Medial parietal cortex encodes perceived heading direction in humans

Abstract

The ability to encode and update representations of heading direction is crucial for successful navigation. In rats, head-direction cells located within the limbic system alter their firing rate in accordance with the animal's current heading. To date, however, the neural structures that underlie an allocentric or viewpoint-independent sense of direction in humans remain unknown. Here we used functional magnetic resonance imaging (fMRI) to measure neural adaptation to distinctive landmarks associated with one of four heading directions in a virtual environment. Our experiment consisted of two phases: a "learning phase," in which participants actively navigated the virtual maze; and a "test phase," in which participants viewed pairs of images from the maze while undergoing fMRI. We found that activity within the medial parietal cortex--specifically, Brodmann area 31--was modulated by learned heading, suggesting that this region contains neural populations involved in the encoding and retrieval of allocentric heading information in humans. These results are consistent with clinical case reports of patients with acquired lesions of medial posterior brain regions, who exhibit deficits in forming and recalling links between landmarks and directional information. Our findings also help to explain why navigation disturbances are commonly observed in patients with Alzheimer's disease, whose pathology typically includes the cortical region we have identified as being crucial for maintaining representations of heading direction.

Figure 1.

Schematics of the virtual environment and spatial judgment task used to examine the representation of allocentric heading. a, Aerial perspective of the virtual maze (never seen by participants) used in the learning phase. The red dots indicate the locations of the 20 symbols that acted as landmarks; the single blue spot represents the center of the virtual maze. The arrows represent the 16 different vantage points from which participants viewed the landmarks during the test phase. b, Example of a single image viewed by participants during the test phase. c, Sequence of events in a typical experimental trial, consisting of a pair of images depicting landmarks representing the same heading direction (repeated trials) or different heading directions (novel trials). Note that participants never viewed the same landmark symbol twice within a trial pair.

Figure 2.

Mean values, expressed as a percentage of optimal efficiency, for spatial and temporal behavioral measures (±1 SE) across the five learning sessions.

Figure 3.

Mean BOLD activity for the comparison of novel heading > repeated heading. MR brain slices are from an MNI-normalized template brain and show heading-direction-selective activity in the left medial parietal cortex (a height threshold of T = 5.18, p = 0.001) was used for display purposes. a, Sagittal view. b, Coronal view. c, Axial view. d, Time course of the average percentage BOLD signal change for the activation cluster shown in a–c. The 0 point on the x-axis represents the onset of the first image within a trial pair.