Hippocampal Cognitive Map Local Transformations
Science 09 Mar 2018: Vol. 359, Issue 6380, pp. 1143-1146 Local transformations of the hippocampal cognitive map Julija Krupic, et.al. Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, CB2 3EG, UK. Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK. Sainsbury Wellcome Centre, University College London, London W1T 4JG, UK. [paraphrase] Grid cells are neurons active in multiple fields arranged in a hexagonal lattice and are thought to represent the “universal metric for space.” However, they become nonhomogeneously distorted in polarized enclosures, which challenges this view. We found that local changes to the configuration of the enclosure induce individual grid fields to shift in a manner inversely related to their distance from the reconfigured boundary. The grid remained primarily anchored to the unchanged stable walls and showed a nonuniform rescaling. Shifts in simultaneously recorded colocalized grid fields were strongly correlated, which suggests that the readout of the animal’s position might still be intact. Similar field shifts were also observed in place and boundary cells—albeit of greater magnitude and more pronounced closer to the reconfigured boundary—which suggests that there is no simple one-to-one relationship between these three different cell types. Place, head-direction, boundary, and grid cells constitute the major units of the hippocampal cognitive map that forms the basis of our ability to navigate and form episodic memories. Based on the grid cell periodic firing pattern and presumed invariance, the predominant hypothesis of grid cell function states that they represent the spatial metric system of the brain. According to the major computational models, place and border cells act predominantly to stabilize the grid without determining its hexagonality. However, it has been recently shown that boundaries can profoundly reshape grid cell symmetry, but the nature of this influence, as well as its relation to other spatial cells, remains unknown. To study the effect of boundaries on grid cell structure, we recorded from 347 spatially periodic cells in the medial entorhinal cortex (seven rats). The firing pattern of the majority (63%) exhibited hexagonal symmetry in at least one of our four enclosures (grid cells), whereas that of other cells was more elliptical and irregular or had too few fields and did not pass the hexagonality criterion. Recordings were made while rats foraged for food in four familiar polygonal enclosures (presented in random order) that varied in shape from a left trapezoid (poly 129°) to a rectangle (poly 180°), with two intermediate shapes being irregular pentagons created by increasing the angle of the west-slanting wall of the trapezoid from 129° to either 145° or 160°. We found that individual grid fields shift by different amounts in response to local changes in enclosure geometry and that the magnitude of the shift is inversely correlated with the distance from the movable wall. Importantly, the grid remains primarily anchored to the stable wall of the enclosure, consistent with previous studies on other spatial cells and behavior, showing that the extent of cue control depends on its perceived stability. These results suggest that the local geometry of the enclosure plays a key role in constructing the grid as indicated by previous behavioral observations that rats relied on local geometry to find a reward location. We have also shown that colocalized grid fields remained in register across all grid cells, including ones from different grid modules, suggesting that in principle these distortions could be corrected by the readout system to estimate the metric. Perhaps more likely, the transformed grids could lead to a misperception of self-location in the room frame of reference. Finally, we found that grid cells could undergo nonuniform transformations that might be implemented either by the Field-Boundary Interaction model or by the Boundary Vector Cell model. Place cells show similar tendencies, albeit overall they shift by larger amounts. Previously it has been shown that place cells can be formed even in the absence of grid cells. Here, we demonstrate that they can undergo a different degree of transformation in response to the same geometric manipulation, suggesting that some place cells may be interacting with grid cells while others interact with border cells, as previously suggested, or alternatively their spatial properties may be formed by different underlying mechanisms. [end of paraphrase]
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