Topographic signatures of global object perception in human visual cortex

Abstract

Our visual system readily groups dynamic fragmented input into global objects. How the brain represents global object perception remains however unclear. To address this question, we recorded brain responses using functional magnetic resonance imaging whilst observers viewed a dynamic bistable stimulus that could either be perceived globally (i.e., as a grouped and coherently moving shape) or locally (i.e., as ungrouped and incoherently moving elements). We further estimated population receptive fields and used these to back-project the brain activity measured during stimulus perception into visual space via a searchlight procedure. Global perception resulted in universal suppression of responses in lower visual cortex accompanied by wide-spread enhancement in higher object-sensitive cortex. However, follow-up experiments indicated that higher object-sensitive cortex is suppressed if global perception lacks shape grouping, and that grouping-related suppression can be diffusely confined to stimulated sites and accompanied by background enhancement once stimulus size is reduced. These results speak to a non-generic involvement of higher object-sensitive cortex in perceptual grouping and point to an enhancement-suppression mechanism mediating the perception of figure and ground.

Keywords: Functional magnetic resonance imaging; Global perception; Population receptive field; Searchlight back-projection; Visual perceptual grouping; Visual space.

Fig. 1

Diamond experiment$|$ Example frames of the diamond stimulus and potential response amplitude profiles when the global percept is contrasted to the local one. A. Local, no-diamond percept. Here, the diamond stimulus was perceived as four individual segments oscillating vertically and incoherently with the segments on the left/right moving towards/away from one another, respectively, or vice versa (not shown). B. Global, diamond percept. Here, the four segments were grouped together and perceived as a diamond shape oscillating horizontally and coherently behind three occluders. The gray dashed frame denotes the inferred (but occluded) contours during the global state. The white arrows indicate the perceived movement direction of the diamond stimulus. Only in the global state, the perceived and physical movement direction coincided. C. Previously suggested response amplitude profile. The whole visual field is suppressed. D. Hypothesized response amplitude profile. The segments and background region are suppressed whereas the corners and center regions are enhanced. E. Response amplitude profile when the segments and corners region are predicted during the global state. The segments region is suppressed (due to a match between bottom-up input and higher-level feedback), the corners region enhanced (due to a mismatch between bottom-up input and higher-level feedback), and activity in the background and center region unchanged. F. The same as E., but if the whole diamond shape is predicted during the global state. The center region is now also enhanced. Black lines represent the extreme positions of the diamond stimulus. Black solid lines denote the visible ungrouped diamond segments (local, no-diamond percept). Black dashed lines additionally illustrate the inferred but invisible diamond shape when the segments were grouped together (global, diamond percept). White lines denote different visual field portions. Blue areas: Suppressive effects. Red areas: Enhancement effects. Black areas: No effect.

Fig. 2

Diamond experiment$|$ Searchlight back-projections of differential brain activity as a function of contrast of interest and visual area. T-statistics surpassing a value of ±25 (first and second row) or ​± ​15 (third row) were set to that value. The saturation of colors reflects the number of vertices with a pRF inside a given searchlight plus the inverse distance of these pRFs from the searchlight center. White lines represent the extreme positions of the diamond stimulus. White solid lines denote the visible ungrouped diamond segments. White dashed lines additionally illustrate the inferred but invisible diamond shape when the segments were grouped together. D ​= ​Global, diamond percept. ND ​= ​Local, no-diamond percept. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. Pooled ​= ​Data pooled across all 5 participants. pRF ​= ​Population receptive field.

Fig. 3

Diamond experiment$|$ Classical (metric) multidimensional scaling of the dissimilarities in Supplementary Fig. S6 as a function of contrast of interest and visual area. D ​= ​Global, diamond percept. ND ​= ​Local, no-diamond percept. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. P1–P5 = Participant 1–5. Pooled ​= ​Data pooled across all 5 participants. Pooled-P1-Pooled-P5 ​= ​Data pooled across 4 participants with 1 participant left out (as indicated by the suffix).

Fig. 4

Dots experiment$|$ Example frames of the dots stimulus. A. Local, vertical condition. Here, the dots oscillated vertically and incoherently with the dots in the left/right apertures moving towards/away from one another, respectively, or vice versa (not shown), so that the apertures were perceived as four individual elements. B. Global, horizontal condition. Here, the dots in all apertures oscillated horizontally and coherently, so that the apertures could be grouped together into a global Gestalt without forming a hybrid shape. Since this stimulus was non-ambiguous, the white arrows naturally indicate the perceived and physical movement direction of the dots within the aperture.

Fig. 5

Dots experiment$|$ Searchlight back-projections of differential brain activity as a function of contrast of interest and visual area. T-statistics surpassing a value of ±35 (first and second row) or ​± ​25 (third row) were set to that value. The saturation of colors reflects the number of vertices with a pRF inside a given searchlight plus the inverse distance of these pRFs from the searchlight center. White lines represent the spatial extent of the circular apertures carrying the RDK. H ​= ​Global, horizontal condition. V ​= ​Local, vertical condition. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. Pooled ​= ​Data pooled across all 5 participants. RDK ​= ​Random dot kinematogram. pRF ​= ​Population receptive field.

Fig. 6

Dots experiment$|$ Classical (metric) multidimensional scaling of the dissimilarities in Supplementary Fig. S10 as a function of contrast of interest and visual area. H ​= ​Global, horizontal condition. V ​= ​Local, vertical condition. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. P1–P2 and P6–P8 = Participant 1–2 and 6–8. Pooled ​= ​Data pooled across all 5 participants. Pooled-P1-Pooled-P2 and Pooled-P6-Pooled-P8 ​= ​Data pooled across 4 participants with 1 participant left out (as indicated by the suffix).

Fig. 7

Dots quadrant experiment$|$ Example frames of the dots quadrant stimulus. A. Local, vertical condition. Here, the dots oscillated vertically and incoherently with the dots in the leftmost/rightmost apertures moving towards/away from one another, respectively, or vice versa (not shown), so that the apertures were perceived as four individual elements. B. Global, horizontal condition. Here, the dots in all apertures oscillated horizontally and coherently, so that the apertures could be grouped together into a global Gestalt without forming a hybrid shape. Since this stimulus was non-ambiguous, the white arrows naturally indicate the perceived and physical movement direction of the dots within the aperture. The dots quadrant stimulus was only presented in the top-right visual field quadrant. For reasons of visibility, we cut out the stimulus region to provide a zoomed-in view, as indicated by the black dashed lines and the black double-headed arrows.

Fig. 8

Dots quadrant experiment$|$ Searchlight back-projections of differential brain activity as a function of contrast of interest and visual area. T-statistics surpassing a value of ±25 (first and second row) or ​± ​15 (third row) were set to that value. The saturation of colors reflects the number of vertices with a pRF inside a given searchlight plus the inverse distance of these pRFs from the searchlight center. White lines represent the spatial extent of the circular apertures carrying the RDK. H ​= ​Global, horizontal condition. V ​= ​Local, vertical condition. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. Pooled ​= ​Data pooled across all 5 participants. RDK ​= ​Random dot kinematogram. pRF ​= ​Population receptive field.

Fig. 9

Dots quadrant experiment$|$ Classical (metric) multidimensional scaling of the dissimilarities in Supplementary Fig. S14 as a function of contrast of interest and visual area. H ​= ​Global, horizontal condition. V ​= ​Local, vertical condition. Fix ​= ​Fixation baseline. VLOC = Ventral-and-lateral occipital complex. P1, P6, and P9–P11 ​= ​Participant 1, 6, and 9–11. Pooled ​= ​Data pooled across all 5 participants. Pooled-P1, Pooled-P6, and Pooled-P9-Pooled-P11 ​= ​Data pooled across 4 participants with 1 participant left out (as indicated by the suffix).