Top-down activation of shape-specific population codes in visual cortex during mental imagery

Abstract

Visual imagery is mediated via top-down activation of visual cortex. Similar to stimulus-driven perception, the neural configurations associated with visual imagery are differentiated according to content. For example, imagining faces or places differentially activates visual areas associated with perception of actual face or place stimuli. However, while top-down activation of topographically specific visual areas during visual imagery is well established, the extent to which internally generated visual activity resembles the fine-scale population coding responsible for stimulus-driven perception remains unknown. Here, we sought to determine whether top-down mechanisms can selectively activate perceptual representations coded across spatially overlapping neural populations. We explored the precision of top-down activation of perceptual representations using neural pattern classification to identify activation patterns associated with imagery of distinct letter stimuli. Pattern analysis of the neural population observed within high-level visual cortex, including lateral occipital complex, revealed that imagery activates the same neural representations that are activated by corresponding visual stimulation. We conclude that visual imagery is mediated via top-down activation of functionally distinct, yet spatially overlapping population codes for high-level visual representations.

Figure 1.

The experimental design. A, During the imagery task, participants were cued (via either a high or low pitch auditory tone) on a trial-by-trial basis to imagine either X or O. The intertrial interval (ITI) was randomized between 3 and 12 s. B, During the perceptual task, participants were instructed to watch a series of visually presented letter stimuli (X or O; duration 250 ms, ITI 3–12 s) and press the same button following the presentation of each stimulus.

Figure 2.

Activation results for the conventional univariate analyses. A, During the imagery task, comparisons against baseline confirmed relative increases in activity distributed throughout visual cortex, including cuneus (Cu), lingual gyrus (LiG) and middle temporal gyrus (MTG). Event-related increases were also observed within superior temporal sulcus/Heschl's gyrus (STG/HG). B, During the perceptual task, a similar network of brain areas was also activated, with peaks in inferior occipital gyrus (IOG), middle occipital gyrus (MOG), middle temporal gyrus (MTG) and fusiform gyrus (FG). Beyond visual cortex, precentral gyrus (PrG) was also active during the perceptual task. All activation maps are corrected for multiple comparisons (p_FDR < 0.05). Shaded brain areas were beyond the functional data acquisition field of view within at least one subject, and therefore not included in the group analyses. The calcarine sulcus (CcS) is indicated by the black line superimposed over coronal slices.

Figure 3.

A, B, Train-test neural classification was used to index population coding during visual imagery (A) and perception (B). C, Pattern analyses were performed in aLOC and pLOC of both hemispheres, shown here on a rendered brain surface. Shading indicates the regions beyond the functional data acquisition field of view. D, Differential population coding of the two alternative states of imagery was observed within all subregions of area LOC. E, During the perceptual task, there was a trend toward above-chance discrimination across all subregions of LOC, however, perceptual classification was only significantly above-chance within the left and right pLOC. Error bars represent ± 1 SEM, calculated across participants.

Figure 4.

Cross-generalization MVPA reveals the coding similarity between visual imagery and perception. A, First, a perceptual classifier was trained to discriminate between patterns of visual activity associated with alternative perceptual conditions during the perceptual task. Second, the perceptual classifier was used to predict the imagery state associated with visual activity observed during the imagery task. B, Cross-generalization pattern analyses were performed in aLOC and pLOC of both hemispheres, shown here on a rendered brain surface with shading to indicate the regions beyond the functional data acquisition field of view. C, Accurate cross-generalization between perception and imagery confirms significant similarity between respective population coding in the left aLOC. Error bars represent ± 1 SEM, calculated across participants.

Figure 5.

Population coding during visual imagery and perception. A, Searchlight MVPA revealed differential population coding of the two alternative states of imagery within the high-level visual areas, including inferior occipital gyrus (IOG), middle occipital gyrus (MOG), fusiform gyrus (FG) and middle temporal gyrus (MTG). Searchlight analyses also identified discriminative clusters in superior temporal gyrus/Heschl's gyrus (STG/HG), and anterior insula/frontal operculum (aI/fO). B, Searchlight MVPA of visual perception revealed a similar network of discriminative clusters, with the exception of STG/HG. Classification accuracies are shown for voxels that survived correction for multiple comparisons (FDR <5%), and shading indicates brain areas that were beyond the functional data acquisition field of view within at least one subject, and therefore not included in the group analyses. For reference, anterior lateral occipital complex (aLOC), posterior lateral occipital complex (pLOC) and calcarine sulcus (CcS) are superimposed in black.