Brain mechanisms for simple perception and bistable perception

Abstract

When faced with ambiguous sensory inputs, subjective perception alternates between the different interpretations in a stochastic manner. Such multistable perception phenomena have intrigued scientists and laymen alike for over a century. Despite rigorous investigations, the underlying mechanisms of multistable perception remain elusive. Recent studies using multivariate pattern analysis revealed that activity patterns in posterior visual areas correlate with fluctuating percepts. However, increasing evidence suggests that vision--and perception at large--is an active inferential process involving hierarchical brain systems. We applied searchlight multivariate pattern analysis to functional magnetic resonance imaging signals across the human brain to decode perceptual content during bistable perception and simple unambiguous perception. Although perceptually reflective activity patterns during simple perception localized predominantly to posterior visual regions, bistable perception involved additionally many higher-order frontoparietal and temporal regions. Moreover, compared with simple perception, both top-down and bottom-up influences were dramatically enhanced during bistable perception. We further studied the intermittent presentation of ambiguous images--a condition that is known to elicit perceptual memory. Compared with continuous presentation, intermittent presentation recruited even more higher-order regions and was accompanied by further strengthened top-down influences but relatively weakened bottom-up influences. Taken together, these results strongly support an active top-down inferential process in perception.

Keywords: Granger causality; MVPA; ambiguous images; fMRI; visual perception.

Fig. 1.

Experimental paradigm and behavioral results. (A) Altered Necker cube and Rubin face-vase images (Upper) presented in the unambiguous (UnAmb) condition and the original images (Lower) presented in the ambiguous (Amb) and discontinuous (Disc) conditions. (B) Experimental design for each condition. Each UnAmb run contained 16 blocks (4 blocks per image), and each Amb and Disc run contained 6 blocks (3 blocks per image). The fMRI frames used for decoding are indicated in the graph. (C) Frequency histograms showing the distribution of percept durations in each subject (n = 11 for Amb; n = 8 for Disc). Percept durations were sorted into nine bins for both Amb and Disc data (combined across both percepts of each ambiguous image). Thick black lines indicate the mean across subjects.

Fig. 2.

Searchlight MVPA results for Necker cube in the UnAmb and Amb conditions and the hemodynamic delay control analysis. (Left) Searchlight MVPA group analysis results for the UnAmb condition and different frames of the Amb condition. Maps were thresholded at P < 0.05, corrected for multiple comparisons. LH, left hemisphere; RH, right hemisphere. (Right) Percept-selective voxels were chosen from searchlight results of each Amb frame and separated according to their preferred UnAmb images. fMRI time courses were averaged across each voxel group for button presses indicating preferred percept (green) vs. nonpreferred percept (red). Data were pooled across the four selective voxel groups (preferring face, vase, the two perspectives of Necker cube, respectively) and averaged across subjects (n = 11). Dashed boxes indicate the corresponding frame of searchlight results from which the selective voxels were chosen. Time point 0 is the frame containing the button press. Error bars denote SEM across subjects.

Fig. 3.

Comparison of searchlight MVPA results between conditions. (A) Comparison between UnAmb and Amb conditions. (B) Comparison between Amb and Disc conditions. Results from Necker cube and Rubin face-vase stimuli are shown in the Upper and Lower row, respectively. All results are from group analysis, thresholded at P < 0.05, corrected for multiple comparisons. The Amb condition results were combined across frames −1 to 3. The Disc condition results were combined across frames 0 to 3. LH, left hemisphere; RH, right hemisphere.

Fig. 4.

ROIs and GC analysis results. (A) All ROIs used for GC analysis are plotted on a standard brain surface. ROIs are ordered according to their posterior–anterior position in the Talairach space. Their abbreviated names are shown on the bottom of each graph. For ROI details, see Table S1. (B) Percentage of significant voxel pairs for each ROI pair in each direction under UnAmb (Left), Amb (Center), and Disc (Right) conditions. Direction of GC influence is from the source ROI to the sink ROI. (C) Changes in connectivity strengths between conditions. Changes from UnAmb to Amb (Left), Amb to Disc (Center), and UnAmb to Disc (Right) conditions with significant increases (red) and decreases (blue) of connectivity strength (McNemar test; P < 0.05, FDR corrected).

Fig. 5.

Total causal flow (out-in degree) for each ROI in each condition. ROIs are ordered posterior (left-most) to anterior (right-most). Out-in degrees were computed for each ROI using binary connectivity matrices thresholded at 50%. The mean and SEM across subjects are plotted (n = 11, 11, and 8 for UnAmb, Amb, and Disc condition, respectively). P values of the ROI × condition interaction effect from a two-way ANOVA are indicated in the graph.

Fig. 6.

GC patterns during perceptual switch vs. maintenance. Percentages of significant voxel pairs were compared between the putative bottom-up (posterior-to-anterior) and top-down (anterior-to-posterior) directions across all ROI pairs by a Wilcoxon signed-rank test (P values are indicated in the graph). The bar graphs plot the mean and SEM across ROI pairs.

Fig. 7.

A conceptual model that can account for our results. (A) Summary of the GC results in the three conditions. Regions A and B represent abstract lower-order and higher-order regions, respectively. Dashed lines, potential (e.g., anatomical) but weak or absent directed influence (as measured by GC). Solid lines indicate GC influences. Thicker lines indicate stronger GC influences. (B) A model that can explain both our MVPA and GC results. Left column, percept 1 is dominant. Right column: percept 2 is dominant. Red arrows, excitatory connections; purple lines, inhibitory connections. Tables on the right describe known (black) or currently unknown (green) fMRI and firing rate (FR) observations about whether activity in lower- or higher-level regions correlates with subjective percept in the three experimental conditions. The fMRI observations come from the MVPA results reported herein. In this graph, region A represents roughly early visual areas and region B represents roughly frontal and anterior temporal regions. We note that this two-level model is highly abstracted; in reality, there are many levels of brain regions in the hierarchy.