Models of place and grid cell firing and theta rhythmicity
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.
References (67)
Hippocampal electrical activity and voluntary movement in the rat
Electroencephalogr Clin Neurophysiol
(1969)Place units in the hippocampus of the freely moving rat
Exp Neurol
(1976)- et al.
Hippocampus-independent phase precession in entorhinal grid cells
Nature
(2008) - et al.
A model of the neural basis of the rat's sense of direction
Adv Neural Inf Process Syst
(1995) - Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL: Phase precession and variable spatial scaling in a...
- et al.
Phase relationship between hippocampal place units and the EEG theta rhythm
Hippocampus
(1993) - et al.
Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding
J Neurophysiol
(2000) - et al.
Independent rate and temporal coding in hippocampal pyramidal cells
Nature
(2003) - et al.
Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing
Hippocampus
(2003) - et al.
Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus
Hippocampus
(2005)
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
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