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.     

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.     

Population receptive field dynamics in human visual cortex

Seminal work in the early nineties revealed that the visual receptive field of neurons in cat primary visual cortex can change in location and size when artificial scotomas are applied. Recent work now suggests that these single neuron receptive field dynamics also pertain to the neuronal population receptive field (pRF) that can be measured in humans with functional magnetic resonance imaging (fMRI). To examine this further, we estimated the pRF in twelve healthy participants while masking the central portion of the visual field. We found that the pRF changes in location and size for two differently sized artificial scotomas, and that these pRF dynamics are most likely due to a combination of the neuronal receptive field position and size scatter as well as modulatory feedback signals from extrastriate visual areas.     

Mechanism of directional sensitivity of receptive fields in the cat visual cortex

Responses of directional-sensitive neurons in area 17 of the cat's cortex were studied to presentation of two flashing bars of light, one located in the center of the field, the other in the inhibitory zone relative to the center. The order of activation of the stimuli and the time interval between them could be varied; presentation of two bars was thus the analog of a moving stimulus. The inhibitory off-zone located at the entrance to the field from the side of the optimal direction of movement was found to have an initial inhibitory phase, followed by a phase of disinhibition, and again by a second inhibitory phase. Presentation of the bars with different time intervals in cases when stimulation of the center of the field coincided in time with one of the inhibitory phases, led to inhibition of the response, but if stimulation coincided with the phase of disinhibition, it led to facilitation. Phases of disinhibition were not found in the inhibitory zone located at the entrance to the field along the course of a nonoptimal direction of movement. The importance of the temporal characteristics of inhibitory zones for the appearance of directional sensitivity of visual courtical neurons is discussed.     

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.     

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.     

Heterogeneity of neuron populations with complex receptive fields in the cat visual cortex

The selectivity of striate neurons with complex receptive fields to the orientation, direction, and velocity of movement of various stimuli was investigated in unanesthetized and uncurarized cats. On the basis of all characteristics obtained by the study of single-unit responses to a stationary flickering slit, a moving spot of light, and a moving oriented stimulus, four groups of complex neurons were distinguished. The characteristics of group I neurons indicate a mechanism of orientation selectivity in the organization of their receptive fields, group IV neurons have a mechanism of directional selectivity, and neurons of groups II and III possess both mechanisms. The existence of separate neuronal systems coding the orientation and direction of stimulus movement is suggested.V. Kapsukas State University, Vilnius. Translated from Neirofiziologiya, Vol. 11, No. 2, pp. 109–116, March–April, 1979.     

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.     

White noise analysis of temporal properties in simple receptive fields of cat cortex

We studied the linear and nonlinear temporal response properties of simple cells in cat visual cortex by presenting at single positions in the receptive field an optimally oriented bar stimulus whose luminance was modulated in a random, binary fashion. By crosscorrelating a cell's response with the input it was possible to obtain the zeroth-, first-, and second-order Wiener kernels at each RF location. Simple cells showed pronounced nonlinear temporal properties as revealed by the presence of prominent second-order kernels. A more conventional type of response histogram was also calculated by time-locking a histogram on the occurrence of the desired stimulus in the random sequence. A comparison of the time course of this time-locked response with that of the kernel prediction indicated that nonlinear temporal effects of order higher than two are unimportant. The temporal properties of simple cells were well represented by a cascade model composed of a linear filter followed by a static nonlinearity. These modelling results suggested that for simple cells, the nonlinearity occurs late and probably is a soft threshold associated with the spike generating mechanism of the cortical cell itself. This result is surprising in view of the known threshold nonlinearities in preceding lateral geniculate and retinal neurons. It suggests that geniculocortical connectivity cancels the earlier nonlinearities to create a highly linear representation inside cortical simple cells.This work comprises a portion of a PhD thesis submitted by the first author. This study was supported in part by NIH Grant EY04630 and EY06679 to R.C.E., and EY01319 (Core Grant) to the Center for Visual Science     

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.     

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.     

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.     

Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex

Direction selectivity in simple cells of primary visual cortex, defined from their spike responses, cannot be predicted using linear models. It has been suggested that the shunting inhibition evoked by visual stimulation is responsible for the nonlinear component of direction selectivity. Cortical inhibition would suppress a neuron's firing when stimuli move in the nonpreferred direction, but would allow responses to stimuli in the preferred direction. Models of direction selectivity based solely on input from the lateral geniculate nucleus, however, propose that the nonlinear response is caused by spike threshold. By extracting excitatory and inhibitory components of synaptic inputs from intracellular records obtained in vivo, we demonstrate that excitation and inhibition are tuned for the same direction, but differ in relative timing. Further, membrane potential responses combine in a linear fashion. Spike threshold, however, quantitatively accounts for the nonlinear component of direction selectivity, amplifying the direction selectivity of spike output relative to that of synaptic inputs.     

Theory of spatial position and spatial frequency relations in the receptive fields of simple cells in the visual cortex

Striate cells showing linear spatial summation obey very general mathematical inequalities relating the size of their receptive fields to the corresponding spatial frequency and orientation tuning characteristics. The experimental data show that, in the preferred direction of stimulus motion, the spatial response profiles of cells in the simple family are well described by the mathematical form of Gabor elementary signals. The product of the uncertainties in signalling spatial position (x) and spatial frequency (f) has, therefore, a theoretical minimum value of xf=1/2. We examine the implications that these conclusions have for the relationship between the spatial response profiles of simple cells and the characteristics of their spatial frequency tuning curves. Examples of the spatial frequency tuning curves and their associated spatial response profiles are discussed and illustrated. The advantages for the operation of the visual system of different relationships between the spatial response profiles and the characteristics of the spatial frequency tuning curves are examined. Two examples are discussed in detail, one system having a constant receptive field size and the other a constant bandwidth.