Dissociable Neural Systems for Recognizing Places and Navigating through Them

Abstract

When entering an environment, we can use the present visual information from the scene to either recognize the kind of place it is (e.g., a kitchen or a bedroom) or navigate through it. Here we directly test the hypothesis that these two processes, what we call "scene categorization" and "visually-guided navigation", are supported by dissociable neural systems. Specifically, we manipulated task demands by asking human participants (male and female) to perform a scene categorization, visually-guided navigation, and baseline task on images of scenes, and measured both the average univariate responses and multivariate spatial pattern of responses within two scene-selective cortical regions, the parahippocampal place area (PPA) and occipital place area (OPA), hypothesized to be separably involved in scene categorization and visually-guided navigation, respectively. As predicted, in the univariate analysis, PPA responded significantly more during the categorization task than during both the navigation and baseline tasks, whereas OPA showed the complete opposite pattern. Similarly, in the multivariate analysis, a linear support vector machine achieved above-chance classification for the categorization task, but not the navigation task in PPA. By contrast, above-chance classification was achieved for both the navigation and categorization tasks in OPA. However, above-chance classification for both tasks was also found in early visual cortex and hence not specific to OPA, suggesting that the spatial patterns of responses in OPA are merely inherited from early vision, and thus may be epiphenomenal to behavior. Together, these results are evidence for dissociable neural systems involved in recognizing places and navigating through them.SIGNIFICANCE STATEMENT It has been nearly three decades since Goodale and Milner demonstrated that recognizing objects and manipulating them involve distinct neural processes. Today we show the same is true of our interactions with our environment: recognizing places and navigating through them are neurally dissociable. More specifically, we found that a scene-selective region, the parahippocampal place area, is active when participants are asked to categorize a scene, but not when asked to imagine navigating through it, whereas another scene-selective region, the occipital place area, shows the exact opposite pattern. This double dissociation is evidence for dissociable neural systems within scene processing, similar to the bifurcation of object processing described by Goodale and Milner (1992).

Keywords: categorization; navigation; occipital place area; parahippocampal place area; retrosplenial complex; scene recognition.

Figure 1.

Example images from the experimental scans. The correct answers for the categorization task (from left to right) are bedroom, kitchen, living room. The correct answers for the navigation task (from left to right) are “left”, “center”, “right”. Note that each task was performed on the exact same image.

Figure 2.

A, Example ROIs, labeled accordingly, from one participant, displayed on the cortical surface. Specifically, using independent data from the localizer runs, PPA, OPA, and RSC were localized bilaterally as regions that responded more strongly to scenes than objects (p < 10⁻⁴, uncorrected). B, The average neural response (percentage signal change) to the categorization and navigation tasks for each independently defined scene-selective ROI, labeled accordingly. C, The average neural response (percentage signal change) to the categorization, navigation, and one-back tasks for each independently defined scene-selective ROI in 11 of 20 participants, labeled accordingly. Error bars represent ± 1 SEM. Asterisks indicate a significant difference in responses between conditions (p < 0.05).

Figure 3.

Classification accuracy from the linear SVM in scene-selective ROIs. In PPA, classification accuracy was above chance for the categorization task, but not the navigation task. By contrast, in OPA, classification accuracy was above chance for both tasks. In RSC, classification accuracy was not above chance for either task. Error bars represent ± 1 SEM. Asterisks indicate classification accuracy significantly greater than chance (p < 0.05).

Figure 4.

A group-level analysis across the entire slice prescription identified regions that responded more during the categorization task than during the navigation task (Cat > Nav), and regions that responded more during the navigation task than during the categorization task (Nav > Cat) At a threshold of p < 0.01 (FWE corrected) we found (1) a bilateral region that responded more to the categorization task than during the navigation task overlapping the group-level functionally defined PPA, and (2) regions that responded more during the navigation task than during the categorization task overlapping the group-level functionally defined OPA. Note the lack of activation to both contrasts in RSC.