scholarly journals Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

2021 ◽  
Author(s):  
Torgeir Waaga ◽  
Haggai Agmon ◽  
Velentin A. Normand ◽  
Anne Nagelhus ◽  
Richard J. Gardner ◽  
...  
Keyword(s):  
Neural Activity ◽  
Activity Patterns ◽  
Internal Representation ◽  
Grid Cell ◽  
Grid Cells ◽  
Sensory Cues ◽  
Population Activity ◽  
Medial Entorhinal Cortex ◽  
True Position ◽  
Cell Modules

The representation of an animal's position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different grid modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, to ensure that grid cells jointly encode a coherent and smooth trajectory of the animal.

scholarly journals An isomorphic mapping hypothesis of the grid representation

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120521 ◽  
Author(s):  
Michael Brecht ◽  
Saikat Ray ◽  
Andrea Burgalossi ◽  
Qiusong Tang ◽  
Helene Schmidt ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Dimensional Space ◽  
Grid Cell ◽  
Propagation Speed ◽  
Connectivity Matrix ◽  
Two Dimensional ◽  
Grid Cells ◽  
Population Activity ◽  
Medial Entorhinal Cortex ◽  
Mapping Hypothesis

We introduce a grid cell microcircuit hypothesis. We propose the ‘grid in the world’ (evident in grid cell discharges) is generated by a ‘grid in the cortex’. This cortical grid is formed by patches of calbindin-positive pyramidal neurons in layer 2 of medial entorhinal cortex (MEC). Our isomorphic mapping hypothesis assumes three types of isomorphism: (i) metric correspondence of neural space (the two-dimensional cortical sheet) and the external two-dimensional space within patches; (ii) isomorphism between cellular connectivity matrix and firing field; (iii) isomorphism between single cell and population activity. Each patch is a grid cell lattice arranged in a two-dimensional map of space with a neural : external scale of approximately 1 : 2000 in the dorsal part of rat MEC. The lattice behaves like an excitable medium with neighbouring grid cells exciting each other. Spatial scale is implemented as an intrinsic scaling factor for neural propagation speed. This factor varies along the dorsoventral cortical axis. A connectivity scheme of the grid system is described. Head direction input specifies the direction of activity propagation. We extend the theory to neurons between grid patches and predict a rare discharge pattern (inverted grid cells) and the relative location and proportion of grid cells and spatial band cells.

scholarly journals New neural activity patterns emerge with long-term learning

2019 ◽  
Vol 116 (30) ◽  
pp. 15210-15215 ◽  
Author(s):  
Emily R. Oby ◽  
Matthew D. Golub ◽  
Jay A. Hennig ◽  
Alan D. Degenhart ◽  
Elizabeth C. Tyler-Kabara ◽  
...  
Keyword(s):  
Neural Activity ◽  
Activity Patterns ◽  
Causal Link ◽  
Neural Population ◽  
Population Activity ◽  
The Brain ◽  
Neural Population Activity

Learning has been associated with changes in the brain at every level of organization. However, it remains difficult to establish a causal link between specific changes in the brain and new behavioral abilities. We establish that new neural activity patterns emerge with learning. We demonstrate that these new neural activity patterns cause the new behavior. Thus, the formation of new patterns of neural population activity can underlie the learning of new skills.

scholarly journals Home, head direction stability, and grid cell distortion

2020 ◽  
Vol 123 (4) ◽  
pp. 1392-1406 ◽  
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.

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

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Haggai Agmon ◽  
Yoram Burak
Keyword(s):  
Entorhinal Cortex ◽  
Activity Patterns ◽  
Grid Cell ◽  
Mechanistic Explanation ◽  
Place Cells ◽  
Mammalian Brain ◽  
Dimensional Manifold ◽  
Grid Cells ◽  
Attractor Dynamics ◽  
Low Dimensional

The representation of position in the mammalian brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here, we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. In addition, our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.

scholarly journals Home, head direction stability and grid cell distortion

2019 ◽  
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.

scholarly journals Effect of reward on electrophysiological signatures of grid cell population activity in human spatial navigation

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Wenjing Wang ◽  
Wenxu Wang
Keyword(s):  
Cell Population ◽  
Entorhinal Cortex ◽  
Grid Cell ◽  
Grid Cells ◽  
Grid Pattern ◽  
Population Activity ◽  
Spatial Measures ◽  
Moving Direction ◽  
Patients With Epilepsy ◽  
Reward Information

AbstractThe regular equilateral triangular periodic firing pattern of grid cells in the entorhinal cortex is considered a regular metric for the spatial world, and the grid-like representation correlates with hexadirectional modulation of theta (4–8 Hz) power in the entorhinal cortex relative to the moving direction. However, researchers have not clearly determined whether grid cells provide only simple spatial measures in human behavior-related navigation strategies or include other factors such as goal rewards to encode information in multiple patterns. By analysing the hexadirectional modulation of EEG signals in the theta band in the entorhinal cortex of patients with epilepsy performing spatial target navigation tasks, we found that this modulation presents a grid pattern that carries target-related reward information. This grid-like representation is influenced by explicit goals and is related to the local characteristics of the environment. This study provides evidence that human grid cell population activity is influenced by reward information at the level of neural oscillations.

scholarly journals Toroidal topology of population activity in grid cells

Nature ◽  
2022 ◽  
Author(s):  
Richard J. Gardner ◽  
Erik Hermansen ◽  
Marius Pachitariu ◽  
Yoram Burak ◽  
Nils A. Baas ◽  
...  
Keyword(s):  
Grid Cell ◽  
Population Level ◽  
Neural System ◽  
Topological Data Analysis ◽  
Small Samples ◽  
Grid Cells ◽  
Population Code ◽  
Grid Pattern ◽  
Population Activity ◽  
Toroidal Manifold

AbstractThe medial entorhinal cortex is part of a neural system for mapping the position of an individual within a physical environment1. Grid cells, a key component of this system, fire in a characteristic hexagonal pattern of locations2, and are organized in modules3 that collectively form a population code for the animal’s allocentric position1. The invariance of the correlation structure of this population code across environments4,5 and behavioural states6,7, independent of specific sensory inputs, has pointed to intrinsic, recurrently connected continuous attractor networks (CANs) as a possible substrate of the grid pattern1,8–11. However, whether grid cell networks show continuous attractor dynamics, and how they interface with inputs from the environment, has remained unclear owing to the small samples of cells obtained so far. Here, using simultaneous recordings from many hundreds of grid cells and subsequent topological data analysis, we show that the joint activity of grid cells from an individual module resides on a toroidal manifold, as expected in a two-dimensional CAN. Positions on the torus correspond to positions of the moving animal in the environment. Individual cells are preferentially active at singular positions on the torus. Their positions are maintained between environments and from wakefulness to sleep, as predicted by CAN models for grid cells but not by alternative feedforward models12. This demonstration of network dynamics on a toroidal manifold provides a population-level visualization of CAN dynamics in grid cells.

scholarly journals Connecting multiple spatial scales to decode the population activity of grid cells

2015 ◽  
Vol 1 (11) ◽  
pp. e1500816 ◽  
Author(s):  
Martin Stemmler ◽  
Alexander Mathis ◽  
Andreas V. M. Herz
Keyword(s):  
Large Scale ◽  
Spatial Scales ◽  
Cell Activity ◽  
Dead Reckoning ◽  
Grid Cell ◽  
Grid Cells ◽  
Population Vector ◽  
Population Activity ◽  
Multiple Spatial Scales ◽  
Scale Ratio

Mammalian grid cells fire when an animal crosses the points of an imaginary hexagonal grid tessellating the environment. We show how animals can navigate by reading out a simple population vector of grid cell activity across multiple spatial scales, even though neural activity is intrinsically stochastic. This theory of dead reckoning explains why grid cells are organized into discrete modules within which all cells have the same lattice scale and orientation. The lattice scale changes from module to module and should form a geometric progression with a scale ratio of around 3/2 to minimize the risk of making large-scale errors in spatial localization. Such errors should also occur if intermediate-scale modules are silenced, whereas knocking out the module at the smallest scale will only affect spatial precision. For goal-directed navigation, the allocentric grid cell representation can be readily transformed into the egocentric goal coordinates needed for planning movements. The goal location is set by nonlinear gain fields that act on goal vector cells. This theory predicts neural and behavioral correlates of grid cell readout that transcend the known link between grid cells of the medial entorhinal cortex and place cells of the hippocampus.

Oscillator-Interference Models of Path Integration Do Not Require Theta Oscillations

2015 ◽  
Vol 27 (3) ◽  
pp. 548-560 ◽  
Author(s):  
Jeff Orchard
Keyword(s):  
Path Integration ◽  
Activity Patterns ◽  
Field Potential ◽  
Grid Cell ◽  
Place Cells ◽  
Theta Oscillations ◽  
Grid Cells ◽  
Neural Oscillators ◽  
Theta Frequency ◽  
Interference Models

Navigation and path integration in rodents seems to involve place cells, grid cells, and theta oscillations (4–12 Hz) in the local field potential. Two main theories have been proposed to explain the neurological underpinnings of how these phenomena relate to navigation and to each other. Attractor network (AN) models revolve around the idea that local excitation and long-range inhibition connectivity can spontaneously generate grid-cell-like activity patterns. Oscillator interference (OI) models propose that spatial patterns of activity are caused by the interference patterns between neural oscillators. In rats, these oscillators have a frequency close to the theta frequency. Recent studies have shown that bats do not exhibit a theta cycle when they crawl, and yet they still have grid cells. This has been interpreted as a criticism of OI models. However, OI models do not require theta oscillations. We explain why the absence of theta oscillations does not contradict OI models and discuss how the two families of models might be distinguished experimentally.

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