Hippocampus-independent phase precession in entorhinal grid cells

Hafting, Torkel; Fyhn, Marianne; Bonnevie, Tora; Moser, May‐Britt; Moser, Edvard I

doi:10.1038/nature06957

Cited by 432 publications

(617 citation statements)

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“…1C and 2A). The strong rhythmicity of neural firing in this model is consistent with experimental data on theta rhythmicity of neural spiking in entorhinal cortex (Stewart et al, 1992;Hafting et al, 2008).…”

Section: Persistent Spiking Model Of Grid Cellssupporting

confidence: 75%

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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ABSTRACT:This article presents a model of grid cell firing based on the intrinsic persistent firing shown experimentally in neurons of entorhinal cortex. In this model, the mechanism of persistent firing allows individual neurons to hold a stable baseline firing frequency. Depolarizing input from speed-modulated head direction cells transiently shifts the frequency of firing from baseline, resulting in a shift in spiking phase in proportion to the integral of velocity. The convergence of input from different persistent firing neurons causes spiking in a grid cell only when the persistent firing neurons are within similar phase ranges. This model effectively simulates the two-dimensional firing of grid cells in open field environments, as well as the properties of theta phase precession. This model provides an alternate implementation of oscillatory interference models. The persistent firing could also interact on a circuit level with rhythmic inhibition and neurons showing membrane potential oscillations to code position with spiking phase. These mechanisms could operate in parallel with computation of position from visual angle and distance of stimuli. In addition to simulating two-dimensional grid patterns, models of phase interference can account for context-dependent firing in other tasks. In network simulations of entorhinal cortex, hippocampus, and postsubiculum, the reset of phase effectively replicates context-dependent firing by entorhinal and hippocampal neurons during performance of a continuous spatial alternation task, a delayed spatial alternation task with running in a wheel during the delay period (Pastalkova et al., Science, 2008), and a hairpin maze task.

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Section: Persistent Spiking Model Of Grid Cellssupporting

confidence: 75%

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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“…Increased preferred theta-phase variability could arise through a rate-phase transformation 19 and a reduced excitatory drive in VR due to a lack of repeatedly paired sensory and motor cues, as described below. The underlying network mechanism could thus generate motif-like activity under a variety of conditions, including hippocampal place cells from normal subjects 21,31,33 and transgenic mice with taupathy 40 , entorhinal cortical grid cells 38 , episode or time cells during wheel or treadmill running 22,23 , neural activity during rapid eye movement sleep 41 and neural activity during free recall in humans 42 .…”

Section: Discussionmentioning

confidence: 99%

“…6b). For all cells, we also computed the difference between the period of theta modulation of spikes and the local field potential (LFP) theta period 18,20,38 . A majority of cells in RW (83%) and VR (78%) had a longer LFP theta period than their spike theta period, which is indicative of intact temporal coding in VR (Fig.…”

mentioning

confidence: 99%

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

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During real-world (RW) exploration, rodent hippocampal activity shows robust spatial selectivity, which is hypothesized to be governed largely by distal visual cues, although other sensory-motor cues also contribute. Indeed, hippocampal spatial selectivity is weak in primate and human studies that use only visual cues. To determine the contribution of distal visual cues only, we measured hippocampal activity from body-fixed rodents exploring a two-dimensional virtual reality (VR). Compared to that in RW, spatial selectivity was markedly reduced during random foraging and goal-directed tasks in VR. Instead we found small but significant selectivity to distance traveled. Despite impaired spatial selectivity in VR, most spikes occurred within ~2-s-long hippocampal motifs in both RW and VR that had similar structure, including phase precession within motif fields. Selectivity to space and distance traveled were greatly enhanced in VR tasks with stereotypical trajectories. Thus, distal visual cues alone are insufficient to generate a robust hippocampal rate code for space but are sufficient for a temporal code. npg © 2015 Nature America, Inc. All rights reserved.1 2 2 VOLUME 18 | NUMBER 1 | JANUARY 2015 nature neurOSCIenCe a r t I C l e S same physical location in space can be approached from multiple different directions at different speeds. We thus investigated the contribution of distal visual cues only in determining selectivity in such an experimental setup. RESULTS Nature of spatial selectivity of hippocampal responsesWe measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a). In VR, the rats were body-fixed, i.e., their bodies were held in place, with a harness on a floating ball, allowing for head movements but precluding full-body turns, thus minimizing vestibular cues (Online Methods) 21,36 . Rats quickly learned to avoid the virtual edges entirely on the basis of visual cues 36 and spent a similar amount of time away from the edges and in the center of the platform (Fig. 1a) compared to in RW. We measured the activity of 1,066 and 1,238 principal neurons in RW and VR, respectively, in the dorsal CA1 of four rats under a variety of conditions (Online Methods). Neurons fired vigorously in restricted regions of space in RW, as expected (Fig. 1b,c, Supplementary Fig. 1a and Supplementary Video 1) 1 . In contrast, the neurons showed little spatial selectivity in VR during random foraging (Fig. 1b,d and Supplementary Fig. 1b).Across the ensemble, neurons had moderately reduced (25%) mean firing rates but greatly reduced (68%) peak firing rates in VR ( Fig. 2a and Supplementary Fig. 2a). Neurons in VR also had greatly reduced spatial information content (75%), stability (59%), sparsity (42%) and coherence (40%) (Fig. 2b-d and Supplementary Fig. 2b,c) compared to spatially localized, stable and sparse RW rate maps (Fig. 2c). Although the mean firing rate was inversely correlated with information content (Supplementary Fig. 2d)...

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“…Theta rhythmicity is associated with phase-locking and phase precession of neuronal spiking, and thereby imposes complex timing relationships typically not evident in vitro. For example, theta phase precession is more prevalent in MEC LII than LIII [63]. It is not yet known what impact this has on LIII-CA1 and LII/LIII-CA2 interactions and the potential recruitment of hippocampal cell assemblies by EC input [73].…”

Section: Selecting Circuits Within Circuits: Who Does What When?mentioning

confidence: 99%

“…Regardless, the recently reported physiology and anatomy [41] suggest that CA2 may be the only hippocampal subregion in which the theta phase precessing grid and border cells of LII and the theta phase locked border, HD, conjunctive and grid cells LIII [63] converge and interact. Thus, in terms of MEC input, CA2 seems well-placed to integrate all available types of spatial, directional, movement and border information.…”

Section: Ca2 Comes In From the Coldmentioning

confidence: 99%

Updating hippocampal representations: CA2 joins the circuit

Jones

McHugh

2011

Trends in Neurosciences

114

106

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The hippocampus integrates the encoding, storage and recall of memories, binding the spatiotemporal and sensory information that constitutes experience and keeping episodes in their correct context. The rapid and accurate processing of such daunting volumes of continuouslychanging data relies on dynamically assigning different aspects of mnemonic processing to specialized, interconnected networks corresponding to the anatomical subfields of dentate gyrus (DG), CA3 and CA1. However, differentially processed information ultimately has to be reintegrated into conjunctive representations, and this is unlikely to be achieved by unidirectional, sequential steps through a DG-CA3-CA1 loop. In this Review, we highlight recently discovered anatomical and physiological features that are likely to necessitate updates to the hippocampal circuit diagram, particularly by incorporating the oft-neglected CA2 region.3

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Hippocampus-independent phase precession in entorhinal grid cells

Cited by 432 publications

References 30 publications

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Updating hippocampal representations: CA2 joins the circuit

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