyes were compared. Directional selectivity was also preserved; the preferred directions of binocularly activated units were found to be in opposition when responses from the normal and the inverted eyes were compared.     

Behavioral modulation of neuronal activity in monkey striate cortex: excitation in the absence of active central fixation

Summary Two rhesus monkeys were trained to fixate a small fixation point for randomly varying periods of time using the dimming paradigm. During single unit recording in the striate cortex the fixation point was turned off for a few hundred milliseconds in the presence of a peripheral stimulus. During the disappearance of the fixation point the peripheral stimulus could dim and because of that, in some trials the monkey's saccade to the stimulus right after the offset of the fixation point. In other trials of the same task the monkeys suppressed the execution of a saccade without missing the dimming of the stimulus. During the monkeys performance of this task, striate cortex neurons display an increase of activity after fixation point offset in the presence of a receptive field stimulus, independent of the monkey's decision to look at it or not. Its occurrence can be interpreted as a sign of the monkey having interrupted active fixation of the fixation point and/or having shifted its visual attention towards the peripheral target without necessarily executing a saccade to it. This work was supported by the Deutsche Forschungsgemeinschaft This work was supported by the Deutsche Forschungsgemeinschaft This work was supported by the Deutsche Forschungsgemeinschaft     

The effects of reverse monocular deprivation in monkeys II. Electrophysiological and anatomical studies

Summary Monkeys had one eye closed at about 30 days of age for 14, 30, 60, or 90 days, then opened, and the fellow eye closed for another 120 days. The animals then had at least 10 months of binocular visual experience before extensive behavioral training and testing were carried out. In terminal experiments concluded more than 18 months later, microelectrode investigations of the striate cortex demonstrated that there was almost a complete absence of binocular neurons in all animals. The initially deprived eyes (IDEs) dominated the majority of cortical neurons, even when soma size measurements of lateral geniculate neurons indicated that the LGN cells driven by the IDE had not regained their normal size. The monkeys which had significant interocular differences in spatial vision also exhibited abnormalities in the distribution of the metabolic enzyme, cytochrome oxidase (CO), within the striate cortex. These results demonstrate that many of the severe alterations in cortical physiology and eye dominance produced by early monocular form deprivation can be reversed, with recovery of normal cortical function, via the reverse-deprivation procedure.Supported by National Eye Institute grants R01 EY01120, R01 EY03611, R01 EY01139, and EY02520