Gravity influences the visual representation of object tilt in parietal cortex

Abstract

Sensory systems encode the environment in egocentric (e.g., eye, head, or body) reference frames, creating inherently unstable representations that shift and rotate as we move. However, it is widely speculated that the brain transforms these signals into an allocentric, gravity-centered representation of the world that is stable and independent of the observer's spatial pose. Where and how this representation may be achieved is currently unknown. Here we demonstrate that a subpopulation of neurons in the macaque caudal intraparietal area (CIP) visually encodes object tilt in nonegocentric coordinates defined relative to the gravitational vector. Neuronal responses to the tilt of a visually presented planar surface were measured with the monkey in different spatial orientations (upright and rolled left/right ear down) and then compared. This revealed a continuum of representations in which planar tilt was encoded in a gravity-centered reference frame in approximately one-tenth of the comparisons, intermediate reference frames ranging between gravity-centered and egocentric in approximately two-tenths of the comparisons, and in an egocentric reference frame in less than half of the comparisons. Altogether, almost half of the comparisons revealed a shift in the preferred tilt and/or a gain change consistent with encoding object orientation in nonegocentric coordinates. Through neural network modeling, we further show that a purely gravity-centered representation of object tilt can be achieved directly from the population activity of CIP-like units. These results suggest that area CIP may play a key role in creating a stable, allocentric representation of the environment defined relative to an "earth-vertical" direction.

Keywords: allocentric; gravity; multisensory; parietal cortex; spatial pose; visual orientation.