What’s the relationship between world-centered (allocentric) and self-centered (egocentric) frames of spatial coding in the hippocampus during navigation?

Jordan Carpenter, Jan Sigurd Blackstad, David Tingley, Valentin A. Normand, Edvard I. Moser, May-Britt Moser, Benjamin A. Dunn. Investigating egocentric tuning in hippocampal CA1 neurons. Journal of Neuroscience, 13 August 2024, e0040242024; DOI: 10.1523/JNEUROSCI.0040-24.2024

Abstract
Navigation requires integrating sensory information with a stable schema to create a dynamic map of an animal’s position using egocentric and allocentric coordinate systems. In the hippocampus, place cells encode allocentric space, but their firing rates may also exhibit directional tuning within egocentric or allocentric reference frames. We compared experimental and simulated data to assess the prevalence of tuning to egocentric bearing (EB) among hippocampal cells in rats foraging in an open field. Using established procedures, we confirmed egocentric modulation of place cell activity in recorded data; however, simulated data revealed a high false positive rate. When we accounted for false positives by comparing with shuffled data that retain correlations between the animal’s direction and position, only a very low number of hippocampal neurons appeared modulated by EB. Our study highlights biases affecting false positive rates and provides insights into the challenges of identifying egocentric modulation in hippocampal neurons.”

Significance Statement

“This study investigates the relationship between world-centered (allocentric) and self-centered (egocentric) frames of spatial coding in the hippocampus during navigation. Through targeted electrophysiological single-unit recordings in hippocampal CA1 area, complemented by simulations of spatially modulated neurons, we find a compelling lack of support in free-foraging rats for recent proposals that the hippocampus relies on internal egocentric signals in relation to reference points distributed through the environment. Our work reveals that ego­centric signals in CA1 may be strongly biased by stereotypical behavioral patterns. The findings suggest that in free-foraging rodents, the principal framework for location coding is allocentric.”

Jordan Carpenter, Jan Sigurd Blackstad, David Tingley, Valentin A. Normand, Edvard I. Moser, May-Britt Moser, Benjamin A. Dunn. Investigating egocentric tuning in hippocampal CA1 neurons. Journal of Neuroscience, 13 August 2024, e0040242024; DOI: 10.1523/JNEUROSCI.0040-24.2024