Receptive field focus of visual area V4 neurons determines responses to illusory surfaces

Abstract

Illusory figures demonstrate the visual system's ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron's peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4.

Keywords: illusory contours; modal completion; nonhuman primate; visual cortex; visual perception.

Fig. 1.

Stimulus paradigm and recording technique. (A) Chronic microarray recording method. Black square indicates the implanted array location in macaque left cortical hemisphere. Sketch of the implanted microelectrode array shown below. (B) Receptive field mapping. (Upper Left) Raster plot showing the response of an example V4 unit to the repeated presentation of a circular random dot field centered at (2, −2 dva). Individual dots represent spikes as a function of time, and each row represents an individual trial. (Lower Left) Trial-averaged spike density function for the raster plot shown at Upper Left (convolved for display purposes). (Right) RFM for the same example unit. Spike density functions for each tested location of visual space are shown in black. The color axis represents the average spike rate over the 500-ms stimulus duration. White lines indicate horizontal and vertical meridians. (C) Illusory figures (IF1 and IF2) and control stimuli (CF1−3) used in the study. (D) Schematic of main task. Monkeys were required to fixate on a central fixation spot while an illusory figure or control stimulus appeared on the monitor for 1000 ms. (E) RFMs for six example units. Each grid location represents visual responses to stimuli at a given position of visual space. Color tables are normalized to each unit’s maximum firing rate. Superimposed black outlines indicate the location and size of stimulus arrays used in the main task.

Fig. 2.

V4 spiking responses to illusory figures. (A) Example RFMs. White asterisks indicate the location of peak retinotopic sensitivity, or RF focus. Dashed white lines indicate the interpolated boundary of significant visual responses (t test, P < 0.05) within the RFM. Solid white lines indicate the horizontal and vertical meridians. Location and size of main stimulus arrangement is indicated by black outlines superimposed on the RFM. (B) Raster plots and respective spike density functions showing responses to the main illusory figure (IF1, purple) and control figure (CF1, green) for the same units shown in A. Spike density functions were convolved with a 50-ms kernel for display purposes. The number of impulse discharges evoked by the main illusory figure was significantly greater than those evoked by the control figure over the displayed time course (t test, P < 0.001). (C) Units with peak retinotopic sensitivity over an isolated element of the stimulus array. All other conventions as in A. (D) Raster plots and spike density functions for the same units shown in C. Responses for the illusory figure and control condition were largely comparable (t test, P ≥ 0.05).

Fig. 3.

Relationship between RF focus and response enhancement for illusory figures. (A, Upper) Population average of evoked responses to the main illusory figure (IF1, purple) and the control stimulus (CF1, green) for all (Left) surface-focused, (Center) contour-focused, and (Right) inducer-focused V4 units. The average time course was convolved with a 50-ms kernel for display purposes. Error bars indicate the SEM across units for the posttransient period (275−1,000 ms). (A, Lower) P value as a function of time (t test for IF1 vs. CF1 across 25-ms nonoverlapping bins). Orange line demarcates α = 0.05. (B) Distribution of RF foci for both animals across the horizontal and vertical dimensions of visual space for all units with significantly greater responses to IF1 compared with CF1 (n = 299, t test, P < 0.05). The x and y axes are in visual degrees. Height and color temperature represent the proportion of recorded units with receptive field foci at each location of visual space. Black underlay indicates the location of the main stimulus arrangement (see Methods for exact scale and location). (C) Distribution of RF foci for the population of units without a significant (t test, P ≥ 0.05) firing difference between IF1 and CF1 (n = 348). Image conventions as in B.

Fig. 4.

V4 responses to different illusory and control stimuli. (A and B) Population response of surface-focused and inducer-focused units to all illusory and control stimuli used in the study. (C) Scatter plot of neural modulation to stimulus pair IF1−CF1 (abscissa) versus stimulus pair IF2−CF2 (ordinate) for the surface-focused population. Each dot represents one unit. The t-scores computed for the average activity within 80–500 ms following stimulus onset. Positive values represent greater spiking activity evoked by an illusory figure compared with a control stimulus. Note the significant correlation between stimulus pairs (R = 0.44, P < 0.001). Flanking histograms show the respective distribution of t-scores (horizontal orientation: IF1 vs. CF1; vertical orientation: IF2 vs. CF2). Blue lines indicate the median two-tailed critical t-values at α = 0.001 using trials as basis for the degrees of freedom (the exact number of trials varied with each monkey’s performance). Orange lines represent a normal distribution fitted to t-score distributions (horizontal Gaussian: μ = 3.6, σ = 3.5; vertical Gaussian: μ = 2.6, σ = 4.6). (D) Neural modulation across stimulus pairs for the inducer-focused population. No significant correlation was found (R = −0.07, P = 0.54). All other conventions as in C (horizontal Gaussian: μ = 0.60, σ = 4.0; vertical Gaussian: μ = −0.42, σ = 3.8).