scholarly journals Perineuronal nets stabilize the grid cell network

2019 ◽  
Author(s):  
Ane Charlotte Christensen ◽  
Kristian Kinden Lensjø ◽  
Mikkel Elle Lepperød ◽  
Svenn-Arne Dragly ◽  
Halvard Sutterud ◽  
...  

AbstractGrid cells are part of a widespread network that supports navigation and spatial memory. Stable grid patterns appear late in development, in concert with extracellular matrix aggregates termed perineuronal nets (PNNs) that condense around inhibitory neurons. To reveal the relationship between stable spatial representations and the presence of PNNs we recorded from populations of neurons in adult rats. We show that removal of PNNs leads to lower inhibitory spiking activity, and reduces grid cells’ ability to create stable representations of a novel environment. Furthermore, in animals with disrupted PNNs, exposure to a novel arena corrupted the spatiotemporal relationships within grid cell modules, and the stored representations of a familiar arena. Finally, we show that PNN removal in entorhinal cortex distorted spatial representations in downstream hippocampal neurons. Together this work suggests that PNNs provide a key stabilizing element for the grid cell network.


2018 ◽  
Vol 115 (7) ◽  
pp. E1637-E1646 ◽  
Author(s):  
Tale L. Bjerknes ◽  
Nenitha C. Dagslott ◽  
Edvard I. Moser ◽  
May-Britt Moser

Place cells in the hippocampus and grid cells in the medial entorhinal cortex rely on self-motion information and path integration for spatially confined firing. Place cells can be observed in young rats as soon as they leave their nest at around 2.5 wk of postnatal life. In contrast, the regularly spaced firing of grid cells develops only after weaning, during the fourth week. In the present study, we sought to determine whether place cells are able to integrate self-motion information before maturation of the grid-cell system. Place cells were recorded on a 200-cm linear track while preweaning, postweaning, and adult rats ran on successive trials from a start wall to a box at the end of a linear track. The position of the start wall was altered in the middle of the trial sequence. When recordings were made in complete darkness, place cells maintained fields at a fixed distance from the start wall regardless of the age of the animal. When lights were on, place fields were determined primarily by external landmarks, except at the very beginning of the track. This shift was observed in both young and adult animals. The results suggest that preweaning rats are able to calculate distances based on information from self-motion before the grid-cell system has matured to its full extent.



2017 ◽  
Author(s):  
Benjamin Dunn ◽  
Daniel Wennberg ◽  
Ziwei Huang ◽  
Yasser Roudi

AbstractResearch on network mechanisms and coding properties of grid cells assume that the firing rate of a grid cell in each of its fields is the same. Furthermore, proposed network models predict spatial regularities in the firing of inhibitory interneurons that are inconsistent with experimental data. In this paper, by analyzing the response of grid cells recorded from rats during free navigation, we first show that there are strong variations in the mean firing rate of the fields of individual grid cells and thus show that the data is inconsistent with the theoretical models that predict similar peak magnitudes. We then build a two population excitatory-inhibitory network model in which sparse spatially selective input to the excitatory cells, presumed to arise from e.g. salient external stimuli, hippocampus or a combination of both, leads to the variability in the firing field amplitudes of grid cells. We show that, when combined with appropriate connectivity between the excitatory and inhibitory neurons, the variability in the firing field amplitudes of grid cells results in inhibitory neurons that do not exhibit regular spatial firing, consistent with experimental data. Finally, we show that even if the spatial positions of the fields are maintained, variations in the firing rates of the fields of grid cells are enough to cause remapping of hippocampal cells.



2017 ◽  
Author(s):  
Sean G. Trettel ◽  
John B. Trimper ◽  
Ernie Hwaun ◽  
Ila R. Fiete ◽  
Laura Lee Colgin

ABSTRACTContinuous attractor network models of grid formation posit that recurrent connectivity between grid cells controls their patterns of co-activation. Grid cells from a common module exhibit stable offsets in their periodic spatial tuning curves across environments, which may reflect recurrent connectivity or correlated sensory inputs. Here we explore whether cell-cell relationships predicted by attractor models persist during sleep states in which spatially informative sensory inputs are absent. We recorded ensembles of grid cells in superficial layers of medial entorhinal cortex during active exploratory behaviors and overnight sleep. Per pair and collectively, we found preserved patterns of spike-time correlations across waking, REM, and non-REM sleep, which reflected the spatial tuning offsets between these cells during active exploration. The preservation of cell-cell relationships across states was not explained by theta oscillations or CA1 activity. These results suggest that recurrent connectivity within the grid cell network drives grid cell activity across behavioral states.



2021 ◽  
Author(s):  
Torgeir Waaga ◽  
Haggai Agmon ◽  
Velentin A. Normand ◽  
Anne Nagelhus ◽  
Richard J. Gardner ◽  
...  

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.



2019 ◽  
Author(s):  
Noam Almog ◽  
Gilad Tocker ◽  
Tora Bonnevie ◽  
Edvard Moser ◽  
May-Britt Moser ◽  
...  

AbstractThe grid cell network in the 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 MEC, to investigate 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.



2018 ◽  
Author(s):  
Dong Chen ◽  
Kai-Jia Sun ◽  
Liang Wang ◽  
Zhanjun Zhang ◽  
Ying-Cheng Lai ◽  
...  

Grid cells constitute a crucial component of the “GPS” in the mammalian brain. Recent experiments revealed that grid cell activity is anchored to environmental boundaries. More specifically, these results revealed a slight yet consistent offset of 8 degrees relative to boundaries of a square environment. The causes and possible functional roles of this orientation are still unclear. Here we propose that this phenomenon maximizes the spatial information conveyed by grid cells. Computer simulations of the grid cell network reveal that the universal grid orientation at 8 degrees optimizes spatial coding specifically in the presence of noise. Our model also predicts the minimum number of grid cells in each module. In addition, analytical results and a dynamical reinforcement learning model reveal the mechanism underlying the noise-induced orientation preference at 8 degrees. Together, these results suggest that the experimentally observed common orientation of grid cells serves to maximize spatial information in the presence of noise.



2018 ◽  
Author(s):  
Sophie Rosay ◽  
Simon N. Weber ◽  
Marcello Mulas

A neuron’s firing correlates are defined as the features of the external world to which its activity is correlated. In many parts of the brain, neurons have quite simple such firing correlates. A striking example are grid cells in the rodent medial entorhinal cortex: their activity correlates with the animal’s position in space, defining ‘grid fields’ arranged with a remarkable periodicity. Here, we show that the organization and evolution of grid fields relate very simply to physical space. To do so, we use an effective model and consider grid fields as point objects (particles) moving around in space under the influence of forces. We are able to reproduce most observations on the geometry of grid patterns. This particle-like behavior is particularly salient in a recent experiment where two separate grid patterns merge. We discuss pattern formation in the light of known results from physics of two-dimensional colloidal systems. Finally, we draw the relationship between our ‘macroscopic’ model for grid fields and existing ‘microscopic’ models of grid cell activity and discuss how a description at the level of grid fields allows to put constraints on the underlying grid cell network.



2021 ◽  
Author(s):  
Johnson Ying ◽  
Alexandra T. Keinath ◽  
Raphael Lavoie ◽  
Erika Vigneault ◽  
Salah El Mestikawy ◽  
...  

AbstractEarly-onset familial Alzheimer’s disease (AD) is marked by an aggressive buildup of amyloid beta (Aβ) proteins, yet the neural circuit operations impacted during the initial stages of Aβ pathogenesis remain elusive. Here, we report a coding impairment of the medial entorhinal cortex (MEC) grid cell network in a transgenic mouse model of familial AD that over-expresses Aβ throughout the hippocampus and entorhinal cortex. Grid cells showed reduced spatial periodicity, spatial stability, and synchrony with interneurons and head-direction cells. In contrast, the spatial coding of non-grid cells within the MEC, and place cells within the hippocampus, remained intact. Grid cell deficits emerged at the earliest incidence of Aβ fibril deposition and coincided with impaired spatial memory performance in a path integration task. These results demonstrate that widespread Aβ-mediated damage to the entorhinal-hippocampal circuit results in an early impairment of the entorhinal grid cell network.



eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Noam Almog ◽  
Gilad Tocker ◽  
Tora Bonnevie ◽  
Edvard I Moser ◽  
May-Britt Moser ◽  
...  

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.



2017 ◽  
Author(s):  
Richard J. Gardner ◽  
Li Lu ◽  
Tanja Wernle ◽  
May-Britt Moser ◽  
Edvard I. Moser

AbstractThe network of grid cells in the medial entorhinal cortex forms a fixed reference frame for mapping physical space. The mechanistic origin of the grid representation is unknown, but continuous attractor network (CAN) models explain multiple fundamental features of grid-cell activity. An untested prediction of CAN grid models is that the grid-cell network should exhibit an activity correlation structure that transcends behavioural or brain states. By recording from MEC cell ensembles during navigation and sleep, we found that spatial phase offsets of grid cells predict arousal-state-independent spike rate correlations. Similarly, state-invariant correlations between conjunctive grid-head-direction and pure head-direction cells were predicted by their head-direction tuning offsets. Spike rates of grid cells were only weakly correlated across modules, and module scale relationships disintegrated during slow-save sleep, suggesting that modules function as independent attractor networks. Collectively, our observations suggest that network states in MEC are expressed universally across brain and behaviour states.



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