scholarly journals Theta phase precession of grid and place cell firing in open environments

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120532 ◽  
Author(s):  
A. Jeewajee ◽  
C. Barry ◽  
V. Douchamps ◽  
D. Manson ◽  
C. Lever ◽  
...  
Keyword(s):  
Hippocampal Formation ◽  
Field Potential ◽  
Place Cells ◽  
Pool Data ◽  
Grid Cells ◽  
Phase Coding ◽  
Physiological Variables ◽  
Phase Precession ◽  
Field Peak ◽  
Theta Phase

Place and grid cells in the rodent hippocampal formation tend to fire spikes at successively earlier phases relative to the local field potential theta rhythm as the animal runs through the cell's firing field on a linear track. However, this ‘phase precession’ effect is less well characterized during foraging in two-dimensional open field environments. Here, we mapped runs through the firing fields onto a unit circle to pool data from multiple runs. We asked which of seven behavioural and physiological variables show the best circular–linear correlation with the theta phase of spikes from place cells in hippocampal area CA1 and from grid cells from superficial layers of medial entorhinal cortex. The best correlate was the distance to the firing field peak projected onto the animal's current running direction. This was significantly stronger than other correlates, such as instantaneous firing rate and time-in-field, but similar in strength to correlates with other measures of distance travelled through the firing field. Phase precession was stronger in place cells than grid cells overall, and robust phase precession was seen in traversals through firing field peripheries (although somewhat less than in traversals through the centre), consistent with phase coding of displacement along the current direction. This type of phase coding, of place field distance ahead of or behind the animal, may be useful for allowing calculation of goal directions during navigation.

scholarly journals Ripple Band Phase Precession of Place Cell Firing during Replay

2021 ◽  
Author(s):  
Daniel Bush ◽  
Freyja Olafsdottir ◽  
Caswell Barry ◽  
Neil Burgess
Keyword(s):  
Hippocampal Formation ◽  
Receptive Fields ◽  
Negative Relationship ◽  
Place Cell ◽  
Place Cells ◽  
Phase Coding ◽  
Equivalent Rate ◽  
Phase Precession ◽  
Cell Firing ◽  
Ripple Phase

Phase coding offers several theoretical advantages for information transmission compared to an equivalent rate code. Phase coding is shown by place cells in the rodent hippocampal formation, which fire at progressively earlier phases of the movement related 6-12Hz theta rhythm as their spatial receptive fields are traversed. Importantly, however, phase coding is independent of carrier frequency, and so we asked whether it might also be exhibited by place cells during 150-250Hz ripple band activity, when they are thought to replay information to neocortex. We demonstrate that place cells which fire multiple spikes during candidate replay events do so at progressively earlier ripple phases, and that spikes fired across all replay events exhibit a negative relationship between decoded location within the firing field and ripple phase. These results provide insights into the mechanisms underlying phase coding and place cell replay, as well as the neural code propagated to downstream neurons.

scholarly journals Independent theta phase coding accounts for CA1 population sequences and enables flexible remapping

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Angus Chadwick ◽  
Mark CW van Rossum ◽  
Matthew F Nolan
Keyword(s):  
Traveling Wave ◽  
Action Potentials ◽  
Theta Rhythm ◽  
Place Cells ◽  
Population Activity ◽  
Phase Coding ◽  
Synaptic Interactions ◽  
Spike Sequences ◽  
Rate Coding ◽  
Theta Phase

Hippocampal place cells encode an animal's past, current, and future location through sequences of action potentials generated within each cycle of the network theta rhythm. These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies. Instead, we find through simulations and analysis of experimental data that rate and phase coding in independent neurons is sufficient to explain the organization of CA1 population activity during theta states. We show that CA1 population activity can be described as an evolving traveling wave that exhibits phase coding, rate coding, spike sequences and that generates an emergent population theta rhythm. We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity. Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

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.

scholarly journals Transformation of Independent Oscillatory Inputs into Temporally Precise Rate Codes

2016 ◽  
Author(s):  
David Tingley ◽  
Andrew A. Alexander ◽  
Laleh K. Quinn ◽  
Andrea A. Chiba ◽  
Douglas Nitz
Keyword(s):  
Field Potential ◽  
Spatial Location ◽  
Brain Regions ◽  
Synaptic Activity ◽  
Specific Rate ◽  
Attention Task ◽  
Potential Oscillations ◽  
Phase Precession ◽  
Theta Phase ◽  
Theta Phase Precession

AbstractComplex behaviors demand temporal coordination among functionally distinct brain regions. The basal forebrain’s afferent and efferent structure suggests a capacity for mediating such coordination. During performance of a selective attention task, synaptic activity in this region was dominated by four amplitude-independent oscillations temporally organized by the phase of the slowest, a theta rhythm. Further, oscillatory amplitudes were precisely organized by task epoch and a robust input/output transform, from synchronous synaptic activity to spiking rates of basal forebrain neurons, was identified. For many neurons, spiking was temporally organized as phase precessing sequences against theta band field potential oscillations. Remarkably, theta phase precession advanced in parallel to task progression, rather than absolute spatial location or time. Together, the findings reveal a process by which associative brain regions can integrate independent oscillatory inputs and transform them into sequence-specific, rate-coded outputs that are adaptive to the pace with which organisms interact with their environment.

scholarly journals Behavior-dependent spatial maps enable efficient theta phase coding

2021 ◽  
Author(s):  
Eloy Parra-Barrero ◽  
Kamran Diba ◽  
Sen Cheng
Keyword(s):  
Place Cells ◽  
Spatial Representations ◽  
Place Field ◽  
Phase Code ◽  
Phase Precession ◽  
Relevant Variables ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
Exact Relationship ◽  
Speed Characteristic

AbstractNavigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations start behind the animal’s location and then sweep forward. However, the exact relationship between phase and represented and true positions remains unclear and even paradoxical. Here, we formalize previous notions as ‘spatial’ or ‘temporal’ sweeps, analyze single-cell and population variables in recordings from rat CA1 place cells, and compare them to model simulations. We show that neither sweep type quantitatively accounts for all relevant variables. Thus we introduce ‘behavior-dependent’ sweeps, which fit our key observation that sweep length, and hence place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. This structured heterogeneity is essential for understanding the hippocampal code.

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 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.

scholarly journals Neural dynamics indicate parallel integration of environmental and self-motion information by place and grid cells

2019 ◽  
Author(s):  
Dmitri Laptev ◽  
Neil Burgess
Keyword(s):  
Path Integration ◽  
Temporal Dynamics ◽  
Hippocampal Formation ◽  
Place Cell ◽  
Place Cells ◽  
Motion Information ◽  
Grid Cells ◽  
Attractor Network ◽  
Cell Firing ◽  
Self Motion

AbstractPlace cells and grid cells in the hippocampal formation are thought to integrate sensory and self-motion information into a representation of estimated spatial location, but the precise mechanism is unknown. We simulated a parallel attractor system in which place cells form an attractor network driven by environmental inputs and grid cells form an attractor network performing path integration driven by self-motion, with inter-connections between them allowing both types of input to influence firing in both ensembles. We show that such a system is needed to explain the spatial patterns and temporal dynamics of place cell firing when rats run on a linear track in which the familiar correspondence between environmental and self-motion inputs is changed (Gothard et al., 1996b; Redish et al., 2000). In contrast, the alternative architecture of a single recurrent network of place cells (performing path integration and receiving environmental inputs) cannot reproduce the place cell firing dynamics. These results support the hypothesis that grid and place cells provide two different but complementary attractor representations (based on self-motion and environmental sensory inputs respectively). Our results also indicate the specific neural mechanism and main predictors of hippocampal map realignment and make predictions for future studies.

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