Models of place and grid cell firing and theta rhythmicity

doi:10.1016/j.conb.2011.07.002

Current Opinion in Neurobiology

Volume 21, Issue 5, October 2011, Pages 734-744

https://doi.org/10.1016/j.conb.2011.07.002 Get rights and content

Neuronal firing in the hippocampal formation (HF) of freely moving rodents shows striking examples of spatialorganization in the form of place, directional, boundary vector and grid cells. The firing of place and grid cells shows an intriguing form of temporal organization known as ‘theta phase precession’. We review the mechanisms underlying theta phase precession of place cell firing, ranging from membrane potential oscillations to recurrent connectivity, and the relevant intra-cellular and extra-cellular data. We then consider the use of these models to explain the spatial structure of grid cell firing, and review the relevant intra-cellular and extra-cellular data. Finally, we consider the likely interaction between place cells, grid cells and boundary vector cells in estimating self-location as a compromise between path-integration and environmental information.

Graphical abstract

Highlights

► Intracellular insights into theta phase precession and spiking in place cells. ► Verification of quantitative predictions from models of place and grid cell firing. ► Functional organization of spatial cell types in the hippocampal formation. ► Inter-relation of environmental information, path integration and theta rhythmicity.

Section snippets

Models of theta-phase precession of place cell firing

Computational work on theta-phase precession has fallen into two broad camps, those focusing on mechanisms within an individual place cell and those focusing on mechanisms arising from the interaction between large networks of neurons. Models from these two viewpoints are reviewed below, and need not be mutually exclusive. Time will tell which types of mechanism prove most productive in explaining the experimental findings and whether both types of mechanism are necessary for a comprehensive

Oscillatory mechanisms

Grid cells show a regularly repeating spatial firing pattern more reminiscent of an interference pattern than the uni-modal firing pattern of most place cells (Figure 3a), suggesting that the Dual Oscillator model might be extended to the grid cells in layer II of mEC [23, 27]. These cells were subsequently shown to exhibit theta-phase precession, see [12^•] and Figure 3b.

In the Dual Oscillator model the frequency of the dendritic oscillation increases with running speed so that its phase

Interactions between the different types of spatial cell

The long-term stability of the firing patterns of place and grid cells relative to the environment indicates that firing locations are determined by environmental information as well as the mechanisms for path integration discussed above. Recording from the same place [14] or grid [54^•] cell during geometric manipulation of a familiar environment indicates a special influence of environmental boundaries on firing locations, see also [64]. Computational modeling of place fields [15, 16•]

Conclusions

A range of models relate theta-phase precession in hippocampal place cell firing to membrane potential oscillations and recurrent connectivity. Some of these models also provide the basis of models of path integration and grid cell firing. However, environmental inputs are also a crucial part of self location, for which boundary-vector cells may play a key role. This field has seen a recent explosion of both experimental results and computational models. Critically, computational modeling has

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

This work was supported by the Medical Research Council and the Wellcome Trust, UK, and the SpaceBrain grant of the European Union.

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Place cells and grid cells are major building blocks of the hippocampal cognitive map. The prominent forward model postulates that grid-cell modules are generated by a continuous attractor network; that a velocity signal evoked during locomotion moves entorhinal activity bumps; and that place-cell activity constitutes summation of entorhinal grid-cell modules. Experimental data support the first postulate, but not the latter two. Several families of solutions that depart from these postulates have been put forward. We suggest a modified model (spatial modulation continuous attractor network; SCAN), whereby place cells are generated from spatially selective nongrid cells. Locomotion causes these cells to move the hippocampal activity bump, leading to movement of the entorhinal manifolds. Such inversion accords with the shift of hippocampal thought from navigation to more abstract functions.
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Theta rhythm recorded as an extracellular synchronous field potential is generated in a number of brain sites including the hippocampus. The physiological occurrence of hippocampal theta rhythm is associated with the activation of a number of structures forming the ascending brainstem-hippocampal synchronizing pathway. Experimental evidence indicates that the supramammillary nucleus and posterior hypothalamic nuclei, considered as the posterior hypothalamic area, comprise a critical node of this ascending pathway. The posterior hypothalamic area plays an important role in movement control, place-learning, memory processing, emotion and arousal. In the light of multiplicity of functions of the posterior hypothalamic area and the influence of theta field oscillations on a number of neural processes, it is the authors’ intent to summarize the data concerning the involvement of the supramammillary nucleus and posterior hypothalamic nuclei in the modulation of limbic theta rhythmicity as well as the ability of these brain structures to independently generate theta rhythmicity.

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View full text

Models of place and grid cell firing and theta rhythmicity

Graphical abstract

Highlights

Section snippets

Models of theta-phase precession of place cell firing

Oscillatory mechanisms

Interactions between the different types of spatial cell

Conclusions

References and recommended reading

Acknowledgements

Electroencephalogr Clin Neurophysiol

Exp Neurol

Nature

Adv Neural Inf Process Syst

Phase relationship between hippocampal place units and the EEG theta rhythm

Hippocampus

Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding

J Neurophysiol

Independent rate and temporal coding in hippocampal pyramidal cells

Nature

Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing

Hippocampus

Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus

Hippocampus

Hippocampal place cell assemblies are speed-controlled oscillators

Proc Natl Acad Sci USA

Head direction cells and the neuropsychological basis for a sense of direction

Prog Neurobiol

Conjunctive representation of position, direction, and velocity in entorhinal cortex

Science

Microstructure of a spatial map in the entorhinal cortex

Nature

Representation of geometric borders in the entorhinal cortex

Science

Geometric determinants of the place fields of hippocampal neurons

Nature

Predictions derived from modelling the hippocampal role in navigation

Biol Cybern

Modeling place fields in terms of the cortical inputs to the hippocampus

Hippocampus

Boundary vector cells in the subiculum of the hippocampal formation

J Neurosci

The spatial periodicity of grid cells is not sustained during reduced theta oscillations

Science

Intracellular dynamics of hippocampal place cells during virtual navigation

Nature

Impact of spikelets on hippocampal CA1 pyramidal cell activity during spatial exploration

Science

Deciphering the hippocampal polyglot: the hippocampus as a path integration system

J Exp Biol

Beyond the Cognitive Map: From Place Cells to Episodic Memory

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

Hippocampus

An oscillatory interference model of grid cell firing

Hippocampus

Grid cells and theta as oscillatory interference: theory and predictions

Hippocampus

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

Hippocampus

A grid and place cell model of path integration utilizing phase precession versus theta

Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials

Hippocampus

Using hippocampal ‘place cells’ for navigation, exploiting phase coding

Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus

Proc Natl Acad Sci USA

Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons

Nat Neurosci