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.     

Sensitivity of the cat lateral geniculate body neurons to orientation of the brightness gradient vector

A new property of visual neurons: their sensitivity to orientation and the vector brightness gradient, was revealed and described. Receptive fields of the lateral geniculate body neurons in the cat have preferred orientation maximum reaction (average mean of orientation sensitivity coefficient--0.55 +/- 0.20). The preferred orientation mainly has a radial or tangential trend in the visual field. Temporal characteristics of the neuronal responses were analysed. A role of inhibition processes in the orientation sensitivity is discussed.     

Visual cells remember earlier applied target: plasticity of orientation selectivity

Background

A canonical proposition states that, in mature brain, neurons responsive to sensory stimuli are tuned to specific properties installed shortly after birth. It is amply demonstrated that that neurons in adult visual cortex of cats are orientation-selective that is they respond with the highest firing rates to preferred oriented stimuli.

Methodology/Principal Findings

In anesthetized cats, prepared in a conventional fashion for single cell recordings, the present investigation shows that presenting a stimulus uninterruptedly at a non-preferred orientation for twelve minutes induces changes in orientation preference. Across all conditions orientation tuning curves were investigated using a trial by trial method. Contrary to what has been previously reported with shorter adaptation duration, twelve minutes of adaptation induces mostly attractive shifts, i.e. toward the adapter. After a recovery period allowing neurons to restore their original orientation tuning curves, we carried out a second adaptation which produced three major results: (1) more frequent attractive shifts, (2) an increase of their magnitude, and (3) an additional enhancement of responses at the new or acquired preferred orientation. Additionally, we also show that the direction of shifts depends on the duration of the adaptation: shorter adaptation in most cases produces repulsive shifts, whereas adaptation exceeding nine minutes results in attractive shifts, in the same unit. Consequently, shifts in preferred orientation depend on the duration of adaptation.

Conclusion/Significance

The supplementary response improvements indicate that neurons in area 17 keep a memory trace of the previous stimulus properties, thereby upgrading cellular performance. It also highlights the dynamic nature of basic neuronal properties in adult cortex since repeated adaptations modified both the orientation tuning selectivity and the response strength to the preferred orientation. These enhanced neuronal responses suggest that the range of neuronal plasticity available to the visual system is broader than anticipated.     

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.     

Reorganization of Receptive Fields of Cortical Field 21a Neurons and Formation of Responses to Moving Visual Stimuli

Using extracellular recording of spike activity from single neurons of field 21a of the cat neocortex, we examined in detail the spatial organization of receptive fields (RFs) of such cells after conditions of presentation of an immobile blinking light spot (a static RF) and moving visual stimuli (dynamic RFs). As was shown, the excitability of different RF subfields of a group of neurons possessing homogeneous on–off organization of the static RF changes significantly depended on the contrast, shape, dimension, orientation, and direction of movement of the applied mobile visual stimulus. This is manifested in changes in the number of discharge centers and shifts of their spatial localization. A hypothesis on the possible role of synchronous activation of the neurons neighboring the cell under study in the formation of an additional neuronal mechanism providing specialization of neuronal responses is proposed.     

Characteristics of Gamma-Oscillations in Responses of Neurons of the Cat Lateral Geniculate Body

There were studied characteristics of gamma-oscillations in responses of neurons of the lateral geniculate body (LGB) in cat to exposure in their receptive fields (RF) of half-tone and binary test images. The gamma-oscillations were observed in 38.8% of cases (69 cells). The spectral characteristics (SC) (the band 20–100 Hz) of the neuronal responses to adequate stimuli (on- and off-responses correspondingly of on- and off-neurons) were analyzed. The total of 5930 poststimulus histograms (PSTH) of responses constructed from 177 900 neuronal impulse responses were considered. The mean value of the SC dominant frequencies of the whole sample of the neuronal responses amounted to 44.74 ± 21.46 Hz. In this cell sample, the neurons were revealed, which generated oscillations with markedly different frequencies in response to the same stimuli. Based on this property, three types of neurons were determined, with the mean oscillation frequencies of 26.95 ± 4.35, 52.02 ± 9.05, and 85.79 ± 7.19 Hz. The histograms of distribution of peak frequency values in SC of the neuronal responses and of index values of these oscillation peaks also revealed three maxima that corresponded to the frequencies of the three described types of neurons. The mean values of dominant frequencies of gamma-oscillations in responses of all three types of neurons remained constant (within the limits of dispersion) at changes of spatial-brightness parameters of test stimuli as well as at changes of the neuronal excitation level (the number of impulses in responses). The oscillation index values of dominant frequencies depended on parameters of the test images and correlated with the neuronal excitation level (the coefficient of correlation was 0.78 from data of 5930 CX). The suggestion is made about the existence in the neuronal network of the synchronization mechanisms functioning on the principle of multiple synchronization.      

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.     

Vector representation of associative learning

I. P. Pavlov [12] has shown that conditioned reflexes are selective both with respect to conditioned stimuli and to conditioned reflexes elicited by those conditioned stimuli. At the neuronal level selective aspects of conditioned stimuli are based on detectors selectively tuned to respective stimuli. The selective aspects of conditioned reflexes are due to command neurons representing specific unconditioned reflexes. It can be assumed that conditioned reflexes result from association between selective detectors and specific command neurons. The detectors activated by a conditioned stimulus constitute a combination of excitations--a detector excitation vector. The detector excitation vector acts on a command neuron via a set of plastic synapses--a synaptic weight vector. Plastic synapses are modified in the process of learning making command neuron selectively tuned to a specific conditioned stimulus. The selective tuning of a particular command neuron to a specific excitation vector referred to a conditioned stimulus is a basis of associative learning. The probabilities of conditioned reflexes elicited by conditioned and differential stimuli implicitly contain information concerning excitation vectors that encode respective stimuli. Contribution of the vector code to associative learning was explored combining differential color conditioning with intracellular recording from color-coding neurons. It was shown that colors in carps and monkeys are represented on a hypersphere in the four-dimensional space similar to human color space. The basis of the color space is constituted by red-green, blue-yellow, brightness and darkness neurons.     

Responses of neurons of the extrastriate cortex of the cat brain to moving stimuli of different forms

We examined responses of neurons of the field 21b of the cat brain cortex to presentation of moving visual stimuli of different forms. Characteristics of the responses of about 54% of the studied neurons showed that in these cases configurations of the contours of moving stimuli were to a certain extent discriminated. Most neurons selectively reacting to changes in the form of the stimulus were dark-sensitive units (they generated optimum responses to presentation of dark visual stimuli on the light background). Detailed examination of the spatial infrastructure of receptive fields (RFs) of the neurons and comparison of this structure with the selectivity of neuronal responses showed that there is no significant correlation between static organization of the RF and responses of the neuron to the movements of stimuli of different forms. We hypothesize that the dynamic infrastructure of the RF and the combined activity of functional groups of neurons, whose RFs spatially overlap the RF of the neuron under study, play a definite role in the mechanisms responsible for neuronal discrimination of the form of the visual stimulus. Neirofiziologiya/Neurophysiology, Vol. 38, No. 1, pp. 61–71, January–February, 2006.     

Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition

To test theories of orientation selectivity in primary visual cortex (V1), we have done experiments to measure the dynamics of orientation tuning of single neurons in the V1 cortex of macaque monkeys. Based on our dynamics results, we propose that a V1 cell's orientation selectivity is generated mainly by both tuned enhancement and global suppression. Enhancement near the preferred orientation is probably caused by feed-forward input from LGN (plus amplification by cortical-cortical interaction). Global suppression could be supplied by cortical inhibition. Additionally, in about 1/3 of V1 neurons (usually the most sharply tuned) there is tuned suppression, centered near the cell's preferred orientation but broader than tuned enhancement. These mechanisms also can explain important features of steady-state selectivity in the V1 neuron population. Furthermore, similar neuronal mechanisms may be used generally throughout the cerebral cortex.     

Spatio-temporal organization of receptive fields of the cat striate cortex

The responses of cortical cells to gratings and bars were compared. The excitatory and inhibitory on-and off-zones of a simple cell are composed of on- and off-subfields of CGL. Any zone is formed by an opponent pair of subfields one of which gives an excitatory effect, the other — inhibitory. Such organization assumes the linear properties of a simple field. The deviations from linearity are due to spatial dis-placements of the subfields, heterogeneity of subfields, or the absence of one subfield in the opponent pair. Subfields may be both phasic and tonic, even in the same RF. Analysis of the most common type of a complex cell with modulated responses against unmodulated background shows that a mask eliminating stimulation of any half of the RF causes (according to the theory of filtres) increasing the bandwidth due to the increase or the appearance of responses to side low and high frequencies. The modulated components of the responses from both halves of the RF are out of phase. Analysis of this fact and the responses to thin bars suggests that a complex field is formed by linear and nonlinear subsystems converging onto output neuron. Other types of complex fields are organized by different combinations of subsystems. Limited in area by masking the RF responds to much higher spatial frequencies than the whole RF. The optimal frequency in two-dimensional spatial frequency characteristics of the RF does not change with orientation. Simple RFs and a part of complex RF calculate the amplitude and the phase of the stimulus, the other part of complex RFs (with unmodulated response) calculate only amplitude. Given all this, the RFs are grating filters of spatial frequency.     

Searching for optimal stimuli: ascending a neuron’s response function

Many methods used to analyze neuronal response assume that neuronal activity has a fundamentally linear relationship to the stimulus. However, some neurons are strongly sensitive to multiple directions in stimulus space and have a highly nonlinear response. It can be difficult to find optimal stimuli for these neurons. We demonstrate how successive linear approximations of neuronal response can effectively carry out gradient ascent and move through stimulus space towards local maxima of the response. We demonstrate search results for a simple model neuron and two models of a highly selective neuron.     

Frequency-dependent response of SI RA-class neurons to vibrotactile stimulation of the receptive field

Three types of experiment were carried out on anesthetized monkeys and cats. In the first, spike discharge activity of rapidly adapting (RA) SI neurons was recorded extracellularly during the application of different frequencies of vibrotactile stimulation to the receptive field (RF). The second used the same stimulus conditions to study the response of RA-I (RA) cutaneous mechanoreceptive afferents. The third used optical intrinsic signal (OIS) imaging and extracellular neurophysiological recording methods together, in the same sessions, to evaluate the relationship between the SI optical and RA neuron spike train responses to low- vs high-frequency stimulation of the same skin site. RA afferent entrainment was high at all frequencies of stimulation. In contrast, SI RA neuron entrainment was much lower on average, and was strongly frequency-dependent, declining in near-linear fashion from 6 to 200 Hz. Even at 200 Hz, however, unambiguous frequencyfollowing responses were present in the spike train activity of some SI RA neurons. These entrainment results support the "periodicity hypothesis" of Mountcastle et al. ( J Neurophysiol 32: 452-484, 1969) that the capacity to discriminate stimulus frequency over the range 5-50 Hz is attributable to the ability of SI RA pyramidal neurons to discharge action potentials in consistent temporal relationship to stimulus motion, and raise the possibility that perceptual frequency discriminative capacity at frequencies between 50 and 200 Hz might be accounted for in the same way. An increase in vibrotactile stimulus frequency within the range 6-200 Hz consistently resulted in an increase in RA afferent mean spike firing rate (M FR). SI RA neuron M FR also increased as frequency increased between 6 and 50 Hz, but declined as stimulus frequency was increased over the range 50-200 Hz. At stimulus frequencies > 100 Hz, and at positions in the RF other than the receptive field center (RF center ), SI RA neuron MFR declined sharply within 0.5-2s of stimulus onset and rebounded transiently upon stimulus termination. In contrast, when the stimulus was applied to the RF center, MFR increased with increasing frequency and tended to remain well maintained throughout the period of high-frequency stimulation. The evidence obtained in "combined" OIS imaging and extracellular microelectrode recording experiments suggests that SI RA neurons with an RF center that corresponds to the stimulated skin site occupy small foci within the much larger SI region activated by same-site cutaneous flutter stimulation, while for the RA neurons located elsewhere in the large SI region activated by a flutter stimulus, the stimulus site and RF center are different.     

Simulation of mechanisms of tuning to incomplete cross-like figures in neurons of visual cortex

We performed a digital simulation of the receptive fields (RF) of cat cortical neurons in the area 17 that are able to detect cross-like figures with partly masked central or peripheral fragments. It was shown that the reciprocal interaction between the RF center and periphery may produce sharp, selective, and pronounced tuning to a cross shape and orientation due to blocking the end-stopping inhibition in the RF by its side-disinhibitory zone. Under conditions of cooperative interaction between the RF center and periphery the sensitivity index (cross/bar response ratio) was typically lower than in the reciprocal model. Features of the model that are critical for sensitivity to cross in cases of small or incomplete figures (the shape, localization, and weight of the RF zones) are specified.     

Spatial summation processes in the receptive fields of visually driven neurons of the cat's cortical area 21a

The spatial summation in receptive fields (RF) of single neurons in cat's extrastriate area 21a was investigated as a basic neurophysiological substrate for central integration processing of visual information. The results showed that the majority of investigated neurons changed their response patterns with gradual increase of applied stimulus size. In approximately 82% of cases the suppression of neuron discharges was observed when the length of the moving strip exceeded that of the RF. In some neurons the increased size of the moving stimulus leads to the changes in the RF substructure. Receptive fields of neurons recorded at the same microelectrode penetration depth showed a great variety of RF superpositions distributed in a spatially asymmetric manner. As a result, every single RF consists of multiple sub-regions within the RF, differing from each other by the number of superimposed RF-s (density factor). We suggest that such complex spatial organization of the RF provides the neurophysiological basis for central integration processing of the visual information.     

Dynamics of light intensity detection by visual cortical neurons in cats

The dynamics of the intensity function of 32 neurons in area 17 of the visual cortex to photic stimuli of optimal size, shape, and orientation flashing in the center of the receptive field was studied by the time slices method, with a step of 10 or 20 msec, in unanesthetized, curarized cats. All neurons tested showed instability of their intensity function reflected in characteristics of successive fragments of the response: It changed both in preferred intensity and in width of the intensity range within which the neuron generated an above-threshold response. In 72% of cases the preferred intensity for the neuron changed successively during the 4–200 msec after the beginning of stimulation by 4–36 dB from greater toward lesser brightnesses, but later it changed more rapidly (in 20–60 msec), rising again apparently in a jump. In four cases the response optimum was shifted up the intensity scale from its initial value by 10–20 dB. Analysis showed that the observed effects are the simple result of the shape of the relationship between temporal characteristics of the response (latent period, time taken to reach the maximum, and time of ending of the burst) to photic stimulus intensity. The possible functional role of these effects for dynamic time coding of information on brightness of photic stimuli by visual cortical neurons is discussed.     

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.     

Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the FMRI adaptation paradigm

fMRI-based adaptation paradigms (fMR-A) have been used to infer neuronal stimulus selectivities in humans. Inferring neuronal selectivities from fMR-A, however, requires an understanding of the relationship between the stimulus selectivity of neuronal adaptation and responses. We studied this relationship by recording single cells in macaque inferior temporal (IT) cortex, an area that shows fMRI adaptation. Repetition of identical object images reduced the responsiveness of single IT neurons. Presentation of an image to which the neuron was unresponsive did not alter the response to a subsequent image that activated the neuron. Successive presentation of two different images to which the neuron responded similarly produced adaptation, but less so than the repeated presentation of an image. The neuronal adaptation at the single-cell level showed a greater degree of stimulus selectivity than the responses. This complicates the interpretation of fMR-A paradigms when inferring neuronal selectivity.     

Vertical Binocular Disparity is Encoded Implicitly within a Model Neuronal Population Tuned to Horizontal Disparity and Orientation

Primary visual cortex is often viewed as a “cyclopean retina”, performing the initial encoding of binocular disparities between left and right images. Because the eyes are set apart horizontally in the head, binocular disparities are predominantly horizontal. Yet, especially in the visual periphery, a range of non-zero vertical disparities do occur and can influence perception. It has therefore been assumed that primary visual cortex must contain neurons tuned to a range of vertical disparities. Here, I show that this is not necessarily the case. Many disparity-selective neurons are most sensitive to changes in disparity orthogonal to their preferred orientation. That is, the disparity tuning surfaces, mapping their response to different two-dimensional (2D) disparities, are elongated along the cell''s preferred orientation. Because of this, even if a neuron''s optimal 2D disparity has zero vertical component, the neuron will still respond best to a non-zero vertical disparity when probed with a sub-optimal horizontal disparity. This property can be used to decode 2D disparity, even allowing for realistic levels of neuronal noise. Even if all V1 neurons at a particular retinotopic location are tuned to the expected vertical disparity there (for example, zero at the fovea), the brain could still decode the magnitude and sign of departures from that expected value. This provides an intriguing counter-example to the common wisdom that, in order for a neuronal population to encode a quantity, its members must be tuned to a range of values of that quantity. It demonstrates that populations of disparity-selective neurons encode much richer information than previously appreciated. It suggests a possible strategy for the brain to extract rarely-occurring stimulus values, while concentrating neuronal resources on the most commonly-occurring situations.