Two scene navigation systems dissociated by deliberate versus automatic processing

Abstract

Successfully navigating the world requires avoiding boundaries and obstacles in one's immediately-visible environment, as well as finding one's way to distant places in the broader environment. Recent neuroimaging studies suggest that these two navigational processes involve distinct cortical scene processing systems, with the occipital place area (OPA) supporting navigation through the local visual environment, and the retrosplenial complex (RSC) supporting navigation through the broader spatial environment. Here we hypothesized that these systems are distinguished not only by the scene information they represent (i.e., the local visual versus broader spatial environment), but also based on the automaticity of the process they involve, with navigation through the broader environment (including RSC) operating deliberately, and navigation through the local visual environment (including OPA) operating automatically. We tested this hypothesis using fMRI and a maze-navigation paradigm, where participants navigated two maze structures (complex or simple, testing representation of the broader spatial environment) under two conditions (active or passive, testing deliberate versus automatic processing). Consistent with the hypothesis that RSC supports deliberate navigation through the broader environment, RSC responded significantly more to complex than simple mazes during active, but not passive navigation. By contrast, consistent with the hypothesis that OPA supports automatic navigation through the local visual environment, OPA responded strongly even during passive navigation, and did not differentiate between active versus passive conditions. Taken together, these findings suggest the novel hypothesis that navigation through the broader spatial environment is deliberate, whereas navigation through the local visual environment is automatic, shedding new light on the dissociable functions of these systems.

Keywords: Navigation; Occipital place area; Retrosplenial complex; Scene perception; fMRI.

Figure 1.. Schematic representation of a single trial of the maze-navigation task.

On each trial, participants (labeled as Player) navigated through a maze structure in first-person viewpoint. First, participants made an approach to the cue location, which triggered the floor color to change for 2 seconds, indicating the navigation condition on each trial. Second, given a particular color, the participant then engaged in one of four navigation conditions: (i) the active navigation condition requiring individuals to move using button pressing; (ii) the passive-navigation condition requiring individuals to watch navigation without pressing any buttons; (iii) the no-navigation condition requiring individuals to wait for a specified duration without pressing any buttons before being ‘teleported’ to the goal, and (iv) the effortful-navigation condition (included for the purposes of another study) requiring individuals to rapidly press buttons in order to move. The center image shows the top view of one of the four maze structures (i.e., single right turn; the others were single left turn, right-then-left turn, left-then-right turn). Participants never saw the maze structure from this top view perspective.

Figure 2.. Localization of scene-selective regions (OPA, RSC, and PPA) in a sample participant.

Each region was individually localized for each participant using the Scene>Object contrast in the functional localizer task, using a voxel-wise threshold of p<10⁻⁶.

Figure 3.. Effects of the broader spatial environment, active navigation, and the passive visual experience of navigation, in RSC and OPA.

(A) Difference scores indexing representation of the broader spatial environment were calculated by subtracting the response to simple maze navigation from that to complex maze navigation, separately for the active and passive navigation conditions. RSC showed robust responses to information about the broader environment during active, but not passive navigation, while OPA did not respond differently to complex versus simple mazes, nor to active versus passive navigation. (B) Difference scores indexing representation of the passive experience of navigation through scenes were calculated by subtracting the response to the no navigation condition (i.e., simply looking at the maze, without moving through it) from that to the passive navigation condition. OPA responded significantly more than RSC to the passive visual experience of navigation. * p<0.05, *** p<0.001. Error bars indicate standard error of the mean. Distributions of individual data are overlaid on each bar plot.

Figure 4.

Results of whole-brain analyses. Consistent with ROI analyses, an interaction between navigation condition (active, passive) and maze structure (complex, simple) was observed in a region overlapping with RSC (p_FWE<0.05 cluster corrected, voxelwise threshold p<0.005). A region overlapping with OPA exhibited greater response to passive navigation compared to the no-navigation condition (p_FWE<0.05 cluster corrected, voxelwise threshold p<0.001). For visualization of ROI location, spheres (r=8mm) were generated around the average peak position of each scene-selective region. RSC: retrosplenial complex, OPA: occipital place area, PPA: parahippocampal place area.