Asymmetric suppression outside the classical receptive field of the visual cortex

Abstract

Areas beyond the classical receptive field (CRF) can modulate responses of the majority of cells in the primary visual cortex of the cat (). Although general characteristics of this phenomenon have been reported previously, little is known about the detailed spatial organization of the surrounds. Previous work suggests that the surrounds may be uniform regions that encircle the CRF or may be limited to the "ends" of the CRF. We have examined the spatial organization of surrounds of single-cell receptive fields in the primary visual cortex of anesthetized, paralyzed cats. The CRF was stimulated with an optimal drifting grating, whereas the surround was probed with a second small grating patch placed at discrete locations around the CRF. For most cells that exhibit suppression, the surrounds are spatially asymmetric, such that the suppression originates from a localized region. We find a variety of suppressive zone locations, but there is a slight bias for suppression to occur at the end zones of the CRF. The spatial pattern of suppression is independent of the parameters of the suppressive stimulus used, although the effect is clearest with iso-oriented surround stimuli. A subset of cells exhibit axially symmetric or uniform surround fields. These results demonstrate that the surrounds are more specific than previously realized, and this specialization has implications for the processing of visual information in the primary visual cortex. One possibility is that these localized surrounds may provide a substrate for figure-ground segmentation of visual scenes.

Fig. 1.

Illustration of our method for investigating the CRF surrounds. All four of these configurations (A–D) are interleaved in a single stimulation set. The CRF is indicated by the rectangle, and theline extending through it denotes the preferred orientation. A, A central grating patch is set to the optimal orientation, spatial frequency, position, and size for each CRF. This stimulus provides a baseline response rate from the cell.B, The surround is investigated by placing the optimal stimulus in the center and presenting small circular patches of drifting gratings in areas beyond the CRF at a variety of locations equidistant from the center of the CRF. The dashed circles indicate the patch locations used in a typical experiment, although only one surround location was stimulated at a time. Unless otherwise noted, the parameters of the surround patch matched those of the center patch and differed only in size and location. A small gap of uniform mean luminance (typically 0.5°) was placed between the surround grating and the central grating.C, As a control measure, the center was stimulated along with an annulus in the surround in which the spatial extent of the annulus covers a region that is the sum of all of the small surround gratings. D, The surround annulus was presented alone to ensure that it does not produce excitation in the cell. Although not illustrated, we also presented the small surround patches by themselves at all locations. The peristimulus time histogram to theleft of each diagram is the response obtained from seven repetitions from one cell in this study (cell 436-13; more of this cell shown in Fig. 4).

Fig. 2.

Examples of surround asymmetry for three cells. All of these responses were obtained with the central and surround gratings set to the preferred orientation for the CRF. The radial axis is the response rate (spikes per second). The angular position indicates the position of the small surround patch (see Fig.1B). The outer dashed circle is the baseline response to center stimulation alone, measured on separate, interleaved trials. The gray region around this circle represents ±SEM. The mean response to stimulation of the center and annular surround ± SEM is indicated by a solid circle and lighter gray shading (e.g., seeC, D) but is not visible if the response is suppressed to near spontaneous levels (e.g., see A, B). If there is ongoing spontaneous activity, it is indicated by acircle and a dark shaded region (±SEM). All plots have been rotated so that the preferred orientation of the cell is vertical, with the preferred direction of motion to theright. The ends (E) and sides (S) are denoted on each plot. The tilted rectangle next to the plot indicates the true orientation and direction preference of the cell. The filled data pointsconnected by the solid line represent the mean response to stimulation of the CRF plus one of the small surround patches. Error bars denote ±1 SEM. The unfilled data points are control responses measured during presentation of the small surround gratings alone. These conditions ensure that our surround patches are truly beyond the CRF and do not drive the cell and, therefore, elicit responses near the spontaneous level of the cell. Thearrow extending outward from the origin is the SI vector (see Results), normalized to the scale of the radial axis for each cell. Thus, an SI₁ vector with a value of 1.0 indicates complete asymmetry and would extend to the edge of the polar plot. For all three cells, the left plot shows the responses when the surround is mapped with four surround locations, and theright plot is obtained during a separate presentation with eight surround locations. A, B, Surround maps from a complex cell. Note that the overall pattern of suppression is equivalent in both of these measures and that the SI₁values are similar. C, D, Surround maps from a simple cell with suppression from one side of the CRF. Again, the overall spatial pattern of surround suppression is similar in the two measures, although it is apparent that the suppressive region can also be activated by surround patches placed in the oblique regions to the left of the CRF. E, F, Complex cell with suppression from one end of the CRF. Surr., Surround.

Fig. 3.

Three examples of suppression from oblique regions of the surround. A, Simple cell with asymmetrical suppression from an oblique region. This plot was obtained with the surround grating drifting in the opposite direction, although a similar plot was obtained with the same direction in the surround.B, Simple cell exhibiting near complete suppression from one side and one oblique area. C, Complex cell with suppression from an oblique region. There is also some suppression from the adjacent end (E) and side (S) regions, but no other surround position causes any modulation of the baseline response of the cell. In this example, it is also easy to see that the surround-only control conditions do not generate any responses that are significantly different from the ongoing spontaneous activity (innermost circle) of the cell.

Fig. 4.

Detailed mapping of oblique surround suppression.A, Another example of suppression arising from an oblique region of the surround, plotted in the same format as Figures 2and 3. E, End; S, side. B, Diagram illustrating the modified reverse correlation method used to obtain a map of the CRF and the suppressive surround. An optimal drifting (conditioning) grating is displayed on one monitor for the duration of the entire block of stimuli (23 sec). During this time, stationary square wave gratings (probe) are presented for 39.5 msec on the other CRT monitor and optically superimposed with the optimal stimulus. The spatial position for each probe grating presentation is randomly chosen from 144 grid locations covering the entire CRF and surround. The spatial phase of the stationary grating is randomly chosen from one of four phases that are multiples of 90°. After all 576 stimuli (144 × 4) have been presented, there is a period of ∼3 sec in which data are stored to a file and the next presentation sequence queued. This process is repeated 100 times. The baseline response from the cell is measured every fifth trial during which the optimal grating is presented alone, without the stationary flashed gratings (these conditions did not count toward the 100 repetitions). The data are processed using our standard reverse correlation analysis software. C, Contour map of the CRF and surround obtained through the modified reverse correlation protocol. The optimal drifting grating in the center measured 4° diameter, indicated by the thick solid circle. The probe grating patch measured 5° in diameter. The 144 grid locations are indicated by the dots in the plot. Darker shading reflects spike rates higher than the maintained discharge, and lighter regions denote regions in which the probe stimulus attenuated the response. D, Average temporal response pattern from the contour map in C, taken at different spatial locations. The top trace is the average temporal response pattern from the CRF. The middle trace is the average response pattern from the suppressive zone (containing points within the fourth contour of the suppressive zone). This curve is smaller in amplitude than the center response and is normalized to facilitate comparisons with the center. The bottom panel compares the temporal responses of the center and suppressive surround, with the trace from the suppressive zone inverted. These traces show that the surround suppression peaks within 10–20 msec of the excitatory center but is more sustained than the center. Additionally, a small secondary peak occurs ∼70 msec after the first peak.

Fig. 5.

Three examples of uniform surround suppression. In all three examples, intermediate levels of suppression are observed from nearly all positions around the center. However, none of the small surround patches produce as much suppression as the annular surround stimulus. Because the suppression is spatially distributed, the SI₁ vector is negligible for each of these cells.E, End; S, side.

Fig. 6.

Examination of axially symmetric surround suppression. A, Example of a complex cell with axial surround symmetry. Strong suppression was obtained with an annulus covering the entire surround. When probed with small patches, intermediate levels of suppression were obtained from either end (E), and even weaker suppression was obtained from the oblique regions. The sides (S) of the CRF had no influence on the response of the cell. Because of strong axial symmetry, SI₁ is small, so SI₂ is shown in this plot. B, Scatterplot showing the comparison between SI₁ and SI₂ for the population of cells with overall suppression >50% (n = 37). Theunfilled circle denotes the cell shown inA.

Fig. 7.

Comparison of the amount of suppression generated by an annular surround stimulus compared with the single most suppressive surround region measured with small grating patches.A, The maximum suppression obtained from one of the eight surround locations is plotted on the x-axis, and the overall (i.e., annular) suppression is plotted on they-axis. Suppression is computed as the absolute spike response rate subtracted from the response obtained with an optimal center stimulus alone. There is a strong and significant (p < 0.0001) correlation (r = 0.83) between the two values. Thus, for most cells, the effect of stimulating the entire surround is matched by a single surround location. B, Typically, suppression is observed at more than one surround location. How far apart are the two most suppressive regions? If suppression is localized, the two most suppressive regions should be adjacent. If suppression is axially symmetric, the next most suppressive region should be 180° away. The histogram in B indicates that the two most suppressive regions were almost always adjacent.

Fig. 8.

Summary of the spatial regions producing surround suppression. A, This polar plot represents the distribution of suppressive regions from all cells that displayed at least 30% suppression with an annulus stimulus and were measured with eight surround locations (n = 40). Each data point represents an SI vector from an individual cell. The origin represents SI = 0.0, and the outer edge represents SI = 1.0. Thefilled and unfilled circles are the end points of SI₁ (n = 24) and SI₂ (n = 16) vectors, respectively. Because the SI₂ vector indicates an axis rather than a single location, we have plotted two points for each SI₂vector, one along each direction of the axis. The angular position of each point represents the location of the suppressive zone, relative to the preferred orientation of the cell, which has been aligned to vertical for all cells in this plot. The numbers in each sector indicate the numbers of cells that displayed their strongest suppression in that location. Although more cells exhibited suppression from along the end zones, the data do not statistically deviate from a uniform distribution. B, We folded the axes so that all the data in A lie in the first quadrant. Only one point was included for the SI₂cells. We then divided this quadrant into three equal regions subtending 30°. The distribution is dispersed but shows that suppression is approximately twice as likely to originate from an end zone as opposed to an oblique or side zone.

Fig. 9.

Suppression patterns with nonoptimal surround stimuli for two complex cells. The grating diagrams at theright of the polar plots indicate the orientation relationship between the central and surround gratings. The central grating is always oriented optimally, and the orientation of the surround grating was either optimal (drifted in the same or opposite direction as the center) or orthogonal. The cell in A–Cexhibits axially symmetry suppression. Accordingly, SI₁ for this cell is small, so we have plotted SI₂. InD–F, SI₁ vectors are plotted. Top row (A, D), The center and surround gratings are matched at the preferred orientation and direction. Suppression is evident from both ends (E) in Aand is absent from either side (S) position. InD, strong suppression is observed only from the bottom end. The annulus suppression is 60.3 and 100% in A andD, respectively. Middle row (B, E), The surround is oriented orthogonally to the central (optimal) grating. The suppression from the annulus and the individual surround gratings is much weaker in B andE with this configuration. The annulus suppression is 33.5 and 36.4% in B and E, respectively.Bottom row (C, F), The surround grating is oriented optimally but is drifted in the opposite (i.e., nonpreferred) direction to that of the center. In C, the pattern of suppression is the same as in A, in which suppression arises from both ends and is absent from the sides. Moreover, the suppression from the annular surround and from the smaller surround patches is slightly stronger than was present inA. The plot in F exhibits the same pattern as in D. The suppression from the annulus is 81.4 and 84% for C and F, respectively.

Fig. 10.

Data are shown from a rare example in which the orthogonal surround patch was effective at suppressing the response. InA, strong suppression occurs at the top position and the two adjacent oblique regions. Annulus suppression is 100%. InB, the orthogonal surround provides strong suppression with the annulus (50.4%), and the spatial pattern of asymmetry closely resembles the pattern in A. E, End;S, side.

Fig. 11.

Effect of varying orientation of the surround stimulus shown for a subpopulation of 42 cells. The percent suppression is defined as the relative change in response between the optimal center stimulus alone and the optimal center stimulus plus surround annulus. The percent suppression can have a negative value if the addition of the surround annulus causes an increase in response relative to the optimal center stimulus alone. Thex-axis indicates the percent suppression when the center and surround gratings are both set to the preferred value. They-axis is the suppression with optimal center stimulus and nonoptimal surround stimulus. The filled symbols(n = 35) indicate the suppression obtained with orthogonal surround gratings, and the unfilled symbols(n = 28) are conditions in which the surround grating was drifted in the opposite (nonpreferred) direction. The twohalf-filled circles near the top rightindicate the two cells shown in Figure 9. For 21 cells, all three conditions were recorded, and the corresponding data points are connected by vertical lines. Of these, seven are overlapping on the plot. The histogram at the top shows the distribution of the percentage suppression obtained with the optimal orientation used in the surround for the 42 cells shown in the scatterplot. This histogram illustrates the spread of suppression that was typical in this experiment. The histogram on theright illustrates the distribution observed when the surround grating was nonoptimal.

Fig. 12.

Tuning properties of suppressive surround zones for two cells. A, D, The orientation tuning of the CRF is shown in the top trace. The complex cell in A responded maximally to an orientation of 331° but also exhibits a strong response to a grating drifting in the opposite direction (orientation, 151°). A surround orientation tuning (bottom trace) was obtained by placing an optimal grating in the center and a second patch in the region that generated the strongest surround suppression (this relationship is schematized by the gratings at the top). The diamondsare data from three separate surround asymmetry mapping experiments and indicate the response to the optimal center stimulus and the surround annulus at the orientation specified. The response is suppressed to spontaneous levels (<SA) when the surround grating is oriented at 331°. As the orientation of the surround grating deviates from optimal, the suppression decreases and is slightly greater thanRopt (the response to the optimal center stimulus alone) at orthogonal orientations. Suppression is also obtained when the surround grating is oriented 180° from optimal. The simple cell inD is clearly direction-selective in the CRF and is narrowly tuned for orientation. The surround is bidirectional and more broadly tuned, but the strongest suppression matches the preferred orientation of the CRF. B, E, Surround field (SF) tuning of CRF (top trace) and the suppressive surround zone (bottom trace). Again, the peak excitatory SF coincides with the most inhibitory SF for the surround patch, although the inhibitory tuning is broader than the excitatory tuning. In E, responses through both left (circles) and right (squares) eyes were examined. LE and RE denote left and right eyes, respectively. C, F, Contrast response function for the inhibitory surround zone. Suppression increases monotonically with increased contrast of the surround grating. At 30% contrast in the surround, the response was almost completely attenuated. The contrast of the central patch was 35 and 30% for C and F, respectively. The average peak response for the cell in A–C andD–F, is 9.15 and 24.5 spikes/sec, respectively.

Fig. 13.

Data from three cells recorded during an LGN experiment, in which the area beyond the CRF (including both classical center and surround) was investigated for suppression. Eachcolumn represents one cell. The two cells on theright are both ON-center X cells found in layer A. The cell on the left could not be unambiguously dentified as X or Y. The top row shows the size-tuning curve for each cell. <SA, Suppression to spontaneous levels. Thesecond row shows the space–time reverse correlation map of the RF. In these plots, the solid and dashed contours represent responses to bright and dark stimuli, respectively. The centers appear prominently and are followed temporally by larger regions that correspond to the classical surround. The true spatial extent of this surround is probably much larger than it appears in the map, because the reverse correlation stimuli do not reveal weak portions of the surround well. The third rowshows the map of the CRF and the surround region, obtained with the method described in Figure 4B. The cell on thefar right was not mapped with this method, because it did not exhibit any surround suppression in other trials. Thebottom row is the surround mapping obtained with our standard grating method. The cell on the left exhibits asymmetric suppression. The middle cell shows some axial symmetry, and the one on the right exhibits very weak but uniform suppression. E, End; S, side.