How reliable are visual context effects in the parahippocampal place area?

Abstract

The parahippocampal place area (PPA) is a region of human cortex that responds more strongly to visual scenes (e.g., landscapes or cityscapes) than to other visual stimuli. It has been proposed that the primary function of the PPA is encoding of contextual information about object co-occurrence. Supporting this context hypothesis are reports that the PPA responds more strongly to strong-context than to weak-context objects and more strongly to famous faces (for which contextual associations are available) than to nonfamous faces. We reexamined the reliability of these 2 effects by scanning subjects with functional magnetic resonance imaging while they viewed strong- and weak-context objects, scrambled versions of these objects, and famous and nonfamous faces. "Contextual" effects for objects were observed to be reliable in the PPA at slow presentation rates but not at faster presentation rates intended to discourage scene imagery. We were unable to replicate the earlier finding of preferential PPA response to famous versus nonfamous faces. These results are difficult to reconcile with the hypothesis that the PPA encodes contextual associations but are consistent with a competing hypothesis that the PPA encodes scenic layout.

Figure 1.

Examples of stimuli. Eighty-eight stimuli were collected for each of the 8 stimulus categories, which were presented at different presentation rates in Experiments 1 and 2. Famous faces were contemporary Hollywood celebrities, whereas famous places were well-known landmarks from around the world. Objects in the strong-context condition in this stimulus set were associated strongly with a specific context (e.g., a slot machine is associated with a casino), whereas objects in the weak-context condition did not have similar associations.

Figure 2.

fMRI response within the left PPA, right PPA, and left PHC for (a) Experiment 1 and (b) Experiment 2. The PPA was functionally defined in each subject as the set of voxels that responded more strongly to places (famous and nonfamous) than to objects (strong context and weak context). The PHC was functionally defined as the set of voxels that responded more strongly to strong-context objects than to weak-context objects in a group analysis. Significance markers reflect the results of 4 pairwise comparisons (famous vs. nonfamous faces, famous vs. nonfamous places, strong-context vs. weak-context objects, and scrambled strong context vs. scrambled weak context); error bars are ±1 standard error of the mean for each condition. Greater response was observed for strong-context objects than for weak-context objects in the left PPA and PHC in Experiment 1 and in all 3 ROIs in Experiment 2. However, a similar “strong” > “weak” advantage was observed for scrambled stimuli in Experiment 1, which is counter to what would be predicted by the context hypothesis. Neither the PPA nor the PHC responds differentially to famous versus nonfamous faces (contrary to previous reports), although they did respond more strongly to famous than to nonfamous places.

Figure 3.

The magnitude and significance of the place and context effects within PHC, plotted on a subject-by-subject basis. “Place effect” is defined as greater response to places (famous and nonfamous) than to objects (strong and weak context); “context effect” is defined as greater response to strong-context objects than to weak-context objects. Red diamonds indicate that the effect was significant at the individual subject level (P < 0.05); blue diamonds indicate a nonsignificant subjectwise effect. Whereas the place effect was significant in almost every subject, the context effect was only reliable in a minority of subjects.

Figure 4.

Anatomical loci of the place and context effects in the PHC region in Experiment 2. As in Figure 3, the place effect is defined as greater response to places than to objects, whereas the context effect is defined as greater response to strong-context objects than to weak-context objects. A more stringent threshold was applied to the place effect (P < 0.0001) than to the context effect (P < 0.01) in order to facilitate comparison of the loci of the 2 effects when plotted at comparable extent. The 2 effects exhibit largely overlapping locations in bilateral PHC/lingual gyrus, although the territory affected by place effect extends more posteriorly. (Note that activations outside of the PHC region are not shown; see text.)