Heading computation in the human retrosplenial complex during full-body rotation

The retrosplenial complex (RSC) plays a crucial role in spatial orientation by computing heading direction and translating between distinct spatial reference frames. While invasive studies allow investigating heading computation in moving animals, established non-invasive analyses of human brain dynamics are restricted to stationary setups. To investigate the role of the RSC in heading computation of actively moving humans, we used a Mobile Brain/Body Imaging approach synchronizing electroencephalography with motion capture and virtual reality. Data from physically rotating participants were contrasted with rotations based only on visual flow. Varying rotation velocities were accompanied by pronounced beta synchronization during physical rotation. In addition, heading computation based only on visual flow replicated alpha desynchronization in the RSC, which was absent during physical rotation. These results suggest an involvement of the human RSC in heading computation based on vestibular input and implicate revisiting traditional findings of alpha desynchronization during spatial orientation in movement-restricted participants. Heading computation is fundamental for spatial orientation in the human and other species. The registration of moment-to-moment changes in orientation with respect to an allocentric reference direction provides information about an animal’s current heading relative to the environment. This is accomplished by the integration of vestibular, proprioceptive, and visual signals providing information about linear and angular velocity signals of the head, the relative position of the head with respect to the trunk, and information about stable aspects of the environment, respectively.1 Single cell recordings in freely behaving animals identified several brain structures involved in heading computation, including the retrosplenial cortex (RSC).2, 3 The RSC receives input from the visual system and from head direction cells in the thalamic nuclei.4 It also hosts subpopulations of heading-sensitive cells that are sentient to local features of the environment, while other cells exhibit mixed activity patterns related to both local and global heading computation.5 These findings suggest that neural activity in the RSC subserves the integration of information about the local and global environment, integrating egocentrically coded landmark cues based on sensory fusion (vision and proprioception)6 with allocentric heading information originating from the Papez circuit.7 This allows the compensation of the rotational offset between egocentric and allocentric spatial representations, routed from the parietal and medial temporal cortices, providing the necessary information for translating between both egocentric and allocentric spatial representational frames in the RSC.8