An oscillatory interference model of grid cell firing

Burgess, Neil; Barry, Caswell; O’Keefe, John

doi:10.1002/hipo.20327

Cited by 630 publications

(1,038 citation statements)

References 64 publications

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“…A recent model for the grid field properties of the entorhinal cortex layer II stellate cells [22,23,38] relies precisely on the ingredients considered in the present study. The model assumes that different dendritic branches emanating from the soma of these cells function as distinct oscillators.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, multiple intrinsic dendritic oscillators have been proposed to underlie the recently discovered intricate firing pattern of entorhinal grid cells [22,23,24]. Motivated by the likely existence of multiple dendritic oscillators in a single cell, we study the dynamics of such interacting oscillators and their impact on signal propagation in single neurons, using mathematical analysis corroborated by numerical simulations of biophysical models.…”

Section: Introductionmentioning

confidence: 99%

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The role of ongoing dendritic oscillations in single-neuron dynamics

2009

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The dendritic tree contributes significantly to the elementary computations a neuron performs while converting its synaptic inputs into action potential output. Traditionally, these computations have been characterized as temporally local, near-instantaneous mappings from the current input of the cell to its current output, brought about by somatic summation of dendritic contributions that are generated in spatially localized functional compartments. However, recent evidence about the presence of oscillations in dendrites suggests a qualitatively different mode of operation: the instantaneous phase of such oscillations can depend on a long history of inputs, and under appropriate conditions, even dendritic oscillators that are remote may interact through synchronization. Here, we develop a mathematical framework to analyze the interactions of local dendritic oscillations, and the way these interactions influence single cell computations. Combining weakly coupled oscillator methods with cable theoretic arguments, we derive phase-locking states for multiple oscillating dendritic compartments. We characterize how the phase-locking properties depend on key parameters of the oscillating dendrite: the electrotonic properties of the (active) dendritic segment, and the intrinsic properties of the dendritic oscillators. As a direct consequence, we show how input to the dendrites can modulate phase-locking behavior and hence global dendritic coherence. In turn, dendritic coherence is able to gate the integration and propagation of synaptic signals to the soma, ultimately leading to an effective control of somatic spike generation. Our results suggest that dendritic oscillations enable the dendritic tree to operate on more global temporal and spatial scales than previously thought. 1 Author SummaryA central issue in biology is how do local sub-cellular processes result in global cellular consequences. For neurons this is especially relevant since these spatially extended cells convert local synaptic inputs into action potential output. The dendritic tree of a neuron, which is where most inputs arrive, expresses membrane conductances that can generate intrinsic nonlinearities. The distributions of these membrane conductances are typically highly nonuniform. The non-uniform distribution of membrane conductances can turn the dendritic tree into a network of sparsely spaced active "hot spots". A prominent phenomenon resulting from the dendritic nonlinearities are intrinsic membrane potential oscillations, which are typically recorded at the neuron's soma. Here we analyze whether the active local oscillatory "hot spots" can produce global membrane voltage oscillations. Our mathematical theory shows that indeed, even when local dendritic oscillators are coupled extremely weakly, they still lead to global oscillations. This global effect arises since the oscillators lock to each other. We then show how the biophysical parameters of the dendrites affect this global locking. It becomes clear that when the oscillators are sy...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The role of ongoing dendritic oscillations in single-neuron dynamics

2009

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“…The oscillatory interference model of grid cells arose naturally out of models simulating the theta phase precession of hippocampal place cells (O'Keefe and Recce, 1993;Lengyel et al, 2003;O'Keefe and Burgess, 2005;Burgess et al, 2005Burgess et al, , 2007, and effectively models theta phase precession in entorhinal cortical neurons Burgess, 2008;Hasselmo and Brandon, 2008). In fact, these place cell precession models automatically generated multiple firing fields, and had to be modified to prevent multiple fields.…”

Section: Theta Phase Precessionmentioning

confidence: 99%

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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“…Various models have been proposed, most suggesting that place fields can emerge from summation of input from grid cells with different orientations and spatial scales [37][38][39].…”

Section: Some Quirks Of Entorhinal-hippocampal Connectivitymentioning

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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An oscillatory interference model of grid cell firing

Cited by 630 publications

References 64 publications

The role of ongoing dendritic oscillations in single-neuron dynamics

The role of ongoing dendritic oscillations in single-neuron dynamics

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

Updating hippocampal representations: CA2 joins the circuit

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