scholarly journals Distinct hippocampal network states support theta phase precession and theta sequences in CA1

2021 ◽  
Author(s):  
Matteo Guardamagna ◽  
Federico Stella ◽  
Francesco P. Battaglia
Keyword(s):  
Spatial Information ◽  
Place Cells ◽  
Temporal Coding ◽  
Temporal Code ◽  
Network State ◽  
Phase Precession ◽  
Hippocampal Network ◽  
Theta Phase ◽  
Network States ◽  
Theta Phase Precession

The hippocampus likely uses temporal coding to represent complex memories via mechanisms such as theta phase precession and theta sequences. Theta sequences are rapid sweeps of spikes from multiple place cells, encoding past or planned trajectories or non-spatial information. Phase precession, the correlation between a place cell's theta firing phase and animal position has been suggested to facilitate sequence emergence. We find that CA1 phase precession varies strongly across cells and environmental contingencies. Phase precession depends on the CA1 network state, and is only present when the medium gamma oscillation (60-90 Hz, linked to Entorhinal inputs) dominates. Conversely, theta sequences are most evident for non-precessing cells or with leading slow gamma (20-45 Hz, linked to CA3 inputs). These results challenge the view that phase precession is the mechanism underlying the emergence of theta sequences and point at a 'dual network states' model for hippocampal temporal code, potentially supporting merging of memory and exogenous information in CA1.

scholarly journals Asymmetry of the temporal code for space by hippocampal place cells

2016 ◽  
Author(s):  
Bryan C. Souza ◽  
Adriano B. L. Tort
Keyword(s):  
Firing Rate ◽  
Spatial Information ◽  
Place Cells ◽  
Spike Timing ◽  
Temporal Coding ◽  
Place Field ◽  
Phase Precession ◽  
Wide Debate ◽  
Rate Coding ◽  
Theta Phase

Hippocampal place cells convey spatial information through spike frequency (“rate coding”) and spike timing relative to the theta phase (“temporal coding”). Whether rate and temporal coding are due to independent or related mechanisms has been the subject of wide debate. Here we show that the spike timing of place cells couples to theta phase before major increases in firing rate, anticipating the animal’s entrance into the classical, rate-based place field. In contrast, spikes rapidly decouple from theta as the animal leaves the place field and firing rate decreases. Therefore, temporal coding has strong asymmetry around the place field center. We further show that the dynamics of temporal coding along space evolves in three stages: phase coupling, phase precession and phase decoupling. These results suggest that place cells represent more future than past locations through their spike timing and that independent mechanisms govern rate and temporal coding.

Cognitive Map Formation Through Sequence Encoding by Theta Phase Precession

2004 ◽  
Vol 16 (12) ◽  
pp. 2665-2697 ◽  
Author(s):  
Hiroaki Wagatsuma ◽  
Yoko Yamaguchi
Keyword(s):  
Field Potential ◽  
Computer Experiments ◽  
Cognitive Map ◽  
Phase Precession ◽  
Spatial Environment ◽  
Hippocampal Network ◽  
Theta Phase ◽  
Space Coding ◽  
Temporal Sequences ◽  
Theta Phase Precession

The rodent hippocampus has been thought to represent the spatial environment as a cognitive map. The associative connections in the hippocampus imply that a neural entity represents the map as a geometrical network of hippocampal cells in terms of a chart. According to recent experimental observations, the cells fire successively relative to the theta oscillation of the local field potential, called theta phase precession, when the animal is running. This observation suggests the learning of temporal sequences with asymmetric connections in the hippocampus, but it also gives rather inconsistent implications on the formation of the chart that should consist of symmetric connections for space coding. In this study, we hypothesize that the chart is generated with theta phase coding through the integration of asymmetric connections. Our computer experiments use a hippocampal network model to demonstrate that a geometrical network is formed through running experiences in a few minutes. Asymmetric connections are found to remain and distribute heterogeneously in the network. The obtained network exhibits the spatial localization of activities at each instance as the chart does and their propagation that represents behavioral motions with multidirectional properties. We conclude that theta phase precession and the Hebbian rule with a time delay can provide the neural principles for learning the cognitive map.

Memory Encoding by Theta Phase Precession in the Hippocampal Network

2003 ◽  
Vol 15 (10) ◽  
pp. 2379-2397 ◽  
Author(s):  
Naoyuki Sato ◽  
Yoko Yamaguchi
Keyword(s):  
Spike Timing ◽  
Temporal Sequence ◽  
Memory Storage ◽  
Trial Experience ◽  
Phase Precession ◽  
Rate Coding ◽  
Hippocampal Network ◽  
Theta Phase ◽  
Theta Phase Precession

Recent experimental evidence on spike-timing-dependent plasticity and on phase precession (i.e., the theta rhythm dependent firing of rat hippocampalcells) associates the contribution of phase precession to episodic memory. This article aims at clarifying the role of phase precession in memory storage. Computer simulations show that the memory storage in the behavioral timescale varies in timescale of the temporal sequence from half a second to several seconds. In contrast, the memory storage caused by traditional rate coding is restricted to the temporal sequence within 40 ms. During phase precession, memory storage of a single trial experience is possible, even in the presence of noise. It is therefore concluded that encoding by phase precession is appropriate for memory storage of the temporal sequence in the behavioral timescale.

scholarly journals Bimodality of Theta Phase Precession in Hippocampal Place Cells in Freely Running Rats

2002 ◽  
Vol 87 (6) ◽  
pp. 2629-2642 ◽  
Author(s):  
Yoko Yamaguchi ◽  
Yoshito Aota ◽  
Bruce L. McNaughton ◽  
Peter Lipa
Keyword(s):  
Place Cells ◽  
Distribution Functions ◽  
Data Sets ◽  
Place Field ◽  
Spike Density ◽  
Phase Versus ◽  
Normal Probability ◽  
Phase Precession ◽  
Theta Phase ◽  
Theta Phase Precession

The firing of hippocampal principal cells in freely running rats exhibits a progressive phase retardation as the animal passes through a cell's “place” field. This “phase precession” is more complex than a simple linear shift of phase with position. In the present paper, phase precession is quantitatively analyzed by fitting multiple (1–3) normal probability density functions to the phase versus position distribution of spikes in rats making repeated traversals of the place fields. The parameters were estimated by the Expectation Maximization method. Three data sets including CA1 and DG place cells were analyzed. Although the phase-position distributions vary among different cells and regions, this complexity is well described by a superposition of two normal distribution functions, suggesting that the firing behavior consists of two components. This conclusion is supported by the existence of two distinct maxima in the mean spike density in the phase versus position plane. In one component, firing phase shifts over a range of about 180°. The second component, which occurs near the end of the traversal of the place field, exhibits a low correlation between phase and position and is anti-phase with the phase-shift component. The functional implications of the two components are discussed with respect to their possible contribution to learning and memory mechanisms.

scholarly journals Phase precession in the human hippocampus and entorhinal cortex

2020 ◽  
Author(s):  
Salman E. Qasim ◽  
Itzhak Fried ◽  
Joshua Jacobs
Keyword(s):  
Entorhinal Cortex ◽  
Spatial Information ◽  
Neural Representation ◽  
Local Network ◽  
Neuron Activity ◽  
Human Hippocampus ◽  
Phase Precession ◽  
Show Evidence ◽  
Theta Phase ◽  
Theta Phase Precession

AbstractKnowing where we are, where we have been, and where we are going is critical to many behaviors, including navigation and memory. One potential neuronal mechanism underlying this ability is phase precession, in which spatially tuned neurons represent sequences of positions by activating at progressively earlier phases of local network theta (~5–10 Hz) oscillations. Phase precession may be a general neural pattern for representing sequential events for learning and memory. However, phase precession has never been observed in humans. By recording human single-neuron activity during spatial navigation, we show that spatially tuned neurons in the human hippocampus and entorhinal cortex exhibit phase precession. Furthermore, beyond the neural representation of locations, we show evidence for phase precession related to specific goal-states. Our findings thus extend theta phase precession to humans and suggest that this phenomenon has a broad functional role for the neural representation of both spatial and non-spatial information.

Enhancement of Hippocampal Spatial Decoding Using a Dynamic Q-Learning Method With a Relative Reward Using Theta Phase Precession

2020 ◽  
Vol 30 (09) ◽  
pp. 2050048
Author(s):  
Bo-Wei Chen ◽  
Shih-Hung Yang ◽  
Yu-Chun Lo ◽  
Ching-Fu Wang ◽  
Han-Lin Wang ◽  
...  
Keyword(s):  
Convergence Rate ◽  
Prediction Accuracy ◽  
Learning Algorithm ◽  
Place Cells ◽  
Goal Location ◽  
Q Learning ◽  
Reward Function ◽  
Phase Precession ◽  
Theta Phase ◽  
Theta Phase Precession

Hippocampal place cells and interneurons in mammals have stable place fields and theta phase precession profiles that encode spatial environmental information. Hippocampal CA1 neurons can represent the animal’s location and prospective information about the goal location. Reinforcement learning (RL) algorithms such as Q-learning have been used to build the navigation models. However, the traditional Q-learning ([Formula: see text]Q-learning) limits the reward function once the animals arrive at the goal location, leading to unsatisfactory location accuracy and convergence rates. Therefore, we proposed a revised version of the Q-learning algorithm, dynamical Q-learning ([Formula: see text]Q-learning), which assigns the reward function adaptively to improve the decoding performance. Firing rate was the input of the neural network of [Formula: see text]Q-learning and was used to predict the movement direction. On the other hand, phase precession was the input of the reward function to update the weights of [Formula: see text]Q-learning. Trajectory predictions using [Formula: see text]Q- and [Formula: see text]Q-learning were compared by the root mean squared error (RMSE) between the actual and predicted rat trajectories. Using [Formula: see text]Q-learning, significantly higher prediction accuracy and faster convergence rate were obtained compared with [Formula: see text]Q-learning in all cell types. Moreover, combining place cells and interneurons with theta phase precession improved the convergence rate and prediction accuracy. The proposed [Formula: see text]Q-learning algorithm is a quick and more accurate method to perform trajectory reconstruction and prediction.

scholarly journals Dynamic control of hippocampal spatial coding resolution by local visual cues

2018 ◽  
Author(s):  
Romain Bourboulou ◽  
Geoffrey Marti ◽  
FranÇois-Xavier Michon ◽  
Morgane Nouguier ◽  
David Robbe ◽  
...  
Keyword(s):  
Virtual Reality ◽  
Visual Cues ◽  
Dynamic Control ◽  
Place Cells ◽  
Spatial Coding ◽  
3D Objects ◽  
Mapping System ◽  
Phase Precession ◽  
Theta Phase ◽  
Theta Phase Precession

AbstractThe ability to flexibly navigate an environment relies on a hippocampal-dependent internal cognitive map. Explored space can be internally mapped at different spatial resolutions. However, whether hippocampal spatial coding resolution can be dynamically controlled within and between environments is unknown. In this work we recorded the firing of hippocampal principal cells in mice navigating virtual reality environments, which differed by the presence of local visual cues (virtual 3D objects). Objects improved spatial coding resolution globally with a higher proportion of place cells, smaller place fields, increased spatial selectivity and stability. Spatial coding resolution was notably enhanced locally near objects and could be rapidly tuned by their manipulations. In the presence of objects, place cells also displayed improved theta phase precession and theta timescale spike coordination. These results suggest that local visual cues can rapidly tune the resolution of the hippocampal mapping system within and between environments.

Position Reconstruction From an Ensemble of Hippocampal Place Cells: Contribution of Theta Phase Coding

2000 ◽  
Vol 83 (5) ◽  
pp. 2602-2609 ◽  
Author(s):  
Ole Jensen ◽  
John E. Lisman
Keyword(s):  
Hippocampal Neurons ◽  
Place Cells ◽  
Place Field ◽  
Reconstruction Accuracy ◽  
Relative Contribution ◽  
Three Phase ◽  
Phase Precession ◽  
Rate Information ◽  
Theta Phase ◽  
Theta Phase Precession

Previous analysis of the firing of individual rat hippocampal place cells has shown that their firing rate increases when they enter a place field and that their phase of firing relative to the ongoing theta oscillation (7–12 Hz) varies systematically as the rat traverses the place field, a phenomenon termed the theta phase precession. To study the relative contribution of phased-coded and rate-coded information, we reconstructed the animal's position on a linear track using spikes recorded simultaneously from 38 hippocampal neurons. Two previous studies of this kind found no evidence that phase information substantially improves reconstruction accuracy. We have found that reconstruction is improved provided epochs with large, systematic errors are first excluded. With this condition, use of both phase and rate information improves the reconstruction accuracy by >43% as compared with the use of rate information alone. Furthermore, it becomes possible to predict the rat's position on a 204-cm track with very high accuracy (error of <3 cm). The best reconstructions were obtained with more than three phase divisions per theta cycle. These results strengthen the hypothesis that information in rat hippocampal place cells is encoded by the phase of theta at which cells fire.

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