How environment and self‐motion combine in neural representations of space

• Published in: The Journal of physiology Vol. 594; no. 22; pp. 6535 - 6546
• Main Authors: Evans, Talfan, Bicanski, Andrej, Bush, Daniel, Burgess, Neil
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 15.11.2016; John Wiley and Sons Inc
• Subjects: Animals; Cognitive and Behavioural Neuroscience; Environment; Head - physiology; Humans; Models, Neurological; Motion; Neurons - physiology; Orientation - physiology; Space Perception - physiology; Symposium Review; Symposium section reviews: Neural circuits for spatial computation
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP270666

Estimates of location or orientation can be constructed solely from sensory information representing environmental cues. In unfamiliar or sensory‐poor environments, these estimates can also be maintained and updated by integrating self‐motion information. However, the accumulation of error dictates that updated representations of heading direction and location become progressively less reliable over time, and must be corrected by environmental sensory inputs when available. Anatomical, electrophysiological and behavioural evidence indicates that angular and translational path integration contributes to the firing of head direction cells and grid cells. We discuss how sensory inputs may be combined with self‐motion information in the firing patterns of these cells. For head direction cells, direct projections from egocentric sensory representations of distal cues can help to correct cumulative errors. Grid cells may benefit from sensory inputs via boundary vector cells and place cells. However, the allocentric code of boundary vector cells and place cells requires consistent head‐direction information in order to translate the sensory signal of egocentric boundary distance into allocentric boundary vector cell firing, suggesting that the different spatial representations found in and around the hippocampal formation are interdependent. We conclude that, rather than representing pure path integration, the firing of head‐direction cells and grid cells reflects the interface between self‐motion and environmental sensory information. Together with place cells and boundary vector cells they can support a coherent unitary representation of space based on both environmental sensory inputs and path integration signals. Spatial navigation is thought to rely on complementary information from environmental sensory cues and an internal path integration system. An estimate of one's location within an environment can be constructed purely from environmental sensory information, however in sensory‐poor environments (e.g. in the dark or far from geometrical cues) this estimate can also be maintained by integrating self‐motion information, a process known as path integration (red dashed line). Path integration tracks changes in both the angular and translational components of movement, but is subject to drift over time due to the accumulation of error. Head direction cells (HDCs) and grid cells (GCs) are thought to represent the neural bases of these components and are known to be anchored to environmental cues, correcting for drift (mountain and purple arrows). Information on the distance to the boundaries of an environment is provided by boundary vector cells (BVCs).