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.     

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.     

Neurons in the posteromedial lateral suprasylvian area of the cat are sensitive to binocular positional depth cues

Single units in the posteromedial lateral suprasylvian area of the cat are known to be very sensitive to movement. A proportion of these cells can encode movement in depth, but it is unclear whether posteromedial lateral suprasylvian cells only rely upon motion cues to evaluate stimulus depth or whether they can also code for spatial cues. The present study aims at assessing the sensitivity to spatial disparity of binocular cells, in the postero-medial lateral suprasylvian area, in order to determine whether these units are tuned to positional depth cues. A total of 126 single cells located in the posteromedial lateral suprasylvian area of anesthetized, paralyzed cats were examined. As recordings were performed in the central visual field representation, receptive fields were small. A third of the receptive fields were surrounded by an inhibitory region and almost three-quarters of the cells were direction-selective. Most cells (110/114) were binocular, and a large proportion of single neurons responded to stimuli appearing on the fixation plane by increasing (tuned excitatory cells, 43%) or decreasing (tuned inhibitory cells, 14%) their response rate. A smaller proportion of cells increased their firing rate in response to crossed (near cells, 10%) or uncrossed (far cells, 6%) spatial disparities, hence demonstrating respective preference for stimuli presumably appearing in front of or behind the fixation plane. As compared to primary visual cortex, the proportion of disparity-sensitive cells in posteromedial lateral suprasylvian area is similar, but selectivity is significantly coarser. As the posteromedial lateral suprasylvian area can code for both spatial and temporal aspects of stimuli, this area might be involved in the spatiotemporal integration of depth cues, a process that may also participate in the control of accommodation and vergence.     

A study of binocular convergence in cat visual cortex neurons

Summary The average latency of cortical neuronal responses to electrical optic nerve (ON) stimulation was 3.0±0.7 s.d. msec. No significant difference between latencies to ipsi- and contralateral ON stimulation was found. Binocularly excitable cells showed almost equal response latencies to stimulation of both nerves. The average latency of subcortically recorded geniculo-cortical fibers was 0.3 msec less, but showed the same variance as that of cortical cells, suggesting that in all cases direct monosynaptic excitation of cortical cells by fibers of either ocularity is possible. Classes of ocular dominance based on electrical stimulation were positively, but not 100% correlated with classes of ocular dominance to visual stimulation. An anatomical study revealed that in cat terminals of geniculo-cortical projection are segregated to a lesser degree into ocularity stripes than in monkey. Direct monosynaptic excitation of cells by fibers of either ocularity which was found physiologically would also on these grounds appear possible for all cells.A preliminary report has been presented at the 46th German Physiological Society Meeting in Spring 1976, Pflügers Archiv, Vol. 362, Abstract No. 155, 1976     

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.     

Spatial properties of binocular neurones in the human visual system

Summary The spatial properties of human binocular mechanisms were investigated using the technique of subthreshold summation. Isolation of binocular mechanisms was achieved by means of interocular stimulus presentation. The contrast detection threshold for a sinusoidal test grating viewed by one eye was found to be reduced by a subthreshold grating of the same spatial frequency and orientation seen by the other eye. The interaction between the gratings was approximately linear. Threshold increased as the spatial frequencies or orientations of test and subthreshold gratings were made increasingly different. Spatial stimulus specificities measured in this way were as great for interocular presentation as for simultaneous monocular presentation. The results suggest that human contrast sensitivity for gratings may depend upon binocularly-activated neurones similar to those found in cat and monkey visual cortex.     

Stimulus specificity of binocular cells in the cat's visual cortex: ocular dominance and the matching of left and right eyes

Summary Most cells in the striate cortex respond to visual stimulation through either eye. We have examined quantitatively the matching of response specificity for the two eyes. Our intention was to determine the degree to which this matching depends on ocular dominance. We used standard single cell recording techniques and studied responses to sinusoidal gratings of different spatial frequencies, orientations, and contrasts. For all tests, stimuli were randomly interleaved both with respect to the value of each parameter, and the eye which was stimulated. After estimating ocular dominance qualitatively and quantitatively, we measured: response modulation (to help identify whether a cell was simple or complex), orientation and spatial frequency tuning, and contrast response functions (to estimate contrast thresholds). Results show that: (1) Response modulation is well matched between the two eyes, but there is a slight tendency for the dominant eye to respond with less modulation. (2) Optimal orientation and spatial frequency and their respective tuning widths were similar for the two eyes. In general, tuning functions for the two eyes differed mainly in slope. However, in each case, there was a tendency for the dominant eye to have broader tuning widths. (3) In most cases, contrast response functions for the two eyes differed mainly in their slopes. Extrapolation to spontaneous levels suggests that estimated contrast thresholds are relatively independent of ocular dominance although, again, there was a tendency for the dominant eye to exhibit slightly lower estimated thresholds. These findings demonstrate that response characteristics between the two eyes are generally well matched regardless of relative response strength. There are, however, small but clear differences between the two eyes for all parameters we measured which are related to and demonstrate that ocular dominance influences the degree of matching between the two eyes.     

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     

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.     

Single unit receptive fields in rabbit primary binocular cortex

Summary The receptive fields of 125 single units recorded from the binocular region of rabbit primary visual cortex have been analysed. The population of 43% radially symmetric, 23% directional, and 23% orientation selective units is similar to that of rabbit monocular visual cortex. The relative scarcity of orientation selective units and the absence of orientation columns differentiates rabbit from cat primary visual cortex. However, the majority of binocular units had similar receptive fields in each eye and very unconventional receptive fields were not encountered. Tested binocular units demonstrated summation upon simultaneous stimulation of both receptive fields. In conjunction with findings reported elsewhere, these results suggest that rabbit and cat possess a similar provision for binocular vision in spite of some differences in their cortical organisation.     

Non-stationarity of ocular dominance in cat striate cortex

Summary Interocular relationships, based on monocular directional tuning curves derived simultaneously for bar and for texture motion interleaved, are described for complex cells in the lightly-anaesthetised feline striate cortex. The results confirm earlier reports of stimulus-dependent differences in ocular dominance (Hammond 1979a, b) and demonstrate that ocular-dominance may be time-dependent and influenced by secondary stimulus characteristics including velocity of motion. Temporal and apparently spontaneous shifts in ocular dominance may take place other than in parallel for different classes of stimuli and may even occur simultaneously but in opposite directions. Thus absolute shifts in eye preference, as well as relative shifts between differing stimuli, must both occur with time, perhaps as the result of non-visual influences. The results present a challenge to strategies classically employed in defining cortical ocular dominance.     

Effects of luminance and flicker on ocular dominance shift in kitten visual cortex

Summary We raised monocularly deprived kittens in visual environments with low level illumination that was either steady or flickering. With steady scotopic luminance ocular dominance shifted as it does in normal photopic lighting. In flickering light with an average frequency of 2 Hz there was virtually no ocular dominance shift, while in flickering light averaging 0.1 Hz there was a significant shift. Recordings from the 2 Hz flicker-reared were similar to the dark-reared recordings. The flickering illumination was produced in one case by a high contrast-low brightness TV near the cage, and in another case, by a low voltage incandescent bulb driven by a pseudo-random sequence generator. This circuit delivered either a maximum ON time of 1.7 s or a maximum of 40 s, for the 2 Hz and 0.1 Hz respectively. Both the TV and flickering bulb produced average illumination comparable to the dim (0.01 cd/ m²) steady scotopic illumination. We conclude that dim flickering light is not a sufficient stimulus for promoting ocular dominance shift in kittens in the critical period unless the flicker rate approaches 0.1 Hz. Furthermore results from the TV rearing suggest that flicker may be capable of preventing an ocular dominance shift expected from a concurrent steady low light level background.This work was supported by ONR Contract N00014-81-K-0136. Flaxedil was supplied by Lederle Laboratories. We thank K. Cullen, M. Sutter, J. Kape and M. Motuz for technical assistance. L.N. Cooper and J.P. Rauschecker provided helpful comments.     

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     

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.     

Topographic organization of orientation columns in the cat visual cortex

Summary Three-dimensional reconstructions of the orientation column system were obtained from the visual cortex of four cats using the deoxyglucose technique. One cat had normal visual experience, one was monocularly deprived and two had selective experience with vertical and horizontal contours, respectively. In areas 17 and 18 orientation columns form a remarkably regular system of equally spaced parallel bands whose trajectory is orthogonal to the borderline between areas 17 and 18. This topographic organization is resistant to manipulations of early visual experience.     

Binocular interaction in the visual cortex of awake cats

Summary The effect of monocular and binocular stimulation on cortical neurons of area 17 was investigated in awake unparalyzed cats with painless head fixation. Two types of stimuli were applied: Stationary gratings of variable orientations, and a 3° wide dark stripe at different orientation and moving in different directions. All neurons which were excited from both eyes showed qualitatively similar input properties (orientation specificity, movement and/or direction sensitivity). Quantitatively, the input from both eyes was either equal or dominant from one eye. Contralateral dominance was found 5 times more frequently than ipsilateral dominance. Various types of binocular interaction were found. Some neurons showed an excitatory response from one eye and inhibitory response from the other (inhibition, 14% of our units), and others showed a response during binocular stimulation which was equal to the sum of the monocular responses (summation, 18%), larger (facilitation, 43%) or smaller (occlusion, 14%) than the sum of the two monocular responses. A few units with binocular responses did not respond to monocular stimulation of one or both eyes. The results are compared with those found by other authors in paralyzed and anesthetized animals, and current theories of neuronal mechanisms of binocular vision are discussed in the context of our findings.This work was supported by the Deutsche Forschungsgemeinschaft as a research project in the Sonderforschungsbereich Kybernetik (SFB 31).Dr. R.B. Freeman, jr. was supported by NIH-grant 363-93600-21, MF-428-69 during the period of this research.     

Ocular dominance in kitten cortex: Induced changes of single cells while they are recorded

Summary We have monitored extracellularly individual neurons in the striate cortex of 4-week-old unparalyzed kittens with the aim of changing the ocular dominance of these cells during recording. To do this, we elicited conjugate eye movements using a bipolar stimulating electrode positioned in the internal medullary lamina (IML) of the thalamus. During electrical stimulation of this region, one eye was occluded and the other was visually activated with optimal stimuli. Receptive fields were studied subjectively and objectively and relative response strengths were assessed. Of 42 cells studied in detail, 62% underwent changes in ocular dominance following conditioning periods of, generally, 15–20 min. Control experiments suggest that this plasticity is: agerelated; requires both visual stimulation and activation of pathways associated with eye movement; and does not appear to be caused solely by increased arousal levels.Supported by grant EY01175 and Research Career Development Award EY00092 from the US National Eye InstituteOn leave from Department of Physiology Kanazawa University Medical School, Kanazawa 920, Japan     

Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex

Summary and Conclusions In six dark reared, 4-weak-old kittens visual experience was restricted to contours of a single orientation, horizontal or vertical, using cylindrical lenses. Subsequently, the deoxyglucose method was used to determine whether these artificial raising conditions had affected the development of orientation columns in the visual cortex. After application of the deoxyglucose pulse one hemifield was stimulated with vertical, the other with horizontal contours. Thus, from interhemispheric comparison, changes in columnar systems corresponding to experienced and inexperienced orientations could be determined. The following results were obtained: (1) Irrespective of the restrictions in visual experience, orientation columns develop in areas 17, 18, 19 and in the visual areas of the posterior suprasylvian sulcus. (2) Within area 17, spacing between columns encoding the same orientations is remarkably regular (1 mm), is not influenced by selective experience and shows only slight interindividual variation. (3) In non-striate areas the spacing of columns is less regular and the spatial frequency of the periodicity is lower. (4) The modifiability of this columnar pattern by selective experience is small within the granular layer of striate cortex but substantial in non-granular layers: Within layer IV columns whose preference corresponds to the experienced orientation are wider and more active than those encoding the orthogonal orientation but the columnar grid remains basically unaltered. Outside layer IV the columnar system is maintained only for columns encoding the experienced orientations. The deprived columns by contrast frequently fail to extend into non-granular layers and remain confined to the vicinity of layer IV. (5) These modifications in the columnar arrangement are more pronounced in striate cortex than in non-striate visual areas and, within the former, more conspicuous in the central than in the peripheral representation of the visual field. It is concluded that within layer IV the blue print for the system of orientation columns is determined by genetic instructions: first order cells in layer IV develop orientation selectivity irrespective of experience whereby the preference for a particular orientation is predetermined by the position in the columnar grid. Dependent on experience is, however, the expansion of the columnar system from layer IV into non-granular layers. It is argued that all distortions following selective rearing can be accounted for by competitive interactions between intracortical pathways, the mechanisms being identical to those established for competitive processes in the domain of ocular dominance columns. It is proposed that such experience dependent modifiability of connections between first and second order cells is a necessary prerequisite for the development of orientation selectivity in cells with large and complex receptive fields.This work has partially been supported by a grant from the Deutsche Forschungsgemeinschaft, SFB 50, A14Dedicated to Prof. D. Ploog on the occasion of his 60th anniversaryResearch Fellow of the Alexander-von Humboldt-Stiftung     

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     

Shortage of binocular cells in area 17 of visual cortex in cats with congenital strabismus

Summary Twenty-nine pigmented offspring of an innately esotropic female cat exhibited varying deficits in the number of binocular cells recorded in area 17 of the visual cortex as compared to 12 normal cats. Misalignment of the two eyes in these cats was found in the awake as well as in the paralysed state. Pupillography combined with measurements of visual disparity yielded abnormal esotropia of up to 8.4° under paralysis, which corresponds to an abnormal convergence of the freely moving eyes of up to 14° (average 7.4°). In the majority of animals cortical binocularity was found reduced by the two eyes controlling independent sets of separate units (U-shaped ocular dominance distribution) whereas in 7 cats the reduction was due to a partial loss of one eye's influence. The proportion of monocular units correlated with the degree of crossover of the visual axes (r = 0.73). Anatomical investigation of the retinofugal projections revealed normal appearance in three previously recorded cats in which more than 50% of cortical units had been monocularly driven. The small angles of esotropia and the normal appearance of eye position judged by the pupillary positions in the orbit of these cats, might suggest that we found an animal model for microstrabismus.