Extrinsic reference frames modify the neural substrates of object-location representations

Edgar Chan, Oliver Baumann, Mark A. Bellgrove, Jason B. Mattingley

The ability to form spatial representations of object locations is an important component of successful spatial navigation. Evidence from behavioral studies suggests that environmental features that have a salient coordinate axis (e.g., a rectangular building or a geometrical room) may provide a reference frame for the encoding of object-location information. Here we used functional magnetic resonance imaging (fMRI) to determine the brain networks engaged when object-location representations are stored with respect to an extrinsic reference frame. Participants learned the layout of an object array in an active, virtual-navigation paradigm. A square mat positioned on the floor of the virtual arena acted as the extrinsic reference frame. Knowledge of the spatial arrangement of the object array was probed while participants underwent fMRI, using a spatial judgment task that required them to imagine orientations of the learned array that were either aligned or misaligned with the geometry of the mat. Consistent with previous findings, participants responded faster and were more accurate when the imagined orientation was aligned, as opposed to misaligned, with the extrinsic reference frame. Analysis of the fMRI data revealed important differences in brain activity between the two conditions. Significantly greater activity was observed in the aligned condition compared with the misaligned condition across a bilateral network of brain areas that included the inferior occipital gyri, inferior and middle temporal gyri, and fusiform gyri. By contrast, activity in the misaligned condition was significantly greater than in the aligned condition in bilateral dorsolateral prefrontal and anterior cingulate cortex, and in the right anterior prefrontal and anterior insular cortex. These results suggest that retrieval of spatial locations that are aligned with an extrinsic reference frame involve direct access to detailed and accurate representations within the ventral visual pathway, whereas spatial locations that are misaligned with this reference frame are only weakly represented and require active inferential processes through the recruitment of prefrontal cortical networks. Our findings are consistent with a "reference direction" account of spatial memory, which posits that inter-object spatial relationships are primarily encoded with respect to specified reference directions.