Geometric cues influence head direction cells only weakly in nondisoriented rats

Abstract

The influential hypothesis that environmental geometry is critical for spatial orientation has been extensively tested behaviorally, and yet findings have been conflicting. Head direction (HD) cells, the neural correlate of the sense of direction, offer a window into the processes underlying directional orientation and may help clarify the issue. In the present study, HD cells were recorded as rats foraged in enclosures of varying geometry, with or without simultaneous manipulation of landmarks and self-motion cues (path integration). All geometric enclosures had single-order rotational symmetry and thus completely polarized the environment. They also had unique features, such as corners, which could, in principle, act as landmarks. Despite these strongly polarizing geometric cues, HD cells in nondisoriented rats never rotated with these shapes. In contrast, when a cue card (white or gray) was added to one wall, HD cells readily rotated with the enclosure. When path integration was disrupted by disorienting the rat, HD cells rotated with the enclosure even without the landmark. Collectively, these findings indicate that geometry exerts little or no influence on heading computations in nondisoriented rats, but it can do so in disoriented rats. We suggest that geometric processing is only a weak influence, providing a backup system for heading calculations and recruited only under conditions of disorientation.