Home, head direction stability and grid cell distortion

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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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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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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During hippocampal inactivation, grid cells maintain synchrony, even when the grid pattern is lost

eLife ◽

10.7554/elife.47147 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 1

Author(s):

Noam Almog ◽

Gilad Tocker ◽

Tora Bonnevie ◽

Edvard I Moser ◽

May-Britt Moser ◽

...

Keyword(s):

Grid Cell ◽

Head Direction ◽

Grid Cells ◽

Regular Grid ◽

Spatial Correlations ◽

Grid Pattern ◽

Medial Entorhinal Cortex ◽

Cell Network ◽

Intrinsic Connectivity ◽

Temporal And Spatial

The grid cell network in the medial entorhinal cortex (MEC) has been subject to thorough testing and analysis, and many theories for their formation have been suggested. To test some of these theories, we re-analyzed data from Bonnevie et al., 2013, in which the hippocampus was inactivated and grid cells were recorded in the rat MEC. We investigated whether the firing associations of grid cells depend on hippocampal inputs. Specifically, we examined temporal and spatial correlations in the firing times of simultaneously recorded grid cells before and during hippocampal inactivation. Our analysis revealed evidence of network coherence in grid cells even in the absence of hippocampal input to the MEC, both in regular grid cells and in those that became head-direction cells after hippocampal inactivation. This favors models, which suggest that phase relations between grid cells in the MEC are dependent on intrinsic connectivity within the MEC.

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Representation of Geometric Borders in the Entorhinal Cortex

Science ◽

10.1126/science.1166466 ◽

2008 ◽

Vol 322 (5909) ◽

pp. 1865-1868 ◽

Cited By ~ 583

Author(s):

Trygve Solstad ◽

Charlotte N. Boccara ◽

Emilio Kropff ◽

May-Britt Moser ◽

Edvard I. Moser

Keyword(s):

Reference Frame ◽

Cell Population ◽

Entorhinal Cortex ◽

Border Cells ◽

Head Direction ◽

Grid Cells ◽

Cell Type ◽

Medial Entorhinal Cortex ◽

Size And Shape ◽

Local Cell

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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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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Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex

eLife ◽

10.7554/elife.16937 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 60

Author(s):

José Antonio Pérez-Escobar ◽

Olga Kornienko ◽

Patrick Latuske ◽

Laura Kohler ◽

Kevin Allen

Keyword(s):

Firing Rate ◽

Entorhinal Cortex ◽

Visual Information ◽

Grid Cell ◽

Grid Cells ◽

Contextual Cues ◽

Context Specificity ◽

Visual Landmarks ◽

Medial Entorhinal Cortex ◽

Geometrical Properties

Neurons of the medial entorhinal cortex (MEC) provide spatial representations critical for navigation. In this network, the periodic firing fields of grid cells act as a metric element for position. The location of the grid firing fields depends on interactions between self-motion information, geometrical properties of the environment and nonmetric contextual cues. Here, we test whether visual information, including nonmetric contextual cues, also regulates the firing rate of MEC neurons. Removal of visual landmarks caused a profound impairment in grid cell periodicity. Moreover, the speed code of MEC neurons changed in darkness and the activity of border cells became less confined to environmental boundaries. Half of the MEC neurons changed their firing rate in darkness. Manipulations of nonmetric visual cues that left the boundaries of a 1D environment in place caused rate changes in grid cells. These findings reveal context specificity in the rate code of MEC neurons.

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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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Shedding light on stellate cells

eLife ◽

10.7554/elife.41041 ◽

2018 ◽

Vol 7 ◽

Author(s):

Andrew S Alexander ◽

Michael E Hasselmo

Keyword(s):

Entorhinal Cortex ◽

Stellate Cells ◽

Grid Cells ◽

Medial Entorhinal Cortex ◽

The Relationship

The relationship between grid cells and two types of neurons found in the medial entorhinal cortex has been clarified.

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Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0523 ◽

2014 ◽

Vol 369 (1635) ◽

pp. 20120523 ◽

Cited By ~ 28

Author(s):

Michael E. Hasselmo

Keyword(s):

Resonance Frequency ◽

Entorhinal Cortex ◽

Functional Role ◽

Grid Cell ◽

Medial Septum ◽

Medial Entorhinal Cortex ◽

Spatial Periodicity ◽

Cell Firing ◽

Rebound Spiking ◽

Relationship Of

Data show a relationship of cellular resonance and network oscillations in the entorhinal cortex to the spatial periodicity of grid cells. This paper presents a model that simulates the resonance and rebound spiking properties of entorhinal neurons to generate spatial periodicity dependent upon phasic input from medial septum. The model shows that a difference in spatial periodicity can result from a difference in neuronal resonance frequency that replicates data from several experiments. The model also demonstrates a functional role for the phenomenon of theta cycle skipping in the medial entorhinal cortex.

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