A model study of the dynamic mechanisms of the double orientation tuning of the visual cortex neurons]

The dynamics of double orientation tuning of neurons in the visual cortex of cat was studied by means of computer simulation. It was possible to test the role of shape, relative localization and weight of the inhibitory and excitatory zones of a receptive field and the dynamics of these characteristics. It was shown that selective and acute double orientation tuning can be achieved only through changes in the weight of zones in the receptive fields with the end-stopping and lateral inhibitory zones whereas only the presence of the end-stopping inhibitory zone in the receptive field is sufficient during changes in zone localization and area.     

Receptive field properties of near neighbor orientation selective neurons in the visual cortex: a modeling study

The primary visual cortex is organized into clusters of cells having similar receptive fields (RFs). A purely feedforward model has been shown to produce realistic simple cell receptive fields. The modeled cells capture a wide range of receptive field properties of orientation selective cortical cells. We have analyzed the responses of 78 nearby cell pairs to study which RF properties are clustered. Orientation preference shows strongest clustering. Orientation tuning width (hwhh) and tuning height (spikes/sec) at the preferred orientation are not as tightly clustered. Spatial frequency is also not as tightly clustered and RF phase has the least clustering. Clustering property of orientation preference, orientation tuning height and width depend on the location of cells in the orientation map. No such location dependence is observed for spatial frequency and RF phase. Our results agree well with experimental data.     

Responses of Neurons of the Extrastriate Area 21b of the Cat Brain Cortex to Changes in Orientation of Moving Visual Stimuli

We studied the responses of neurons of the extrastriate cortical area 21b of the cat to changes in orientation of the movements of visual stimuli within the receptive field (RF) of the neuron under study. Our experiments demonstrated that 24 of 108 cells (22%) responded differentially to a certain extent to orientation of the movements of visual stimuli. As a whole, neurons of the area 21b did not demonstrate fine tuning on the optimum angle of orientation. In many cases, neuronal responses to different orientations of the movement of visual stimulus depended significantly on specific parameters of this stimulus (its shape, dimensions, and contrast). Some directionally sensitive neurons responded to a change in orientation of the movement of visual stimuli by modification of the index of directionality. We also studied spatial organization of the RF of neurons with the presentation of stationary visual stimuli. Comparison of the neuronal responses to a change in orientation of the movements of stimuli and to presentation of stationary stimuli showed that the correlation between the orientation sensitivity of the neuron under study and the stationary functional organization of its RF was insignificant. We hypothesize that inhibitory processes and subthreshold influences from a space surrounding the RF play a special role in the formation of the neuronal responses generated in the associative visual cortical regions to visual stimulation.     

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.     

Receptive field dynamics of neurons in the cat visual cortex and lateral geniculate body

Spike responses of single neurons in the primary visual cortex and lateral geniculate body to random presentation of local photic stimuli in different parts of the receptive field of the cell were studied in acute experiments on curarized cats. Series of maps of receptive fields with time interval of 20 msec obtained by computer enabled the dynamics of the excitatory and inhibitory zones of the field to be assessed during development of on- and off-responses to flashes. Receptive fields of all cortical and lateral geniculate body neurons tested were found to undergo regular dynamic reorganization both after the beginning and after the end of action of the photic stimulus. During the latent period of the response no receptive field was found in the part of the visual field tested, but later a small zone of weak responses appeared only in the center of the field. Gradually (most commonly toward 60–100 msec after application of the stimulus) the zone of the responses widened to its limit, after which the recorded field began to shrink, ending with complete disappearance or disintegration into separate fragments. If two bursts of spikes were generated in response to stimulation, during the second burst the receptive field of the neuron changed in the same way. The effects described were clearly exhibited if the level of background illumination, the intensity of the test bars, their contrast with the background, duration, angles subtended, and orientation were varied, although the rate and degree of reorganization of the receptive field in this case changed significantly. The functional importance of the effect for coding of information about the features of a signal by visual cortical neurons is discussed.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 14, No. 6, pp. 622–630, November–December, 1982.     

Functional characteristics of visual cortical neurons during local photic stimulation of their receptive fields in cats

A group of functional characteristics of 103 neurons in visual cortical area 17 was investigated in acute experiments on curarized, light-adapted cats during a change in various parameters of the local photic stimuli. The average threshold sensitivity of the neuron population was 32 dB (0.052 nit), the sharpness of orientation tuning was 37°, the critical summation time was 57 msec, and the reactivity recovery time 190 msec. Photic sensitivity was lower during light adaptation than during dark adaptation, orientation selectivity of the neurons was increased, temporal summation was lengthened, and the time required by the neuron to recovery from after-inhibition was shortened. Several properties of the cortical neurons depended on the accentricity of their receptive fields: Cells with centrally localized receptive fields on average had lower thresholds and shorter summation time and they recovered their reactivity more quickly; their activity was of a higher frequency and they more often generated short phasic discharges than neurons with receptive fields in the peripheral part of the visual field. The mechanisms responsible for changes in the properties of neurons in the central and peripheral visual channels during dark and light adaptation are discussed. The presence of several inhibitory subsystems in the cortex regulating unit activity in the primary visual projection area is postulated.     

Dynamics of orientational tuning of cat visual cortical neurons

Orientational tuning of primary visual cortical unit activity was investigated in acute experiments on cats immobilized by a muscle relaxant, by the time slices method. Poststimulus histograms of responses of a neuron to presentation of a flashing bar of light in the center of its receptive field, with different orientations, were plotted; graphs of orientational tuning with respect to mean discharge frequency in consecutive time cuts of the responses with a 10 or 20 msec step were then plotted. Orientational tuning in all cortical neurons studied exhibited considerable dynamic changes in sharpness and preferred orientation. In two thirds of cells an effect of scanning a certain part of the range of orientations was observed, in the form of a successive shift of the maximum of the orientational tuning curve from some preferred orientations to others was discovered. The possible functional significance of spike discharges of visual cortical neurons is discussed.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 13, No. 5, pp. 451–459, September–October, 1981.     

A geometric model of orientation tuning dynamics in visual neurons]

A geometrical model for the dynamics of orientation tuning of visual neurones was proposed, which makes it possible to study the dynamics of configuration, localization, and weight of excitatory and inhibitory subzones of the receptive field. The model reproduces typical patterns of orientation tuning dynamics, observed in neurophysiological experiments on cat visual cortex neurones. The parameters of the model (size and mutual position of excitatory and inhibitory zones of the receptive field, their weight, and dynamics type) were estimated that correspond to the main types of orientation tuning dynamics in natural conditions. It is shown that selective and acute tuning of neurones can be formed and/or sharpened by intracotrical inhibition, while the dynamics of preferred orientation is due to changes in the geometry of the inhibitory subzone of the receptive field.     

Orientation selectivity of visual cortical neurons at different stimulus intensities in cats

Orientation selectivity of 24 neurons in area 17 of the visual cortex at different intensities of test bars of light, flashing against a constant light background in the center of the receptive field, was investigated in acute experiments on immobilized cats. Five neurons were invariant in orientation tuning to stimulus intensity (contrast): Although the magnitude of the response and acuteness of orientation selectivity were modified, preferential orientation was unchanged. More than half of the cells studied (13) were classed as noninvariant, for their preferential orientation was significantly shifted by 22–90° with a change in contrast. Small shifts of the peak of orientation selectivity, not statistically significant, were observed for the other neurons. Invariant neurons, unlike noninvariant, were characterized by preferential horizontal and vertical orientation, a lower frequency of spontaneous and evoked discharges, and the more frequent presence of receptive fields of simple type. The mechanisms of the change of orientation selectivity during contrast variation and also the different use of the two types of cells in orientation detection operations are discussed.     

Simulation of the role of intracortical inhibition as a source of sensitivity to cross-like figures

Simulation of receptive fields of striate neurons sensitive to cross-like figures under the blockade of intracortical inhibition was performed. It was shown that without the inhibition, a neuron with convergence of signals from two orientation detectors widens its tuning to a cross in such a way that the tuning becomes invariant to the shape and orientation of the cross. Detector of a cross whose orientation is based on the disinhibition mechanisms becomes a bar orientation detector under conditions of inhibition blockade. Another scheme of receptive field is advanced, in which the inhibitory zones mask tuning to cross-like figures, but the blockade of inhibition unveils such sensitivity. We specified the features of the receptive fields (shape, localization, and weight of their zones), which, being applied in simulation, imitate properties of the real striate neurons sensitive to shape and orientation of a cross-like figures.     

Computational Modeling of Orientation Tuning Dynamics in Monkey Primary Visual Cortex

In the primate visual pathway, orientation tuning of neurons is first observed in the primary visual cortex. The LGN cells that comprise the thalamic input to V1 are not orientation tuned, but some V1 neurons are quite selective. Two main classes of theoretical models have been offered to explain orientation selectivity: feedforward models, in which inputs from spatially aligned LGN cells are summed together by one cortical neuron; and feedback models, in which an initial weak orientation bias due to convergent LGN input is sharpened and amplified by intracortical feedback. Recent data on the dynamics of orientation tuning, obtained by a cross-correlation technique, may help to distinguish between these classes of models. To test this possibility, we simulated the measurement of orientation tuning dynamics on various receptive field models, including a simple Hubel-Wiesel type feedforward model: a linear spatiotemporal filter followed by an integrate-and-fire spike generator. The computational study reveals that simple feedforward models may account for some aspects of the experimental data but fail to explain many salient features of orientation tuning dynamics in V1 cells. A simple feedback model of interacting cells is also considered. This model is successful in explaining the appearance of Mexican-hat orientation profiles, but other features of the data continue to be unexplained.     

Orientation sensitive properties of visually driven neurons in extrastriate area 21a of cat cortex

Orientation sensitive properties of extrastriate area 21a neurons were investigated. Special attention was paid to the qualitative characteristics of neuron responses to the different orientations of visual stimulus motion across neuron classical receptive fields (CRF). The results of experiments have shown that a group of neurons (31%) in area 21a with specialized responses to moving visual stimuli changed their direction selective (DS) characteristics depending on the orientation of the stimulus movement. Some neurons reveal an abrupt drop of the direction sensitivity index (DI) to certain orientation (58%), and some show significant increase of DI at one of applied orientations of stimulus motion (22%). Detailed investigation of response patterns of non-directional neurons to different orientations of stimulus motion have revealed clear-cut qualitative differences, such as different regularities in the distribution of inter-peak inhibitory intervals in the response pattern in dependence of the orientation of stimulus motion. The investigation of neuron CRF stationary functional organization did not reveal correlations between RF's spatial functional organization, and that of qualitative modulations of neuron response patterns. A suggestion was put forward, that visual information central processing of orientation discrimination is a complex integrative process that includes quantitative as well as qualitative transformations of neuron activity.     

Orientation and spatiotemporal tuning of cells in the primary visual cortex of an Australian marsupial,the wallaby<Emphasis Type="Italic"> Macropus eugenii</Emphasis>

The metatherians (marsupials) have been separated from eutherians (placentals) for approximately 135 million years. It might, therefore, be expected that significant independent evolution of the visual system has occurred. The present paper describes for the first time the orientation, direction and spatiotemporal tuning of neurons in the primary visual cortex of an Australian marsupial, the wallaby Macropus eugenii. The stimuli consisted of spatial sinusoidal gratings presented within apertures covering the classical receptive fields of the cells. The neurons can be classified as those with clear ON and OFF zones and those with less well-defined receptive field structures. Seventy-percent of the total cells encountered were strongly orientation selective (tuning functions at half height were less than 45 degrees ). The preferred orientations were evenly distributed throughout 360 degrees for cells with uniform receptive fields but biased towards the vertical and horizontal for cells with clear ON-OFF zones. Many neurons gave directional responses but only a small percentage of them (4%) showed motion opponent properties (i.e. they were excited by motion in one direction and actively inhibited by motion in the opposite direction). The median peak temporal tuning for cells with clear ON-OFF zones and those without were 3 Hz and 6 Hz, respectively. The most common peak spatial frequency tuning for the two groups were 2 cycles per degree and 0.5 cycles per degree, respectively. Spatiotemporal tuning was not always the same for preferred and antipreferred direction motion. In general, the physiology of the wallaby cortex was similar to well studied eutherian mammals suggesting either convergent evolution or a highly conserved architecture that stems from a common therian ancestor.     

Spatial and Feature-Based Attention in a Layered Cortical Microcircuit Model

Directing attention to the spatial location or the distinguishing feature of a visual object modulates neuronal responses in the visual cortex and the stimulus discriminability of subjects. However, the spatial and feature-based modes of attention differently influence visual processing by changing the tuning properties of neurons. Intriguingly, neurons'' tuning curves are modulated similarly across different visual areas under both these modes of attention. Here, we explored the mechanism underlying the effects of these two modes of visual attention on the orientation selectivity of visual cortical neurons. To do this, we developed a layered microcircuit model. This model describes multiple orientation-specific microcircuits sharing their receptive fields and consisting of layers 2/3, 4, 5, and 6. These microcircuits represent a functional grouping of cortical neurons and mutually interact via lateral inhibition and excitatory connections between groups with similar selectivity. The individual microcircuits receive bottom-up visual stimuli and top-down attention in different layers. A crucial assumption of the model is that feature-based attention activates orientation-specific microcircuits for the relevant feature selectively, whereas spatial attention activates all microcircuits homogeneously, irrespective of their orientation selectivity. Consequently, our model simultaneously accounts for the multiplicative scaling of neuronal responses in spatial attention and the additive modulations of orientation tuning curves in feature-based attention, which have been observed widely in various visual cortical areas. Simulations of the model predict contrasting differences between excitatory and inhibitory neurons in the two modes of attentional modulations. Furthermore, the model replicates the modulation of the psychophysical discriminability of visual stimuli in the presence of external noise. Our layered model with a biologically suggested laminar structure describes the basic circuit mechanism underlying the attention-mode specific modulations of neuronal responses and visual perception.     

The influence of cortical feature maps on the encoding of the orientation of a short line

The inhomogeneous distribution of the receptive fields of cortical neurons influences the cortical representation of the orientation of short lines seen in visual images. We construct a model of the response of populations of neurons in the human primary visual cortex by combining realistic response properties of individual neurons and cortical maps of orientation and location preferences. The encoding error, which characterizes the difference between the parameters of a visual stimulus and their cortical representation, is calculated using Fisher information as the square root of the variance of a statistically efficient estimator. The error of encoding orientation varies considerably with the location and orientation of the short line stimulus as modulated by the underlying orientation preference map. The average encoding error depends only weakly on the structure of the orientation preference map and is much smaller than the human error of estimating orientation measured psychophysically. From this comparison we conclude that the actual mechanism of orientation perception does not make efficient use of all the information available in the neuronal responses and that it is the decoding of visual information from neuronal responses that limits psychophysical performance. Action Editor: Terrence Sejnowski     

Rabbit visual cortical neurons with simple and complex receptive fields

Receptive fields of neurons of the rabbit visual cortex selective for stimulus orientation were investigated. These receptive fields were less well differentiated than those of the analogous neurons of the cat visual cortex (large in size and circular in shape). Two mechanisms of selectivity for stimulus orientation were observed: inhibition between on and off zones of the receptive field (sample type) and oriented lateral inhibition within the same zone of the receptive field (complex type). Lateral inhibition within the same zone of the receptive field also took place in unselective neurons; "complex" selective neurons differed from them in the orientation of this inhibition. A combination of both mechanisms was possible in the receptive field of the same neuron. It is suggested that both simple and complex receptive fields are derivatives of unselective receptive fields and that "complex" neurons are not the basis for a higher level of analysis of visual information than in "simple" neurons.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 10, No. 1, pp. 13–21, January–February, 1978.     

The Role of Thalamic Population Synchrony in the Emergence of Cortical Feature Selectivity

In a wide range of studies, the emergence of orientation selectivity in primary visual cortex has been attributed to a complex interaction between feed-forward thalamic input and inhibitory mechanisms at the level of cortex. Although it is well known that layer 4 cortical neurons are highly sensitive to the timing of thalamic inputs, the role of the stimulus-driven timing of thalamic inputs in cortical orientation selectivity is not well understood. Here we show that the synchronization of thalamic firing contributes directly to the orientation tuned responses of primary visual cortex in a way that optimizes the stimulus information per cortical spike. From the recorded responses of geniculate X-cells in the anesthetized cat, we synthesized thalamic sub-populations that would likely serve as the synaptic input to a common layer 4 cortical neuron based on anatomical constraints. We used this synchronized input as the driving input to an integrate-and-fire model of cortical responses and demonstrated that the tuning properties match closely to those measured in primary visual cortex. By modulating the overall level of synchronization at the preferred orientation, we show that efficiency of information transmission in the cortex is maximized for levels of synchronization which match those reported in thalamic recordings in response to naturalistic stimuli, a property which is relatively invariant to the orientation tuning width. These findings indicate evidence for a more prominent role of the feed-forward thalamic input in cortical feature selectivity based on thalamic synchronization.     

A multi-stage model for fundamental functional properties in primary visual cortex

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (～4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.     

Orientation-selective neurons in the squirrel visual cortex

The organization of receptive fields of neurons sensitive to orientation of visual stimuli was investigated in the squirrel visual cortex. Neurons with mutually inhibitory on- and off-areas of the receptive field, with partially and completely overlapping excitatory and inhibitory mechanisms, were distinguished. Neurons of the second group are most typical. They exhibit orientation selectivity within the excitatory area of the receptive field because, if the stimulus widens in the zero direction, perpendicular to the preferred direction, lateral inhibition is much stronger than if it widens in the preferred direction. Additional inhibitory areas (outside the excitatory area) potentiate this inhibition and increase selectivity. It is suggested that there is no strict separation of simple (with separate excitatory and inhibitory mechanisms in the receptive field) and complex (with overlapping of these mechanisms) neurons in the squirrel visual cortex.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 11, No. 6, pp. 540–549, November–December, 1979.