scholarly journals Efficient phase coding in hippocampal place cells

2019 ◽  
Author(s):  
Pavithraa Seenivasan ◽  
Rishikesh Narayanan
Keyword(s):  
High Efficiency ◽  
Place Cells ◽  
Intrinsic Properties ◽  
Place Field ◽  
Phase Coding ◽  
Efficient Coding ◽  
Coding Efficiency ◽  
Synergistic Interactions ◽  
Phase Precession ◽  
Sequence Compression

ABSTRACTHippocampal place cells encode space through phase precession, whereby neuronal spike phase progressively advances during place-field traversals. What neural constraints are essential for achieving efficient transfer of information through such phase codes, while concomitantly maintaining signature neuronal excitability specific to individual cell types? We developed a conductance-based model for phase precession in CA1 pyramidal neurons within the temporal sequence compression framework, and defined phase-coding efficiency using information theory. We recruited an unbiased stochastic search strategy to build a model population that exhibited physiologically observed heterogeneities in intrinsic properties. Place-field responses elicited from these models matched signature sub- and supra-threshold place-cell characteristics, including phase precession, sub-threshold voltage ramps, increases in theta-frequency power and firing rate during place-field traversals. Employing this model population, we show that disparate parametric combinations with weak pair-wise correlations resulted in models with similar high-efficiency phase codes and similar excitability characteristics. Mechanistically, the emergence of such parametric degeneracy was dependent on the differential and variable impact of individual ion channels on phase-coding efficiency in different models, and importantly, on synergistic interactions between synaptic and intrinsic properties. Furthermore, our analyses predicted a dominant role for calcium-activated potassium channels in regulating phase precession and coding efficiency. Finally, change in afferent statistics, manifesting as input asymmetry, induced an adaptive shift in the phase code that preserved its efficiency, apart from introducing asymmetry in sub-threshold ramps and firing profiles during place-field traversals. Our study postulates degeneracy as a potential framework to attain the twin goals of efficient temporal coding and robust homeostasis.SIGNIFICANCE STATEMENTNeuronal intrinsic properties exhibit significant baseline heterogeneities, and change with activity-dependent plasticity and neuromodulation. How do hippocampal neurons encode spatial locations through the precise timings of their action potentials in the face of such heterogeneities? Here, employing a unifying synthesis of the temporal sequence compression, efficient coding and degeneracy frameworks, we show that there are several disparate routes for neurons to achieve high-efficiency spatial information transfer through such temporal codes. These disparate routes were consequent to the ability of neurons to produce precise encoding through distinct structural components, critically involving synergistic interactions between intrinsic and synaptic properties. Our results point to an explosion in the degrees of freedom available to a neuron in concomitantly achieving efficient coding and excitability homeostasis.

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 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 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 Intracellular Dynamics of Virtual Place Cells

2011 ◽  
Vol 23 (3) ◽  
pp. 651-655 ◽  
Author(s):  
Sandro Romani ◽  
Terrence J. Sejnowski ◽  
Misha Tsodyks
Keyword(s):  
Hippocampal Neurons ◽  
Theta Rhythm ◽  
Spatial Location ◽  
Place Cells ◽  
Intracellular Recordings ◽  
Place Field ◽  
Potential Oscillations ◽  
Phase Precession ◽  
Intracellular Mechanism ◽  
Membrane Potential Oscillations

The pattern of spikes recorded from place cells in the rodent hippocampus is strongly modulated by both the spatial location in the environment and the theta rhythm. The phases of the spikes in the theta cycle advance during movement through the place field. Recently intracellular recordings from hippocampal neurons (Harvey, Collman, Dombeck, & Tank, 2009 ) showed an increase in the amplitude of membrane potential oscillations inside the place field, which was interpreted as evidence that an intracellular mechanism caused phase precession. Here we show that an existing network model of the hippocampus (Tsodyks, Skaggs, Sejnowski, & McNaughton, 1996 ) can equally reproduce this and other aspects of the intracellular recordings, which suggests that new experiments are needed to distinguish the contributions of intracellular and network mechanisms to phase precession.

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.

Inheritance of Hippocampal Place Fields Through Hebbian Learning: Effects of Theta Modulation and Phase Precession on Structure Formation

2015 ◽  
Vol 27 (8) ◽  
pp. 1624-1672 ◽  
Author(s):  
Tiziano D’Albis ◽  
Jorge Jaramillo ◽  
Henning Sprekeler ◽  
Richard Kempter
Keyword(s):  
Hebbian Learning ◽  
Learning Rule ◽  
Place Cells ◽  
Spike Timing ◽  
Upstream Region ◽  
Place Field ◽  
Hebbian Learning Rule ◽  
Phase Precession ◽  
Place Fields ◽  
Field Formation

A place cell is a neuron that fires whenever the animal traverses a particular location of the environment—the place field of the cell. Place cells are found in two regions of the rodent hippocampus: CA3 and CA1. Motivated by the anatomical connectivity between these two regions and by the evidence for synaptic plasticity at these connections, we study how a place field in CA1 can be inherited from an upstream region such as CA3 through a Hebbian learning rule, in particular, through spike-timing-dependent plasticity (STDP). To this end, we model a population of CA3 place cells projecting to a single CA1 cell, and we assume that the CA1 input synapses are plastic according to STDP. With both numerical and analytical methods, we show that in the case of overlapping CA3 input place fields, the STDP learning rule leads to the formation of a place field in CA1. We then investigate the roles of the hippocampal theta modulation and phase precession on the inheritance process. We find that theta modulation favors the inheritance and leads to faster place field formation whereas phase precession changes the drift of CA1 place fields over time.

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.

scholarly journals Directional Tuning of Phase Precession Properties in the Hippocampus

2021 ◽  
Author(s):  
Yuk-Hoi Yiu ◽  
Jill K Leutgeb ◽  
Christian Leibold
Keyword(s):  
Place Cells ◽  
Spike Timing ◽  
Motor Drive ◽  
Place Field ◽  
Directional Information ◽  
Field Activity ◽  
Phase Precession ◽  
Cornu Ammonis ◽  
Theta Phase ◽  
Theta Phase Precession

Running direction in the hippocampus is encoded by rate modulations of place field activity but also by spike timing correlations known as theta sequences. Whether directional rate codes and the directionality of place field correlations are related, however, has so far not been explored and therefore the nature of how directional information is encoded in the cornu ammonis remains unresolved. Here, using a previously published dataset that contains the spike activity of rat hippocampal place cells in the CA1, CA2 and CA3 subregions during free foraging of male Long-Evans rats in a 2D environment, we found that rate and spike timing codes are related. Opposite to a place field's preferred firing rate direction spikes are more likely to undergo theta phase precession and, hence, more strongly impact paired correlations. Furthermore, we identified a subset of field pairs whose theta correlations are intrinsic in that they maintain the same firing order when the running direction is reversed. Both effects are associated with differences in theta phase distributions, and are more prominent in CA3 than CA1. We thus hypothesize that intrinsic spiking is most prominent when the directionally modulated sensory-motor drive of hippocampal firing rates is minimal, suggesting that extrinsic and intrinsic sequences contribute to phase precession as two distinct mechanisms.

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