Impaired path integration in mice with disrupted grid cell firing

Gil, Mariana; Ancau, Mihai; Schlesiger, Magdalene I.; Neitz, Angela; Allen, Kevin; Marco, Rodrigo J. De; Monyer, Hannah

doi:10.1038/s41593-017-0039-3

Cited by 146 publications

(137 citation statements)

References 47 publications

(49 reference statements)

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“…We show degraded positional memory as a function of environmental geometry, in line with larger position decoding errors based on the eigenvector grid patterns of the SR as well as with impaired positional decoding from simulated grid cells with locally distorted firing patterns (Krupic et al, 2018). In concert with evidence for impaired path integration with disrupted grid cell firing in rodents (Gil et al, 2018) and increased path integration errors in older adults with weaker hexadirectional signals measured with fMRI (Stangl et al, 2018), previous studies support the interpretation that the integrity of the grid pattern is beneficial for human spatial memory. The strength of hexadirectional signals and the directional coherence of the orientation of these signals across voxels in the entorhinal cortex are associated with memory performance across participants learning object positions in circular enclosures (Doeller et al, 2010;Kunz et al, 2015).…”

Section: Discussionsupporting

confidence: 67%

Deforming the metric of cognitive maps distorts memory

Bellmund

Ruiter

Nau

et al. 2018

Preprint

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Environmental boundaries anchor cognitive maps that support memory. However, trapezoidal boundary geometry distorts the regular firing patterns of entorhinal grid cells proposedly providing a metric for cognitive maps. Here, we test the impact of trapezoidal boundary geometry on human spatial memory using immersive virtual reality. Consistent with reduced regularity of grid patterns in rodents and a grid-cell model based on the eigenvectors of the successor representation, human positional memory was degraded in a trapezoid compared to a square environment; an effect particularly pronounced in the trapezoid's narrow part. Congruent with spatial frequency changes of eigenvector grid patterns, distance estimates between remembered positions were persistently biased; revealing distorted memory maps that explained behavior better than the objective maps. Our findings demonstrate that environmental geometry affects human spatial memory similarly to rodent grid cell activity -thus strengthening the putative link between grid cells and behavior along with their cognitive functions beyond navigation.

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Section: Discussionsupporting

confidence: 67%

Deforming the metric of cognitive maps distorts memory

Bellmund

Ruiter

Nau

et al. 2018

Preprint

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“…Grid cells are generally assumed to be the primary determinant of place cell firing (5,8,13), although this notion has been challenged in both experimental and computational work (10,46,47 ).…”

Section: Pnn Removal In Mec Changes the Hippocampal Place Codementioning

confidence: 99%

“…Spatially tuned neurons in the hippocampus and entorhinal cortex are key units for navigation and spatial memory. Neurons in the medial entorhinal cortex (MEC) represent information such as self-location (1), the direction of the animal's head (2), proximity to geometric borders (3), speed (4), and possibly the distance traveled by the animal (5). The precise position of the animal can be decoded from the activity of grid cell ensembles, where each cell has multiple firing fields forming a characteristic hexagonal pattern spanning the entire surface of the area visited by the animal (6).…”

Section: Introductionmentioning

confidence: 99%

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Perineuronal nets stabilize the grid cell network

Christensen

Lensjø

Lepperød

et al. 2019

Preprint

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Grid 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.(9, 11). Once established, the periodic spiking pattern of grid cells is remarkably stable when animals revisit the same environment. Local perturbations of different cell types in MEC cause changes to grid field spike rates or an increased number of out-of-field spikes, but the location of the fields remains unaltered (12)(13)(14). Furthermore, when placed in a different environment, neighboring populations of grid cells show a coherent shift of grid fields (15) that retains their relative spatiotemporal relationships (16). In contrast the hippocampal place cells remap by independently and unpredictably changing their activity. This suggests that the mature grid cell network is more hardwired and less plastic than the hippocampal place cell network.The network that controls grid cell spiking is not yet fully understood, but recurrent inhibition appears to be fundamental to the specific activity of grid cells. Stellate cells, one of the two principal cell types that display grid cell firing (7 ), are connected via parvalbumin expressing (PV + ) inhibitory interneurons (17 , 18). PV + cells account for about 50% of the inhibitory cells in MEC (19), making them the main inhibitory mediator in the local grid cell network. In sensory cortex, PV + cells play a central role in shaping the excitatory activity of principal neurons by regulating the onset of periods of high synaptic plasticity (20). Whether PV + inhibitory neurons in MEC play a similar role for development of the grid cell network remains elusive.A hallmark of maturing PV + cells is that aggregates of specialized extracellular matrix, called perineuronal nets (PNNs), condense on the cell soma and proximal dendrites, leaving openings only for synaptic connections (21). PNNs are believed to help stabilize the activity of PV + cells by supporting synaptic integrity and limiting synaptogenesis, in addition to supporting PV + cell physiology (22). By the time PNNs in sensory cortex are fully mature, plasticity in the local network is strongly reduced. However, juvenile levels of plasticity can be r...

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“…Path integration. The MEC has been hypothesized to be the brain area responsible for idiothetic path integration for several reasons (Burak, 2014;Hafting et al, 2005;McNaughton et al, 2006) among them the highly geometric nature of grid cell spatial selectivity, the existence of inputs to the MEC that convey information about the animal's self-motion and heading (Kropff et al, 2015;Sargolini et al, 2006), and the impairment of path integration following disruption of grid cell activity (Gil et al, 2018). The similarity in response patterns of grid cells across environments implies that implementation of path integration in the MEC could be accomplished in different environments by the same synaptic connectivity, whereas implementation in the hippocampus (McNaughton et al, 1996) would require establishment of dedicated synaptic connectivity in each environment.…”

Section: Functional Consequences: Path Integration and Dynamic Couplingmentioning

confidence: 99%

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

Agmon

Burak

2020

Preprint

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The representation of position in the 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.We then show that 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.

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Impaired path integration in mice with disrupted grid cell firing

Cited by 146 publications

References 47 publications

Deforming the metric of cognitive maps distorts memory

Deforming the metric of cognitive maps distorts memory

Perineuronal nets stabilize the grid cell network

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

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