Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells

O’Keefe, John; Burgess, Neil

doi:10.1002/hipo.20115

Cited by 476 publications

(552 citation statements)

References 69 publications

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“…4B). These data support the prediction of a model (3,8) related to other models of grid cells and theta phase precession (18)(19)(20). In this model, grid cell periodicity arises from an interference pattern generated by intrinsic temporal oscillations in the soma and dendrites of a single cell.…”

supporting

confidence: 86%

Section: Nih-pa Author Manuscriptsupporting

confidence: 72%

“…S4 & S5). Spiking does not alter soma or dendritic phase, but occurs with theta rhythmicity, consistent with in vivo recordings in entorhinal cortex (5-7) and hippocampus (2,9,18), and potentially causing precession relative to field potential oscillations (3,8,19,20).The model (3,8) was modified to include shifts in dendritic frequency proportional to soma frequency and to utilize a scaling factor H (Fig. S6) determined from the experimental data.…”

mentioning

confidence: 58%

“…Neurons closer to the dorsal border of entorhinal cortex have shorter distances between firing fields. Computational models explicitly predict that differences in grid field spacing should correspond to differences in intrinsic frequencies of neurons along the dorsal to ventral axis (3,8). This could provide systematic variation in the gain of a movement-speed signal for path integration (2,3,9).…”

Section: Discussionmentioning

confidence: 99%

“…The model is compatible with maintenance of grid cell representations by persistent firing (23) or attractor dynamics arising from patterned excitatory connectivity (2,24,25). Long-term stability of grid fields could require place cell input dependent on external landmarks (3,8,26). Differences in intrinsic frequency along the dorsal to ventral axis of entorhinal cortex could contribute to differences in place field size along the septal to temporal axis of the hippocampus (9,27).…”

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confidence: 89%

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Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing

Giocomo

Zilli

Fransén

et al. 2007

Science

361

527

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SummaryIntracellular recording shows how differences in single cell subthreshold oscillation frequency could directly underlie the differences in spacing of grid cell firing locations shown previously in awake, behaving animals.Grid cells in layer II of entorhinal cortex fire to spatial locations in a repeating hexagonal grid with smaller spacing between grid fields for neurons in more dorsal anatomical locations. Data from in vitro whole-cell patch recordings show a corresponding difference in frequency of subthreshold membrane potential oscillations in entorhinal neurons at different positions along the dorsal to ventral axis, supporting a model of physiological mechanism for grid cell responses.The entorhinal cortex plays an important role in encoding of spatial information (1-3) and episodic memory (4). Many layer II neurons of rat entorhinal cortex are "grid cells," firing when the rat is in an array of spatial locations forming a hexagonal grid within the environment (5-7). The spacing of firing fields in the grid varies with anatomical position of the cell along the dorsal to ventral axis of entorhinal cortex, as measured by distance from the postrhinal border (5). Neurons closer to the dorsal border of entorhinal cortex have shorter distances between firing fields. Computational models explicitly predict that differences in grid field spacing should correspond to differences in intrinsic frequencies of neurons along the dorsal to ventral axis (3,8). This could provide systematic variation in the gain of a movement-speed signal for path integration (2,3,9).Subthreshold membrane potential oscillations in entorhinal cortical stellate cells (10) arise from a single-cell mechanism involving voltage-sensitive currents (11-13) and could contribute to network dynamics (14). We recorded subthreshold oscillations from 57 stellate cells in layer II of medial entorhinal cortex (Fig. S1) in slices from different anatomical positions along the dorsal to ventral axis, using whole-cell patch clamp techniques (15). The position of individual horizontal slices was measured relative to the dorsal surface of the brain (Fig. 1A).Stellate cells in dorsal entorhinal cortex show higher temporal frequencies of subthreshold membrane potential oscillations compared to lower frequencies in cells from more ventral entorhinal slices (Fig. 1B). Dorsal cells (n = 30) are defined as cells recorded in slices taken between 3.8 mm (the border with postrhinal cortex (16)) and 4.9 mm from the dorsal surface of the brain. Ventral cells (n = 27) are defined as cells recorded in slices between 4.9 and 7.1 mm from the dorsal surface. Fig. 1B shows the group means of the frequency of subthreshold oscillations recorded from these populations. Because frequency of subthreshold oscillations can depend upon the mean membrane potential voltage, we performed this analysis separately for data gathered at different approximate holding membrane potentials of −50 mV and −45 mV. The mean frequency in dorsal cells was significantly higher than the mean frequ...

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supporting

confidence: 86%

Section: Nih-pa Author Manuscriptsupporting

confidence: 72%

mentioning

confidence: 58%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 89%

See 3 more Smart Citations

Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing

Giocomo

Zilli

Fransén

et al. 2007

Science

361

527

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In Vitro and In Vivo Recording of Local Field Potential Oscillations in Mouse Hippocampus

et al. 2012

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Oscillations in hippocampal local field potentials (LFP) reflect the coordinated, rhythmic activity of constituent interneuronal and principal cell populations. Quantifying changes in oscillatory patterns and power therefore provides a powerful metric through which to infer mechanisms and functions of hippocampal network activity at the mesoscopic level, bridging single-neuron studies to behavioral assays of hippocampal function. Here, complementary protocols that enable mechanistic analyses of oscillation generation in vitro (in slices and a whole hippocampal preparation) and functional analyses of hippocampal circuits in behaving mice are described. Used together, these protocols provide a comprehensive view of hippocampal phenotypes in mouse models, highlighting oscillatory biomarkers of hippocampal function and dysfunction. Curr. Protoc. Mouse Biol. 2:273-294 © 2012 by John Wiley & Sons, Inc.

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Neuroscience of Navigation

Minear

Sensibaugh

2020

Position, Navigation, and Timing Technologies in the 21st Century

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Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells

Cited by 476 publications

References 69 publications

Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing

Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing

In Vitro and In Vivo Recording of Local Field Potential Oscillations in Mouse Hippocampus

Neuroscience of Navigation

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