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

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.

Animals↗

Operant conditioning of single-unit response patterns in visual cortex.

Unit responses to photic stimuli were studied in cat visual cortex. After the baseline response pattern of a cell was determined, conditioning trials were given during which reinforcement was contingent upon increased firing during a selected segment of the poststimulus interval. Density of reinforcement increased substantially in about half the cells studied; significant increases in firing occurred within, but not outside, the criterion segment.

Animals↗

Infusion of nerve growth factor (NGF) into kitten visual cortex increases immunoreactivity for NGF, NGF receptors, and choline acetyltransferase in basal forebrain without affecting ocular dominance plasticity or column development.

Intracerebroventricular or intracortical administration of nerve growth factor (NGF) has been shown to block or attenuate visual cortical plasticity in the rat. In cats and ferrets, the effects of exogenous NGF on development and plasticity of visual cortex have been reported to be small or nonexistent. To determine whether locally delivered NGF affects ocular dominance column formation or the plasticity produced by monocular deprivation in cats at the height of the critical period, we infused recombinant human NGF into the primary visual cortex of kittens using an implanted cannula minipump. NGF had no effect on the normal developmental segregation of geniculocortical afferents into ocular dominance columns as determined both physiologically and anatomically. The plasticity of binocular visual cortical responses induced by monocular deprivation was also normal in regions of immunohistochemically detectable NGF infusion, as measured using intrinsic signal optical imaging and single-unit electrophysiology. Immunohistochemical analysis of the basal forebrain regions of the same animals demonstrated that the NGF infused into cortex was biologically active, producing an increase in the number of NGF-, TrkA-, p75(NTR)-, and choline acetyltransferase-positive neurons in basal forebrain nuclei in the hemisphere ipsilateral to the NGF minipump compared to the contralateral basal forebrain neurons. We conclude that NGF delivered locally to axon terminals of cholinergic basal forebrain neurons resulted in increases in protein expression at the cell body through retrograde signaling.

Animals↗

Functional magnetic resonance imaging of brightness induction in the human visual cortex.

A grey surface on a bright background appears to be darker than the same surface on a dark background. We used functional magnetic resonance imaging to study this phenomenon called brightness induction. While being scanned, participants viewed centre-surround displays in which either centre or surround luminance was modulated in time. In both cases, participants perceive similar brightness changes in the central surface. In the region of the visual cortex encoding this central surface, both modulations evoked comparable functional magnetic resonance imaging responses. However, the surround modulation signal showed a considerable delay relative to the onset of the brightness percept. This suggests that, although correlated, the functional magnetic resonance imaging signals do not bear a direct relationship with perceived brightness. We conclude that retinotopically organized visual cortex does not represent brightness per se.

Adult↗

Factors that are critical for plasticity in the visual cortex.

Factors that may be critical for plasticity in the visual cortex are evaluated according to three criteria. (1) Do antagonists to the factor abolish plasticity? (2) Does the concentration or activity of the factor peak with the critical period for plasticity? (3) Does rearing in the dark, which postpones the critical period, affect the factor in a similar fashion? N-methyl-D-aspartate receptors fulfil all three criteria. Metabotropic glutamate receptors fulfil two of them. Most other putative factors do not fulfil more than one.

Animals↗

The role of NMDA receptors in long-term potentiation (LTP) and depression (LTD) in rat visual cortex.

The purpose of the present study was to improve our understanding of the role of NMDA receptors in neocortical synaptic plasticity. In slices of rat visual cortex the field potential elicited in layer III in response to white matter stimulation consisted of two components with peak latencies at 5-8 ms (EPSP1) and 12-19 ms (EPSP2). EPSP2 appeared to be polysynaptic since it did not follow stimulation at 0.5 Hz. EPSP1 consisted of both kainate/AMPA and NMDA receptor activity, as revealed by bath application of DNQX and APV. EPSP2 displayed a variable sensitivity to bath-applied APV. Tetanic stimulation of the white matter in normal medium consistently induced long-term potentiation of EPSP1. In the presence of APV, LTP of EPSP1 was induced only when EPSP2 was still present, while there was no change, or LTD was induced, when EPSP2 was completely blocked by APV. In rat visual cortex, blockade of NMDA receptor participation in the postsynaptic response to tetanic stimulation reduces the probability for LTP induction but does not necessarily prevent LTP; synaptic strength may still change in either direction depending, in part, on factors affecting the magnitude of postsynaptic depolarization during tetanus.

2-Amino-5-phosphonovalerate↗

Formal and attribute-specific information in primary visual cortex.

We estimate the rates at which neurons in the primary visual cortex (V1) of anesthetized macaque monkeys transmit stimulus-related information in response to three types of visual stimulus. The stimuli-randomly modulated checkerboard patterns, stationary sinusoidal gratings, and drifting sinusoidal gratings-have very different spatiotemporal structures. We obtain the overall rate of information transmission, which we call formal information, by a direct method. We find the highest information rates in the responses of simple cells to drifting gratings (median: 10.3 bits/s, 0.92 bits/spike); responses to randomly modulated stimuli and stationary gratings transmit information at significantly lower rates. In general, simple cells transmit information at higher rates, and over a larger range, than do complex cells. Thus in the responses of V1 neurons, stimuli that are rapidly modulated do not necessarily evoke higher information rates, as might be the case with motion-sensitive neurons in area MT. By an extension of the direct method, we parse the formal information into attribute-specific components, which provide estimates of the information transmitted about contrast and spatiotemporal pattern. We find that contrast-specific information rates vary across neurons-about 0.3 to 2.1 bits/s or 0.05 to 0.22 bits/spike-but depend little on stimulus type. Spatiotemporal pattern-specific information rates, however, depend strongly on the type of stimulus and neuron (simple or complex). The remaining information rate, typically between 10 and 32% of the formal information rate for each neuron, cannot be unambiguously assigned to either contrast or spatiotemporal pattern. This indicates that some information concerning these two stimulus attributes is confounded in the responses of single neurons in V1. A model that considers a simple cell to consist of a linear spatiotemporal filter followed by a static rectifier predicts higher information rates than are found in real neurons and completely fails to replicate the performance of real cells in generating the confounded information.

Action Potentials↗

Retinofugal projections following early lesions of the visual cortex in the ferret.

Extensive lesions of the occipital cortex comprising the developing occipital visual areas and beyond in young ferrets (postnatal day 5) are followed by massive, but incomplete, degeneration of the lateral geniculate (LGN) and lateralis posterior (LP) nuclei of the thalamus, and minor volumetric reduction of the superior colliculus. Retinal projections (revealed by intraocular tracer injections), while reduced, remain confined to their territories of normal termination, both in the adult and throughout development. Comparisons with other mammalian species point to several common features in the developmental plasticity of retinofugal pathway.

Animals↗

Correlated neuronal variability in monkey visual cortex revealed by a multi-microelectrode.

Recordings from the visual cortex of anaesthetized monkeys taken with a 30-fold multi-microelectrode demonstrate that the neuronal variability, defined as the change in response strength over time spans of a few seconds to several minutes, is highly correlated within groups of neurones. Several such groups exhibiting independent variability between groups, coexist within the area recorded. This within-group covariance suggests that a major part of neuronal variability is due not to a noise process in the cells, but rather to additional inputs to the neurones, which are not under control of the experimenter.

Animals↗

Tangential segregation of simple and complex cells in the visual cortex and their connections. A universal neocortical module.

In the visual cortex of the guinea pig brain, the primary convergence zones for afferents correspond to basal modules--columns which are about 200 microm in diameter-and are separated by secondary convergence zones. The former are characterized by their concentrations of neurons with simple receptive fields and afferent inhibitory cells, and have a different organization of local interneuronal connections as compared with secondary convergence zones, which have an increased proportion of inhibitory influences, addressed excitatory inputs, and more selectivity in their cellular reactions. The basal modules have parameters similar to those of higher mammals; secondary convergence zones are smaller in rodents, and have simpler organization.

Animals↗

A local circuit approach to understanding integration of long-range inputs in primary visual cortex.

Integration of inputs by cortical neurons provides the basis for the complex information processing performed in the cerebral cortex. Here, we have examined how primary visual cortical neurons integrate classical and nonclassical receptive field inputs. The effect of nonclassical receptive field stimuli and, correspondingly, of long-range intracortical inputs is known to be context-dependent: the same long-range stimulus can either facilitate or suppress responses, depending on the level of local activation. By constructing a large-scale model of primary visual cortex, we demonstrate that this effect can be understood in terms of the local cortical circuitry. Each receptive field position contributes both excitatory and inhibitory inputs; however, the inhibitory inputs have greater influence when overall receptive field drive is greater. This mechanism also explains contrast-dependent modulations within the classical receptive field, which similarly switch between excitatory and inhibitory. In order to simplify analysis and to explain the fundamental mechanisms of the model, self-contained modules that capture nonlinear local circuit interactions are constructed. This work supports the notion that receptive field integration is the result of local processing within small groups of neurons rather than in single neurons.

Contrast Sensitivity↗

[Computation of color and brightness differences by neurons in the rabbit visual cortex].

Changes in activity of 54 neurons in the rabbit visual cortex evoked by the replacement of eight color and eight achromatic stimuli in pairs were analyzed. The diffused stimuli generated by color SVGA monitor were used in the experiments. The earliest response of phasic neurons (50-90 ms after the replacement) was strongly correlated with differences between stimuli in color or intensity. This response ("the signal of differences") was used as a basis of a matrix (8 x 8) constructed for each neuron. Such matrices included mean numbers of spikes per second in responses to changes of different stimuli pairs. All matrices were subjected to factor analysis, and the basic axes (the main factors) of sensory spaces were revealed. It was found that 16 neurons (30%) detected only achromatic differences between stimuli. Perceptual spaces of these neurons were two-dimensional with brightness and darkness orthogonal axes. The spaces of 12 neurons (22%) were four-dimensional with two chromatic and two achromatic axes. The structure of the perceptual space reconstructed from neuronal spikes was similar to the space calculated from the early VEP components recorded under similar conditions and to another space reconstructed on the basis of rabbit's instrumental learning. The fundamental coincidence of color spaces revealed by different methods may reflect the general principle of vector coding in the visual system and suggests the coexistence of two independent cortical mechanisms of the detection of chromatic and achromatic differences.

Animals↗

Regressive events in the postnatal development of association projections in the visual cortex.

In newborn kittens, neurones in area 17 of the visual cortex projecting to area 18 are distributed in bands of uniform density across the superficial layers (laminae II, III and the upper part of IV) and the deep layers (V and VI). During weeks 2 and 3 postnatal, the cells of origin of this association pathway become mainly restricted to discrete, dense clusters, approximately 600 microns from centre to centre, in the upper layers, with intervening zones free of association cells, as in the adult cat. We have used retrogradely transported, long-lasting neuronal markers to investigate this developmental refinement of the pattern of cortico-cortical connections. The results, reported here, indicate that axonal retraction plays a significant part in the maturation of the clustered organization of superficial layer neurones projecting to area 18, but that cell death may also be a factor in the elimination of the inappropriate projection from the deep laminae.

Amidines↗

Abnormal retinotopic representations in human visual cortex revealed by fMRI.

The representation of the visual field in early visual areas is retinotopic. The point-to-point relationship on the retina is therefore maintained on the convoluted cortical surface. Functional magnetic resonance imaging (fMRI) has been able to demonstrate the retinotopic representation of the visual field in occipital cortex of normal subjects. Furthermore, visual areas that are retinotopic can be identified on computationally flattened cortical maps on the basis of positions of the vertical and horizontal meridians. Here, we investigate abnormal retinotopic representations in human visual cortex with fMRI. We present three case studies in which patients with visual disorders are investigated. We have tested a subject who only possesses operating rod photoreceptors. We find in this case that the cortex undergoes a remapping whereby regions that would normally represent central field locations now map more peripheral positions in the visual field: In a human albino we also find abnormal visual cortical activity. Monocular stimulation of each hemifield resulted in activations in the hemisphere contralateral to the stimulated eye. This is consistent with abnormal decussation at the optic chiasm in albinism. Finally, we report a case where a lesion to white matter has resulted in a lack of measurable activity in occipital cortex. The activity was absent for a small region of the visual field, which was found to correspond to the subject's field defect. The cases selected have been chosen to demonstrate the power of fMRI in identifying abnormalities in the cortical representations of the visual field in patients with visual dysfunction. Furthermore, the experiments are able to show how the cortex is capable of modifying the visual field representation in response to abnormal input.

Albinism↗

Origins of cross-orientation suppression in the visual cortex.

The response of a neuron in striate cortex to an optimally oriented stimulus is suppressed by a superimposed orthogonal stimulus. The neural mechanism underlying this cross-orientation suppression (COS) may arise from intracortical or subcortical processes or from both. Recent studies of the temporal frequency and adaptation properties of COS suggest that depression at thalamo-cortical synapses may be the principal mechanism. To examine the possible role of synaptic depression in relation to COS, we measured the recovery time course of COS. We find it too rapid to be explained by synaptic depression. We also studied potential subcortical processes by measuring single cell contrast response functions for a population of LGN neurons. In general, contrast saturation is a consistent property of LGN neurons. Combined with rectifying nonlinearities in the LGN and spike threshold nonlinearities in visual cortex, contrast saturation in the LGN can account for most of the COS that is observed in the visual cortex.

Animals↗

Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex. A study with deoxyglucose.

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 nonstriate 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.

Animals↗

Motion selectivity and the contrast-response function of simple cells in the visual cortex.

The responses of simple cells were recorded from the visual cortex of cats, as a function of the position and contrast of counterphase and drifting grating patterns, to assess whether direction selectivity can be accounted for on the basis of linear summation. The expected responses to a counterphase grating, given a strictly linear model, would be the sum of the responses to the two drifting components. The measured responses were not consistent with the linear prediction. For example, nearly all cells showed two positions where the responses approached zero (i.e. two "null phase positions"); this was true, even for the most direction selective cells. However, the measured responses were consistent with the hypothesis that direction selectivity is a consequence of the linear spatiotemporal receptive-field structure, coupled with the nonlinearities revealed by the contrast-response function: contrast gain control, halfwave rectification, and expansive exponent. When arranged in a particular sequence, each of these linear and nonlinear mechanisms performs a useful function in a general model of simple cells. The linear spatiotemporal receptive field initiates stimulus selectivity (for direction, orientation, spatial frequency, etc.). The expansive response exponent enhances selectivity. The contrast-set gain control maintains selectivity (over a wide range of contrasts, in spite of the limited dynamic response range and steep slope of the contrast-response function). Rectification conserves metabolic energy.

Animals↗

Deoxyglucose mapping in the cat visual cortex following carotid artery injection and cortical flat-mounting.

Two techniques are described for improving the efficiency of the deoxyglucose metabolic mapping procedure for studies on the cat visual cortex. The first technique involves the bilateral cannulation of the lingual arteries and the symmetrical injection of 2-deoxy-D-[U-14C]glucose in amounts significantly smaller than required with systemic intravenous administration. The second technique is carried out at the end of the stimulation period and involves unfolding the grey matter of the occipital region of the unfixed cortex by blunt dissection (defibrillation) and cutting of the white matter to make a cortical flat-mount: this permits the preparation of large sections parallel to the cortical laminae and thus the interpretation of deoxyglucose uptake patterns in any one lamina over a large area of the visual cortex. The experiments are relatively cheap and the time required to flat-mount the cortices does not seem to produce any significant decrease in spatial resolution of the autoradiograms. In appropriate experiments (published elsewhere) the techniques allow a comparative analysis of the deoxyglucose patterns between hemispheres receiving different visual stimulation.

Animals↗