Ripple band phase precession of place cell firing during replay

Bush, Daniel; Ólafsdóttir, Hildur; Barry, Caswell; Burgess, Neil

doi:10.1016/j.cub.2021.10.033

Cited by 11 publications

(9 citation statements)

References 59 publications

(109 reference statements)

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“…More generally, in principle, any form of sufficiently ordered and compressed trajectory would allow STDP plasticity to approximate a successor representation. Hippocampal replay is a well documented phenomena where previously experienced trajectories are rapidly recapitulated during sharp-wave ripple events [75], within which spikes show a form of phase precession relative to the ripple band oscillation (150-250Hz) [76]. Thus, our model might explain the abundance of sharp-wave ripples during early exposure to novel environments [77] – when new ‘informative’ trajectories, for example those which lead to reward, are experienced it is desirable to rapidly incorporate this information into the existing predictive map [78].…”

Section: Discussionmentioning

confidence: 99%

Rapid learning of predictive maps with STDP and theta phase precession

George

Cothi

Stachenfeld

et al. 2022

Preprint

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The predictive map hypothesis is a promising candidate principle for hippocampal function. A favoured formalisation of this hypothesis, called the successor representation, proposes that each place cell encodes the expected state occupancy of its target location in the near future. This predictive framework is supported by behavioural as well as electrophysiological evidence and has desirable consequences for both the generalisability and efficiency of reinforcement learning algorithms. However, it is unclear how the successor representation might be learnt in the brain. Error-driven temporal difference learning, commonly used to learn successor representations in artificial agents, is not known to be implemented in hippocampal networks. Instead, we demonstrate that spike-timing dependent plasticity (STDP), a form of Hebbian learning, acting on temporally compressed trajectories known as “theta sweeps”, is sufficient to rapidly learn a close approximation to the successor representation. The model is biologically plausible – it uses spiking neurons modulated by theta-band oscillations, diffuse and overlapping place cell-like state representations, and experimentally matched parameters. We show how this model maps onto known aspects of hippocampal circuitry and explains substantial variance in the true successor matrix, consequently giving rise to place cells that demonstrate experimentally observed successor representation-related phenomena including backwards expansion on a 1D track and elongation near walls in 2D. Finally, our model provides insight into the observed topographical ordering of place field sizes along the dorsal-ventral axis by showing this is necessary to prevent the detrimental mixing of larger place fields, which encode longer timescale successor representations, with more fine-grained predictions of spatial location.

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Section: Discussionmentioning

confidence: 99%

Rapid learning of predictive maps with STDP and theta phase precession

George

Cothi

Stachenfeld

et al. 2022

Preprint

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“…As an animal crosses a place field, spikes of pyramidal cells (PYRs) in the hippocampus and associated regions occur at progressively earlier theta phases (1)(2)(3). Precession also occurs outside of the hippocampal formation (4,5) and in relation to high-frequency (6) and nonoscillatory (7) bands. In the hippocampus, precession encodes space (8)(9)(10), time (11)(12)(13), objects (14), and events (15).…”

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confidence: 99%

Local activation of CA1 pyramidal cells induces theta-phase precession

Sloin,

Spivak,

Levi

et al. 2024

Science

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Hippocampal theta-phase precession is involved in spatiotemporal coding and in generating multineural spike sequences, but how precession originates remains unresolved. To determine whether precession can be generated directly in hippocampal area CA1 and disambiguate multiple competing mechanisms, we used closed-loop optogenetics to impose artificial place fields in pyramidal cells of mice running on a linear track. More than one-third of the CA1 artificial fields exhibited synthetic precession that persisted for a full theta cycle. By contrast, artificial fields in the parietal cortex did not exhibit synthetic precession. These findings are incompatible with precession models based on inheritance, dual-input, spreading activation, inhibition-excitation summation, or somato-dendritic competition. Thus, a precession generator resides locally within CA1.

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“…During replay, the neural representations of a past experience can be compressed in time [15][16][17][18][19] . These replay events frequently coincide with sharp-wave ripples (SWRs), which are high-frequency (150-220 Hz) ripple oscillations 20,21 observed in the local field potential 22,23 associated with learning processes [24][25][26] . Thus far, existing studies exclusively focused on replay induced by sequence learning within task-dependent contexts.…”

Section: Introductionmentioning

confidence: 97%

Non-feature-specific elevated responses and feature-specific backward replay in human brain induced by visual sequence exposure

He,

Gong,

Wang

et al. 2023

Preprint

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The brain demonstrates a sustained capacity for cortical plasticity, as extensively studied in task-dependent training contexts. However, the cortical plasticity induced by exposure-based learning has been largely ignored despite its potential significance in promoting generalization and adaptability, thereby allowing individuals to effortlessly apply their knowledge across diverse tasks. One of the key mechanisms underlying the cortical plasticity induced by learning is the replay of learned events, as originally described for rodents and recently identified in humans. In the current study, we recorded magnetoencephalography (MEG) signals to investigate the relationship between exposure-based sequence learning and replay in the human brain. Participants were exposed to a predefined sequence of four motion directions for 30 min, and subsequently presented with start/end motion direction of the sequence as a cue aiming to induce replay of the motion sequence. During the post-cue blank period, we observed a backward replay of the motion sequence in a time-compressed manner. These effects were marginally significant even for a very brief exposure. However, when we flashed the second or third motion direction of the sequence as a cue, no replay events were observed. Further analyses revealed that activity in the medial temporal lobe (MTL) preceded the ripple power in the visual cortex at replay onset, implying a potentially coordinated relationship between the activity in the MTL and visual cortex. Taken together, our study demonstrated the rapid development of replay events induced by simple visual exposure in humans, providing new insights into the mechanisms underlying cortical plasticity even without explicit training tasks.

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Ripple band phase precession of place cell firing during replay

Cited by 11 publications

References 59 publications

Rapid learning of predictive maps with STDP and theta phase precession

Rapid learning of predictive maps with STDP and theta phase precession

Local activation of CA1 pyramidal cells induces theta-phase precession

Non-feature-specific elevated responses and feature-specific backward replay in human brain induced by visual sequence exposure

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