Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after‐spike dynamics

Navratilova, Zaneta; Giocomo, Lisa M.; Fellous, Jean-Marc; Hasselmo, Michael E.; McNaughton, Bruce L.

doi:10.1002/hipo.20939

Cited by 149 publications

(220 citation statements)

References 71 publications

(128 reference statements)

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“…formation, including one based on attractors (30) and those based on oscillatory interference (6,(31)(32)(33). It seems possible that these temporal changes might be triggered by the release of a neuromodulator, such as ACh, which is implicated in novelty detection (34,35) and affects both the frequency of theta-band oscillations (36) and the resonant properties of mEC stellate cells (37).…”

Section: Discussionmentioning

confidence: 99%

Grid cell firing patterns signal environmental novelty by expansion

Barry

Ginzberg²,

O’Keefe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

192

255

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The hippocampal formation plays key roles in representing an animal's location and in detecting environmental novelty to create or update those representations. However, the mechanisms behind this latter function are unclear. Here, we show that environmental novelty causes the spatial firing patterns of grid cells to expand in scale and reduce in regularity, reverting to their familiar scale as the environment becomes familiar. Simultaneously recorded place cell firing fields remapped and showed a smaller, temporary expansion. Grid expansion provides a potential mechanism for novelty signaling and may enhance the formation of new hippocampal representations, whereas the subsequent slow reduction in scale provides a potential familiarity signal.single unit | spatial memory | hippocampus G rid cells in the medial entorhinal cortex (mEC) of freely moving rodents exhibit a striking triangular grid-like firing pattern (1). Although the grid patterns are anchored to familiar environmental cues (1, 2), their maintenance in darkness and across different environments (1, 3) suggests that they provide a constant metric for self-motion (1, 3-7). Place cells in hippocampal regions CA1 and CA3 tend to fire in single firing fields (8), coding for self-location within an environment. Place cells create novel representations for new environments ("remapping") (3, 9, 10) providing a neural substrate for memory; they show attractor dynamics (11-13) and long-term plasticity (14), and they become increasingly stable and focal with prolonged experience of an environment (15,16). In contrast, grid cells are thought to retain their regular spatial structure, scale, and position relative to other grids in novel environments (1, 3), changing only their orientation and spatial offset relative to the environment and showing a brief reduction in spatial stability (1). Grid cells (1,7,17), in conjunction with other environmental inputs (6,(18)(19)(20)(21), are thought to provide an important input to hippocampal place cells. Conversely, direct and indirect projections from CA1 to the deep layers of the mEC (22, 23) have been proposed as a possibly route by which extrinsic sensory information might reach grids (21), a view supported by developmental and inactivation studies (24-26). Together, these points raise questions about the relationship between entorhinal and hippocampal activity; for example: Does stable grid cell firing co-occur with labile place fields, and what drives place cell remapping?In experiment 1, we investigated grid cell firing on first exposure to a new environment and as it became increasingly familiar during trials conducted on the same day and then on subsequent days. In experiment 2, we replicated the experiment using different environments, while corecording grid cells and place cells from a second cohort of rats that had received bilateral mEC and hippocampal implants. Together, these experiments showed that grid cell firing patterns were spatially expanded and less regular in novel arenas than in a similarly size...

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Section: Discussionmentioning

confidence: 99%

Grid cell firing patterns signal environmental novelty by expansion

Barry

Ginzberg²,

O’Keefe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

192

255

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“…OI models have successfully explained some properties of temporal organization in grid cells, such as theta phase precession 105,207 , an aspect that has not been addressed in attractor models, except in one dimension 208 . However, OI models have faced serious challenges as an explanation of the spatial periodicity of the grid cells.…”

Section: Box 4: Oscillatory Interference Models Of Grid Cellsmentioning

confidence: 99%

Grid cells and cortical representation

et al. 2014

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One of the grand challenges in neuroscience is to comprehend neural computation in the association cortices, the parts of the cortex that have shown the largest expansion and differentiation during mammalian evolution and that are thought to contribute so profoundly to the emergence of advanced cognition in humans. In this review, we will use grid cells in the medial entorhinal cortex as a gateway to understanding network computation at a stage of cortical processing where firing patterns are shaped not primarily by incoming sensory signals but to a large extent by intrinsic properties of the local circuit.

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“…In response to oscillating current injection that increases in frequency, the neuron shows a gradual increase in amplitude of membrane potential deflection that reaches a peak at resonance frequency, and then decreases. constants of synaptic potentials [55,56]. As an alternative to slow synaptic interactions, one attractor model overcame the problem of simulating long interspike intervals by using an alternative solution involving rebound spiking dependent on prior spikes [56].…”

Section: Extracellular Data On Theta Cycle Skipping and Loss Of Thetamentioning

confidence: 99%

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

Hasselmo

2014

Phil. Trans. R. Soc. B

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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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Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after‐spike dynamics

Cited by 149 publications

References 71 publications

Grid cell firing patterns signal environmental novelty by expansion

Grid cell firing patterns signal environmental novelty by expansion

Grid cells and cortical representation

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

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