Representation of Geometric Borders in the Entorhinal Cortex

We report the existence of an entorhinal cell type that fires when an animal is close to the borders of the proximal environment. The orientation-specific edge-apposing activity of these “border cells” is maintained when the environment is stretched and during testing in enclosures of different size and shape in different rooms. Border cells are relatively sparse, making up less than 10% of the local cell population, but can be found in all layers of the medial entorhinal cortex as well as the adjacent parasubiculum, often intermingled with head-direction cells and grid cells. Border cells may be instrumental in planning trajectories and anchoring grid fields and place fields to a geometric reference frame.

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Functional connectivity of the entorhinal–hippocampal space circuit

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0516 ◽

2014 ◽

Vol 369 (1635) ◽

pp. 20120516 ◽

Cited By ~ 23

Author(s):

Sheng-Jia Zhang ◽

Jing Ye ◽

Jonathan J. Couey ◽

Menno Witter ◽

Edvard I. Moser ◽

...

Keyword(s):

Entorhinal Cortex ◽

Cell Types ◽

Place Cells ◽

Projection Neurons ◽

Border Cells ◽

Head Direction ◽

Grid Cells ◽

Head Direction Cells ◽

Dynamic Interactions ◽

Cell Groups

The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. We have developed an optogenetic strategy to identify functionally defined cell types in the MEC that project directly to the hippocampus. By expressing channelrhodopsin-2 (ChR2) selectively in the hippocampus-projecting subset of entorhinal projection neurons, we were able to use light-evoked discharge as an instrument to determine whether specific entorhinal cell groups—such as grid cells, border cells and head-direction cells—have direct hippocampal projections. Photoinduced firing was observed at fixed minimal latencies in all functional cell categories, with grid cells as the most abundant hippocampus-projecting spatial cell type. We discuss how photoexcitation experiments can be used to distinguish the subset of hippocampus-projecting entorhinal neurons from neurons that are activated indirectly through the network. The functional breadth of entorhinal input implied by this analysis opens up the potential for rich dynamic interactions between place cells in the hippocampus and different functional cell types in the entorhinal cortex (EC).

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Local microcircuitry of parasubiculum shows distinct and common features of excitatory and inhibitory connectivity

10.1101/2020.12.18.423400 ◽

2020 ◽

Author(s):

Rosanna P Sammons ◽

Alexandra Tzilivaki ◽

Dietmar Schmitz

Keyword(s):

Random Network ◽

Spatial Navigation ◽

Border Cells ◽

Head Direction ◽

Grid Cells ◽

Medial Entorhinal Cortex ◽

Common Features ◽

Layer 2 ◽

Firing Properties ◽

Local Circuitry

The parasubiculum is located within the parahippocampal region, where it is thought to be involved in the processing of spatial navigational information. It contains a number of functionally specialised neuron types including grid cells, head direction cells and border cells, and provides input into layer 2 of the medial entorhinal cortex where grid cells are abundantly located. The local circuitry within the parasubiculum remains so far undefined but may provide clues as to the emergence of spatially tuned firing properties of neurons in this region. We used simultaneous patch-clamp recordings to determine the connectivity rates between the three major groups of neurons found in the parasubiculum. We find high rates of interconnectivity between the pyramidal class and interneurons, as well as features of pyramid to pyramid interactions indicative of a non-random network. The microcircuit that we uncover shares both similarities and divergences to those from other parahippocampal regions also involved in spatial navigation.

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Home, head direction stability, and grid cell distortion

Journal of Neurophysiology ◽

10.1152/jn.00518.2019 ◽

2020 ◽

Vol 123 (4) ◽

pp. 1392-1406 ◽

Cited By ~ 2

Author(s):

Juan Ignacio Sanguinetti-Scheck ◽

Michael Brecht

Keyword(s):

Entorhinal Cortex ◽

Home Cage ◽

Cell Activity ◽

Grid Cell ◽

Head Direction ◽

Grid Cells ◽

Head Direction Cells ◽

Medial Entorhinal Cortex ◽

Abstract Approach ◽

Globally Stable

The home is a unique location in the life of humans and animals. In rats, home presents itself as a multicompartmental space that involves integrating navigation through subspaces. Here we embedded the laboratory rat’s home cage in the arena, while recording neurons in the animal’s parasubiculum and medial entorhinal cortex, two brain areas encoding the animal’s location and head direction. We found that head direction signals were unaffected by home cage presence or translocation. Head direction cells remain globally stable and have similar properties inside and outside the embedded home. We did not observe egocentric bearing encoding of the home cage. However, grid cells were distorted in the presence of the home cage. While they did not globally remap, single firing fields were translocated toward the home. These effects appeared to be geometrical in nature rather than a home-specific distortion and were not dependent on explicit behavioral use of the home cage during a hoarding task. Our work suggests that medial entorhinal cortex and parasubiculum do not remap after embedding the home, but local changes in grid cell activity overrepresent the embedded space location and might contribute to navigation in complex environments. NEW & NOTEWORTHY Neural findings in the field of spatial navigation come mostly from an abstract approach that separates the animal from even a minimally biological context. In this article we embed the home cage of the rat in the environment to address some of the complexities of natural navigation. We find no explicit home cage representation. While both head direction cells and grid cells remain globally stable, we find that embedded spaces locally distort grid cells.

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Home, head direction stability and grid cell distortion

10.1101/602771 ◽

2019 ◽

Cited By ~ 2

Author(s):

Juan Ignacio Sanguinetti-Scheck ◽

Michael Brecht

Keyword(s):

Entorhinal Cortex ◽

Home Cage ◽

Grid Cell ◽

Neural Representation ◽

Head Direction ◽

Grid Cells ◽

Medial Entorhinal Cortex ◽

Home Location ◽

Single Firing ◽

Behavioral Studies

AbstractThe home is a unique location in the life of humans and animals. Numerous behavioral studies investigating homing indicate that many animals maintain an online representation of the direction of the home, a home vector. Here we placed the rat’s home cage in the arena, while recording neurons in the animal’s parasubiculum and medial entorhinal cortex. From a pellet hoarding paradigm it became evident that the home cage induced locomotion patterns characteristic of homing behaviors. We did not observe home-vector cells. We found that head-direction signals were unaffected by home location. However, grid cells were distorted in the presence of the home cage. While they did not globally remap, single firing fields were translocated towards the home. These effects appeared to be geometrical in nature rather than a home-specific distortion. Our work suggests that medial entorhinal cortex and parasubiculum do not contain an explicit neural representation of the home direction.

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Functional network topography of the medial entorhinal cortex

10.1101/2021.09.20.461016 ◽

2021 ◽

Author(s):

Horst A. Obenhaus ◽

Weijian Zong ◽

R. Irene Jacobsen ◽

Tobias Rose ◽

Flavio Donato ◽

...

Keyword(s):

Entorhinal Cortex ◽

Grid Cell ◽

Cell Types ◽

List Type ◽

Head Direction ◽

Grid Cells ◽

Activity Data ◽

Medial Entorhinal Cortex ◽

Depth Analysis ◽

Low Levels

SummaryThe medial entorhinal cortex (MEC) creates a map of local space, based on the firing patterns of grid, head direction (HD), border, and object-vector (OV) cells. How these cell types are organized anatomically is debated. In-depth analysis of this question requires collection of precise anatomical and activity data across large populations of neurons during unrestrained behavior, which neither electrophysiological nor previous imaging methods fully afford. Here we examined the topographic arrangement of spatially modulated neurons in MEC and adjacent parasubiculum using miniaturized, portable two-photon microscopes, which allow mice to roam freely in open fields. Grid cells exhibited low levels of co-occurrence with OV cells and clustered anatomically, while border, HD and OV cells tended to intermingle. These data suggest that grid-cell networks might be largely distinct from those of border, HD and OV cells and that grid cells exhibit strong coupling among themselves but weaker links to other cell types.Highlights- Grid and object vector cells show low levels of regional co-occurrence- Grid cells exhibit the strongest tendency to cluster among all spatial cell types- Grid cells stay separate from border, head direction and object vector cells- The territories of grid, head direction and border cells remain stable over weeks

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Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity

Science ◽

10.1126/science.1232627 ◽

2013 ◽

Vol 340 (6128) ◽

pp. 1232627 ◽

Cited By ~ 145

Author(s):

Sheng-Jia Zhang ◽

Jing Ye ◽

Chenglin Miao ◽

Albert Tsao ◽

Ignas Cerniauskas ◽

...

Keyword(s):

Functional Connectivity ◽

Entorhinal Cortex ◽

Cell Types ◽

Place Cell ◽

Projection Neurons ◽

Functional Identity ◽

Border Cells ◽

Head Direction ◽

Medial Entorhinal Cortex ◽

Adeno Associated Virus

We used a combined optogenetic-electrophysiological strategy to determine the functional identity of entorhinal cells with output to the place-cell population in the hippocampus. Channelrhodopsin-2 (ChR2) was expressed selectively in the hippocampus-targeting subset of entorhinal projection neurons by infusing retrogradely transportable ChR2-coding recombinant adeno-associated virus in the hippocampus. Virally transduced ChR2-expressing cells were identified in medial entorhinal cortex as cells that fired at fixed minimal latencies in response to local flashes of light. A large number of responsive cells were grid cells, but short-latency firing was also induced in border cells and head-direction cells, as well as cells with irregular or nonspatial firing correlates, which suggests that place fields may be generated by convergence of signals from a broad spectrum of entorhinal functional cell types.

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Head-direction cells escaping attractor dynamics in the parahippocampal region

10.1101/268110 ◽

2018 ◽

Author(s):

Olga Kornienko ◽

Patrick Latuske ◽

Laura Kohler ◽

Kevin Allen

Keyword(s):

Entorhinal Cortex ◽

Computational Models ◽

Head Direction ◽

Grid Cells ◽

Visual Landmarks ◽

Head Direction Cells ◽

Medial Entorhinal Cortex ◽

Attractor Dynamics ◽

Freely Moving ◽

Uniform Population

AbstractNavigation depends on the activity of head-direction (HD) cells. Computational models postulate that HD cells form a uniform population that reacts coherently to changes in landmarks. We tested whether this applied to HD cells of the medial entorhinal cortex and parasubiculum, areas where the HD signal contributes to the periodic firing of grid cells. Manipulations of the visual landmarks surrounding freely-moving mice altered the tuning of HD cells. Importantly, these tuning modifications were often non-coherent across cells, refuting the notion that HD cells form a uniform population constrained by attractor-like dynamics. Instead, examination of theta rhythmicity 1revealed two types of HD cells, theta rhythmic and non-rhythmic cells. Larger tuning alterations were observed predominantly in non-rhythmic HD cells. Moreover, only non-rhythmic HD cells reorganized their firing associations in response to visual land-mark changes. These findings reveal a theta non-rhythmic HD signal whose malleable organization is controlled by visual landmarks.

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A geometric attractor mechanism for self-organization of entorhinal grid modules

eLife ◽

10.7554/elife.46687 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 7

Author(s):

Louis Kang ◽

Vijay Balasubramanian

Keyword(s):

Entorhinal Cortex ◽

Network Models ◽

Recurrent Inhibition ◽

Modular Structure ◽

Self Organization ◽

Periodic Lattice ◽

Grid Cells ◽

Medial Entorhinal Cortex ◽

Attractor Network ◽

Discrete Values

Grid cells in the medial entorhinal cortex (MEC) respond when an animal occupies a periodic lattice of ‘grid fields’ in the environment. The grids are organized in modules with spatial periods, or scales, clustered around discrete values separated on average by ratios in the range 1.4–1.7. We propose a mechanism that produces this modular structure through dynamical self-organization in the MEC. In attractor network models of grid formation, the grid scale of a single module is set by the distance of recurrent inhibition between neurons. We show that the MEC forms a hierarchy of discrete modules if a smooth increase in inhibition distance along its dorso-ventral axis is accompanied by excitatory interactions along this axis. Moreover, constant scale ratios between successive modules arise through geometric relationships between triangular grids and have values that fall within the observed range. We discuss how interactions required by our model might be tested experimentally.

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