Prediction of orientation selectivity from receptive field architecture in simple cells of cat visual cortex

From the intracellularly recorded responses to small, rapidly flashed spots, we have quantitatively mapped the receptive fields of simple cells in the cat visual cortex. We then applied these maps to a feedforward model of orientation selectivity. Both the preferred orientation and the width of orientation tuning of the responses to oriented stimuli were well predicted by the model. Where tested, the tuning curve was well predicted at different spatial frequencies. The model was also successful in predicting certain features of the spatial frequency selectivity of the cells. It did not successfully predict the amplitude of the responses to drifting gratings. Our results show that the spatial organization of the receptive field can account for a large fraction of the orientation selectivity of simple cells.     

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.     

Self-organization of orientation sensitive cells in the striate cortex

A nerve net model for the visual cortex of higher vertebrates is presented. A simple learning procedure is shown to be sufficient for the organization of some essential functional properties of single units. The rather special assumptions usually made in the literature regarding preorganization of the visual cortex are thereby avoided. The model consists of 338 neurones forming a sheet analogous to the cortex. The neurones are connected randomly to a retina of 19 cells. Nine different stimuli in the form of light bars were applied. The afferent connections were modified according to a mechanism of synaptic training. After twenty presentations of all the stimuli individual cortical neurones became sensitive to only one orientation. Neurones with the same or similar orientation sensitivity tended to appear in clusters, which are analogous to cortical columns. The system was shown to be insensitive to a background of disturbing input excitations during learning. After learning it was able to repair small defects introduced into the wiring and was relatively insensitive to stimuli not used during training.     

Structure of a complex receptive field in the cat visual cortex

The most common type of complex receptive field, whose response to the passage of sinusoidal gratings across it consisted of modulated and unmodulated components, was analyzed. The use of a mask to cover half the field, according to the filter theory, led to widening of the transmission band of the field as a spatial frequency filter, due to the appearance or enhancement of the response at lateral low and high frequencies. Modulated components of responses from the left and right halves of the field were out of phase. Analysis of this fact, and also of responses of the field to thin light and dark bars enabled the field structure to be described. It consists of linear and nonlinear subsystems, converging on the output neuron of the complex field. The former is composed of several pairs of on- and off-subfields of the lateral geniculate body. The on- and off-subfields in the pair overlap spatially and converge on the output neuron of the linear subsystem with opposite signs. The nonlinear subsystem is composed of either on- or off-subfields. Other types of complex fields may include different combinations of subsystems. The results indicate that complex fields are spatiotemporal grating filters.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 14, No. 1, pp. 19–25, January–February, 1982.     

Role of intracortical inhibition in orientation tuning dynamics in the cat striate cortex neurons

A suggestion about the leading role of GABA-induced intracortical inhibition in the dynamics of orientation tuning (OT) of the cat striate cortical neurons was tested in acute experiments before and during the local blockade of their inhibition by iontophoretic application of bicucculine. In the course of the investigation of these dynamics, with the use of a temporal scanning method, two types of neurons differing in the inhibition blockade-induced OT changes were found. In the neurons of the first type (57%), bicuculline induced the OT dynamics or enhanced it, if it pre-existed before the bicuculline application. In the neurons of the second type (43%), bicuculline strongly reduced or eliminated the dynamic shift of a preferred orientation. These results mean that under normal conditions the inhibition stabilizes and sharpens OT in some cells, while in other cells, in contrast, it causes the OT dynamics. The following mechanisms may underlie the observed effects: an elimination of the inhibition originating from lateral non-isoorientational excitatory inputs of a receptive field; an inhibition of these inputs via the adjacent interneurons activated by a powerful discharge of the examined neuron; a long-term afterhyperpolarization of the neuron, and the dynamics of the excitatory and inhibitory zones of the receptive field.Neirofiziologiya/Neurophysiology, Vol. 27, No. 2, pp. 100–109, March–April, 1995.     

Investigation of functional organization of receptive fields in the cat visual cortex

Receptive fields of neurons in Area 17 of the visual cortex were investigated in cats. Concentrically shaped fields, fields responding selectively to orientation of a strip or edge, and fields which can be regarded as intermediate between the first two types are described. The boundary between zones of summation and of lateral inhibition coincides in some receptive fields with the boundary between central and peripheral zones with opposite forms of response, while in other fields they do not coincide. For some cells there is no peripheral zone or it may disappear with worsening of the state of function. Cells were observed for which an increase in area of the stimulus in the central zone inhibits the response reaction. Analysis of these data suggests that several cells of the geniculate ganglion converge on some cortical neurons, and several cortical cells on others. An effect of adaptive inhibition was found in which constant illumination of an area in the center of the receptive field inhibits the response in another part. It is shown that this effect is unconnected with the action of scattered light. Constant illumination of the peripheral part of the receptive field deinhibits adaptive inhibition. The boundary between the zones of summation and of lateral inhibition coincides with the boundary between the zones of adaptive inhibition and deinhibition.I. V. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 90–100, July–August, 1969.     

Structure of the simple receptive field of the cat visual cortex

Comparison of unit responses of simple receptive fields of the cat visual cortex (area 17) to presentation of sinusoidal gratings and thin light and dark bars showed that excitatory and inhibitory on- and off-zones of the field are composed of on- and off-subfields of the lateral geniculate body converging on the cortical neuron. Each zone is formed by a pair of opposing subfields, activation of one of which gives an excitatory, and the other, an inhibitory effect. This organization is evidence that the simple field has linear properties. However, a real simple field is not a linear system because of deviations from the ideal organization described above, namely displacement of the subfields relative to each other, nonhomogeneity of the properties of the subfields, and absence of an antagonistic subfield in one of the zones. Even within the same field phasic and tonic subfields may be present.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 13, No. 4, pp. 339–344, July–August, 1981.     

Formation and functional significance of the dark receptive fields of the cat visual cortex

Receptive fields (RFs) of single units in the 17th field of the visual cortex of immobilized cat were investigated under dark adaptation. The mean RF size was equal to 67 degrees and varied from 3 degrees up to 120 degrees. The RFs with centres located near gaze were from 3 degrees up to 120 degrees in dia, but with growth of excentricity the number of small RFs decreased, and in the region of 70 to 100 degrees from gaze only RFs with diameters equal to 100 degrees were found. The shape of "dark" RFs was either ellipsoidal (in most cases) or round. Detector properties (orientational, directional, size and velocity selectivity) of the "dark" RFs were significantly less manifest or absent. Under photopic light adaptation the same units reorganized their RFs to well known sizes and configuration. The hypothesis is discussed of the formation of local detector RF in the visual cortex in light adaptation by selective cortical inhibition which is activated in darkness only slightly. This view is an alternative to the commonly-accepted scheme of local cortical RF formation by the hierarchical and selective excitatory convergence.     

The distribution of orientation of optimal stimuli for cells of striate cortex

The mechanism mediating the adaptation of cortical Area 17 oriented line detector cells is modeled. A novel form of environment and convergence property (which places a requirement on distribution of optimal stimuli) is utilized to show that classical concepts of synaptic efficiency loss due only to disuse are inadequate under the convergence property. A reasonable alternative is presented: a form of synaptic control which reduces synaptic efficiency at non-active synapses as a function of cell firing rate. We show that adequate solutions to our convergence property exist for members of this class. Simulations of this adequate mechanism indicate that under the very disjoint environment defined, small perturbations of the environment's distribution of stimuli may lead to large perturbations of the distribution of stimuli to which Area 17 cells are optimally responsive. A simulation indicates that this effect may be accentuated by a lateral interaction which causeslike cell optimal stimuli to form near each other in cortex; and the effect may be reduced by a lateral interaction which causes like cell optimal stimuli to not form near each other. A form of neurophysiological experiment is suggested for verification.     

Excitatory inputs to spiny cells in layers 4 and 6 of cat striate cortex

The principal target of lateral geniculate nucleus in the cat visual cortex is the stellate neurons of layer 4. In previously reported work with intracellular recording and extracellular stimulation in slices of visual cortex, three general classes of fast excitatory synaptic potentials (EPSPs) in layer 4a spiny stellate neurons were identified. One of these classes, characterized by large and relatively invariant amplitudes (mean 1.7 mV, average coefficient of variation (CV) 0.083) were attributed to the action of geniculate axons because, unlike the other two classes, they could not be matched by intracortical inputs, using paired recording. We have examined in detail the properties of this synaptic input in twelve examples, selecting for study those EPSPs where there was secure extracellular stimulation of the single fibre input to a pair of stimuli 50 ms apart. In our analysis, we conclude that the depression that these inputs show to the second stimulus is entirely postsynaptic, since the evidence strongly suggests that the probability of transmitter release at the synaptic site(s) remains 1.0 for both stimuli. We argue that the most plausible explanation for this postsynaptic depression is a reduction in the average probability of opening the synaptic channels. Using a simple biochemical analysis (c.f. Sigworth plot), it is then possible to calculate the number of synaptic channels and their probability of opening, for each of the 12 connections. The EPSPs had a mean amplitude of 1.91 mV (+/- 1.3 mV SD) and a mean CV of 0.067 (+/- 0.022). The calculated number of channels ranged from 20 to 158 (59.4 +/- 48.7) and their probability of opening to the first EPSP had an average of 0.83 (+/- 0.09), with an average depression of the probability to 0.60 for the second EPSP. Geniculate afferents also terminate in layer 6. Intracellular recordings were also made in the upper part of this layer and a total of 51 EPSPs were recorded from pyramidal cells of three principal types. Amongst this dataset we sought EPSPs with similar properties to those characterized in layer 4a. Three examples were found, which is a much lower percentage (6%) than the incidence of putative geniculate EPSPs found in layer 4a (42%).     

Relationship between size and eccentricity of receptive fields in the cat cerebral cortex area 21

Sizes of receptive fields (RF) in areas 21, 7, and 19 of the cerebral cortex were measured in cats. No correlation between size of RF and eccentricity (average: R=0.15; p>0.05) was found in area 21, as distinct from areas 7 and 19, where size of RF increased with distance from the center to the periphery (R=0.5; p<0.01 and R=0.9; p<0.0001 respectively). Larger RF were found in the left hemisphere than in the right in field 21; size of RF also decreased and leveled out with a move away from area 21 and towards areas 7 and 19.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 19, No. 2, pp. 233–236, March–April, 1987.     

Temporal pattern discrimination within the receptive field of cat retinal ganglion cells

ON-center and OFF-center receptive fields of cat retinal ganglion cells can be divided into two categories: sensitive (type N) and insensitive (type L) to three statistical temporal visual stimuli with different second order statistics but identical first order statistics (Tsukada et al. 1982). The temporal pattern sensitivity of type N response is closely related to the nonlinear stage of Y cells depending on the interaction between center and surround mechanism. The temporal pattern sensitivity of type N responses has a spatial profile within the receptive field; it is highly sensitive in the center region of the receptive field and less sensitive toward the field periphery. The temporal pattern sensitivity in the center region of the receptive field to statistical properties (irregular or regular) of a surrounding flash annulus shows modulation like a switching element: when the surrounding area is stimulated by a more regular flash stimulus with normal distribution of inter-stimulus intervals the system is sensitive (switching on) to the temporal pattern, while a change to an irregular one with an exponential distribution makes it insensitive (switching off) to the temporal pattern.     

A neural network model on self-organizing emergence of simple-cell receptive field with orientation selectivity in visual cortex

In order to probe into the self-organizing emergence of simple cell orientation selectivity, we tried to construct a neural network model that consists of LGN neurons and simple cells in visual cortex and obeys the Hebbian learning rule. We investigated the neural coding and representation of simple cells to a natural image by means of this model. The results show that the structures of their receptive fields are determined by the preferred orientation selectivity of simple cells. However, they are also decided by the emergence of self-organization in the unsupervision learning process. This kind of orientation selectivity results from dynamic self-organization based on the interactions between LGN and cortex.     

A neural network model on self-organizing emergence of simple-cell receptive field with orientation selectivity in visual cortex

In order to probe into the self-organizing emergence of simple cell orientation selectivity, we tried to construct a neural network model that consists of LGN neurons and simple cells in visual cortex and obeys the Hebbian learning rule. We investigated the neural coding and representation of simple cells to a natural image by means of this model. The results show that the structures of their receptive fields are determined by the preferred orientation selectivity of simple cells. However, they are also decided by the emergence of self-organization in the unsupervision learning process. This kind of orientation selectivity results from dynamic self-organization based on the interactions between LGN and cortex.     

Characteristics of inhibition in receptive fields of the cat visual cortex

Unit responses of neurons of zone 17 in the cat striate cortex to stripes of different widths were studied. Changes in the number of spikes during different time intervals (cuts) from the beginning of the response were analyzed in relation to stimulus area. Comparison of the results with those obtained by the study of receptive fields of the lateral geniculate body showed a significant difference in the dynamics of inhibition between cortical and geniculate receptive fields. Similar results were obtained when cortical unit responses to simultaneous and consecutive appearance of two stripes in the receptive field, one in the excitatory zone and the other at the inhibitory periphery, were studied. Evidence of the longer duration of cortical inhibition also was obtained by the same technique. When both stripes were placed in the excitatory center of the field another feature of cortical inhibition was revealed: its dependence on the order of stimulus application. If the order of stimulus application coincided with the optimal direction of movement of the stripe for the given field, the unit response to the next stimulus was strongly facilitated by the action of the stimulus applied previously. Application of stimuli in the opposite order invoked inhibition. The sensitivity of inhibition to the order of stimulus application was observed in the center of the field; it diminished toward the periphery, where application of the stimuli in any order evokes inhibition of the response.Medical Academy, Sofia, Bulgaria, I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 4, pp. 339–346, July–August, 1977.     

Construction of complex receptive fields in cat primary visual cortex.

In primary visual cortex, neurons are classified into simple cells and complex cells based on their response properties. Although the role of these two cell types in vision is still unknown, an attractive hypothesis is that simple cells are necessary to construct complex receptive fields. This hierarchical model puts forward two main predictions. First, simple cells should connect monosynaptically to complex cells. Second, complex cells should become silent when simple cells are inactivated. We have recently provided evidence for the first prediction, and here we do the same for the second. In summary, our results suggest that the receptive fields of most layer 2+3 complex cells are generated by a mechanism that requires simple cell inputs.     

The emergence of contrast-invariant orientation tuning in simple cells of cat visual cortex

Simple cells in primary visual cortex exhibit contrast-invariant orientation tuning, in seeming contradiction to feed-forward models that rely on lateral geniculate nucleus (LGN) input alone. Contrast invariance has therefore been thought to depend on the presence of intracortical lateral inhibition. In vivo intracellular recordings instead suggest that contrast invariance can be explained by three properties of the excitatory pathway. (1) Depolarizations evoked by orthogonal stimuli are determined by the amount of excitation a cell receives from the LGN, relative to the excitation it receives from other cortical cells. (2) Depolarizations evoked by preferred stimuli saturate at lower contrasts than the spike output of LGN relay cells. (3) Visual stimuli evoke contrast-dependent changes in trial-to-trial variability, which lead to contrast-dependent changes in the relationship between membrane potential and spike rate. Thus, high-contrast, orthogonally oriented stimuli that evoke significant depolarizations evoke few spikes. Together these mechanisms, without lateral inhibition, can account for contrast-invariant stimulus selectivity.     

Relationship between level of vigilance and changes in the receptive fields of the cat visual cortex]

The activity of 118 neurones of the primary visual cortex (17th field) was studied in unanesthetized cats, immobilized with d-tubocurarine, in a state of calm wakefulness and in strained attention, alarm. The strained attention was elicited by an air-puff directed to the corner of the closed eye, not used for the photic stimulation. Considerable rearrangments of the receptive field of neurones (94%) were observed in the state of strained attention. In the majority of the studied cortical cells (75%) during 10-30 minutes the excitatory centres of their receptive fields became narrower while their inhibitory periphery widened; in the cells with the inhibitory centres of the receptive fields they were larger in 80% of the cases. It is shown that with dark, mesopic and scotopic adaptation the major characteristics of the changes in the receptive fields remain unaltered. It is assumed that these effects have a behavioural value for the organism, because the created rise in the level of alertness is accompanied by a sharpening of the receptive fields, i.e. by a greater ability to a fine analysis and recognition of visual images.     

The role of visual experience in the development of cat striate cortex

By the third postnatal week, intrinsic developmental programs have established a framework within the cat visual system; this will be used to guide the course of subsequent experience-dependent development. Key elements in this framework are precociously mature cells in visual cortex area 17. These orientation-selective cells are predominantly first-order neurons, they are concentrated in layers IV and VI of area 17, most of them are activated monocularly, many may receive their direct excitatory input from lateral geniculate nucleus X cells, and the distribution of their preferred orientations is biased toward horizontal and vertical. Between the third and the sixth postnatal week, most of the remaining cells in area 17 develop orientation selectivity; this extension of orientation selectivity is blocked or delayed if kittens are deprived of normal patterned visual stimulation. Furthermore, exposure to a limited range of stimulus orientations can lead to an increase in the proportion of orientation-selective cells, and the range of orientation preferences that the cells acquire is restricted by the range of orientations to which the animal is exposed. This occurs with no apparent change in the physiology or morphology of intrinsically selective area 17 cells. Thus selective exposure may have its effect by influencing the connections between the intrinsically selective cells and higher-order neurons in area 17. Experience-dependent changes in the visual system may function to "fine-tune" sensory processing and thus optimize the system's response to the dominant features of the environment. This experience-dependent process could help the young animal to focus its "attention" on those features of its environment that are critical to its survival.