A Map-like Micro-Organization of Grid Cells in the Medial Entorhinal Cortex

Abstract

Summary: How the topography of neural circuits relates to their function remains unclear. Although topographic maps exist for sensory and motor variables, they are rarely observed for cognitive variables. Using calcium imaging during virtual navigation, we investigated the relationship between the anatomical organization and functional properties of grid cells, which represent a cognitive code for location during navigation. We found a substantial degree of grid cell micro-organization in mouse medial entorhinal cortex: grid cells and modules all clustered anatomically. Within a module, the layout of grid cells was a noisy two-dimensional lattice, in which the anatomical distribution of grid cells largely matched their spatial tuning phases. This micro-arrangement of phases demonstrates the existence of a topographical map encoding a cognitive variable in rodents. It contributes to a foundation for evaluating circuit models of the grid cell network, and is consistent with continuous attractor models as the mechanism of grid formation.

A neuronal signature for monogamous reunion

“…Both clustered and distributed cellular organization has been observed for networks involved in higher order cognitive processing. For instance, grid cells display functional micro-organization and clustering within the medial entorhinal cortex (Gu et al, 2018;Heys et al, 2014). However, in mouse brain areas projecting to the NAc, including the medial prefrontal cortex, amygdala, and hypothalamus (Walum and Young, 2018), ensembles encoding social information seem to lack meaningful spatial organization (Kingsbury et al, 2019;Li et al, 2017;Remedios et al, 2017).…”

Inter- and intra-animal variation of integrative properties of stellate cells in the medial entorhinal cortex

“…In the crab stomatogastric ganglion, inter-animal variation correlates with circuit performance (Goaillard et al, 2009) . Accordingly, variation in intrinsic properties of SCs might correlate with differences in grid firing (Domnisoru et al, 2013;Gu et al, 2018;Rowland et al, 2018;Schmidt-Hieber and Häusser, 2013) or behaviours that rely on SCs (Kitamura et al, 2014;Qin et al, 2018;Tennant et al, 2018) . It is interesting in this respect that there appear to be inter-animal differences in the spatial scale of grid modules (cf.…”

“…The spatial scale of grid fields follows a dorsoventral organisation (Hafting et al, 2005) , which is mirrored by a dorsoventral organisation in key electrophysiological features of SCs (Boehlen et al, 2010;Dodson et al, 2011;Garden et al, 2008;Giocomo and Hasselmo, 2008a;Giocomo et al, 2007;Pastoll et al, 2012a) . Grid cells are organised into discrete modules (Stensola et al, 2012) , cells in a module have a similar grid scale and orientation (Barry et al, 2007;Gu et al, 2018;Stensola et al, 2012) and progressively more ventral modules are composed of cells with wider grid spacing (Stensola et al, 2012) . Studies that demonstrate dorsoventral organisation of integrative properties of SCs have so far relied on pooling of relatively few measurements per animal.…”

Flexible representation of higher-dimensional cognitive variables with grid cells

“…Even the physical layout of grid cells in the brain mirrors, and likely drives, the rigid 2D nature of the functional response of grid modules. Grid cells are spatially organized in a 2D grid-like topographical pattern based on their spatial tuning in 2D environments (Heys et al, 2014;Gu et al, 2018). Thus, the intrinsically 2D nature of the grid cell representations across diverse tasks and variables is not only functional, but physical.…”