Neural dynamics indicate parallel integration of environmental and self-motion information by place and grid cells

Abstract

Place cells and grid cells in the hippocampal formation are thought to integrate sensory and self-motion information into a representation of estimated spatial location, but the precise mechanism is unknown. We simulated a parallel attractor system in which place cells form an attractor network driven by environmental inputs and grid cells form an attractor network performing path integration driven by self-motion, with interconnections between them allowing both types of input to influence firing in both ensembles. We show that such a system is needed to explain the spatial patterns and temporal dynamics of place cell firing when rats run on a linear track in which the familiar correspondence between environmental and self-motion inputs is changed (Gothard et al., 1996b;Redish et al., 2000). In contrast, the alternative architecture of a single recurrent network of place cells (performing path integration and receiving environmental inputs) cannot reproduce the place cell firing dynamics. These results support the hypothesis that grid and place cells provide two different but complementary attractor representations (based on self-motion and environmental sensory inputs respectively). Our results also indicate the specific neural mechanism and main predictors of hippocampal map realignment and make predictions for future studies.

A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial hippocampal remapping and individual grid cell field-to-field variability

“…Despite the hypothesized role of recurrent connectivity in shaping spatial responses in the hippocampus and the MEC, theoretical research on the relationship between these brain areas has mostly treated them as successive stages in a processing hierarchy involving feed-forward connectivity from grid cells to place cells, or vice-versa, (Fig. 1a) [but see (Laptev and Burgess, 2019;Rennó-Costa and Tort, 2017)]. It is easy to show that summed inputs from multiple grid cells, combined with thresholding or competitive dynamics, can produce placecell like responses (de Almeida et al, 2009;Monaco and Abbott, 2011;Neher et al, 2017;Rolls et al, 2006;Solstad et al, 2006).…”