Experience-Driven Rate Modulation is Reinstated During Hippocampal Replay

Replay, the sequential reactivation of a neuronal ensemble, is thought to play a central role in the hippocampus during the consolidation of a recent experience into a long-term memory. Following a contextual change (e.g. entering a novel environment), hippocampal place cells typically modulate their in-field firing rate and shift the position of their place field, providing a rate and place representation for the behavioral episode, respectively. However, replay has been largely defined by only the latter- based on the fidelity of sequential activity across neighboring place fields. Here we show that dorsal CA1 place cells in rats can modulate their firing rate between the replay of two different contexts, mirroring the same pattern of rate modulation observed during behavior. This context-driven rate modulation within replay events was experience-dependent, observable during both behavioral episodes and throughout the subsequent rest period, but not prior to experience. Furthermore, we demonstrate that both the temporal order and firing rate of place cells can independently be used to decode contextual information within a replay event, revealing the existence of two separable but complementary neural representations available for memory consolidation processes.

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Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3

10.1101/2021.02.18.431868 ◽

2021 ◽

Author(s):

Andras Ecker ◽

Bence Bagi ◽

Eszter Vertes ◽

Orsolya Steinbach-Nemeth ◽

Maria Rita Karlocai ◽

...

Keyword(s):

Place Cells ◽

Data Driven ◽

Long Term Memory ◽

Term Memory ◽

Cellular Adaptation ◽

Sharp Wave ◽

Synaptic Interactions ◽

Area Ca3 ◽

Reversed Order

Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated ("replayed"), either in the same or reversed order, during bursts of activity (sharp wave-ripples; SWRs) that occur in sleep and awake rest. SWR-associated replay is thought to be critical for the creation and maintenance of long-term memory. We sought to identify the cellular and network mechanisms of SWRs and replay by constructing and simulating a data-driven model of area CA3 of the hippocampus. Our results show that the structure of recurrent excitatory interactions established during learning not only determines the content of replay, but is essential for the generation of the SWRs as well. We find that bidirectional replay requires the interplay of the experimentally confirmed, temporally symmetric plasticity rule, and cellular adaptation. Our model provides a unifying framework for diverse phenomena involving hippocampal plasticity, representations, and dynamics.

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Memory in multiple sclerosis: Contextual encoding deficits

Journal of the International Neuropsychological Society ◽

10.1017/s1355617702813200 ◽

2002 ◽

Vol 8 (3) ◽

pp. 395-409 ◽

Cited By ~ 53

Author(s):

ALLEN E. THORNTON ◽

NAFTALI RAZ ◽

KAREN A. TUCKER

Keyword(s):

Multiple Sclerosis ◽

Semantic Network ◽

Contextual Information ◽

Long Term Memory ◽

Term Memory ◽

Encoding Specificity ◽

The Impact ◽

Selective Impairment ◽

Encoding And Retrieval

Long-term memory (LTM) is one of the diverse cognitive functions adversely affected by multiple sclerosis (MS). The LTM deficits have often been attributed to failure of retrieval, whereas encoding processes are presumed intact. However, support for this view comes primarily from studies in which encoding and retrieval operations were not investigated systematically. In the current study, we used an encoding specificity paradigm to examine the robustness of encoding in MS and to specifically evaluate the impact of the disease on contextual memory. We hypothesized that persons with MS would exhibit a selective impairment in retrieving items from LTM when required to generate new cue-target associations at encoding, but not when cues held a strong preexisting relationship to the targets. The findings supported the hypotheses. We conclude that the mnemonic deficits associated with MS affect both encoding and retrieval. Specifically, problems with binding of contextual information at encoding impair effective retrieval of memories. Nonetheless, access to these memories can be gained through preexisting associations organized in the semantic network. (JINS, 2002, 8, 395–409.)

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Brief targeted memory reactivation during the awake state enhances memory stability and benefits the weakest memories

10.1101/196436 ◽

2017 ◽

Author(s):

Arielle Tambini ◽

Alice Berners-Lee ◽

Lila Davachi

Keyword(s):

Long Term Memory ◽

Recent Experience ◽

Memory Reactivation ◽

Retrieval Processes ◽

Initial Learning ◽

Explicit Recognition ◽

The Stability ◽

Task Oriented ◽

Or Task

ABSTRACTReactivation of representations corresponding to recent experience is thought to be a critical mechanism supporting long-term memory stabilization. Targeted memory reactivation, or the re-exposure of recently learned cues, seeks to induce reactivation and has been shown to benefit later memory when it takes place during sleep. However, despite recent evidence for endogenous reactivation during post-encoding awake periods, less work has addressed whether awake targeted memory reactivation modulates memory. Here, we found that brief (50ms) visual stimulus re-exposure during a repetitive foil task enhanced the stability of cued versus uncued associations in memory. The extent of external or task-oriented attention prior to re-exposure was inversely related to cueing benefits, suggesting that an internally-orientated state may be most permissible to reactivation. Critically, cueing-related memory benefits were greatest in participants without explicit recognition of cued items and remained reliable when only considering associations not recognized as cued, suggesting that explicit cue-triggered retrieval processes did not drive cueing benefits. Cueing benefits were strongest for items and participants with the poorest initial learning. These findings expand our knowledge of the conditions under which targeted memory reactivation can benefit memory, and in doing so, support the notion that reactivation during awake time periods improves memory stabilization.

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Asymmetry of the temporal code for space by hippocampal place cells

10.1101/060590 ◽

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.

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Storage and erasure of behavioural experiences at the single neuron level

Scientific Reports ◽

10.1038/s41598-019-51331-5 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 3

Author(s):

T. L. Dyakonova ◽

G. S. Sultanakhmetov ◽

M. I. Mezheritskiy ◽

D. A. Sakharov ◽

V. E. Dyakonova

Keyword(s):

Firing Rate ◽

Single Neuron ◽

Lymnaea Stagnalis ◽

Cellular Level ◽

Pond Snail ◽

Recent Experience ◽

Terrestrial Locomotion ◽

Major Interest ◽

The Difference

Abstract Although predictions from the past about the future have been of major interest to current neuroscience, how past and present behavioral experience interacts at the level of a single neuron remains largely unknown. Using the pond snail Lymnaea stagnalis we found that recent experience of terrestrial locomotion (exercise) results in a long-term increase in the firing rate of serotonergic pedal (PeA) neurons. Isolation from the CNS preserved the “memory” about previous motor activity in the neurons even after the animals rested for two hours in deep water after the exercise. In contrast, in the CNS, no difference in the firing rate between the control and “exercise-rested” (ER) neurons was seen. ER snails, when placed again on a surface to exercise, nevertheless showed faster locomotor arousal. The difference in the firing rate between the control and ER isolated neurons disappeared when the neurons were placed in the microenvironment of their home ganglia. It is likely that an increased content of dopamine in the CNS masks an increased excitation of PeA neurons after rest: the dopamine receptor antagonist sulpiride produced sustained excitation in PeA neurons from ER snails but not in the control. Therefore, our data suggest the involvement of two mechanisms in the interplay of past and present experiences at the cellular level: intrinsic neuronal changes in the biophysical properties of the cell membrane and extrinsic modulatory environment of the ganglia.

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Primate ventral striatum maintains neural representations of the value of previously rewarded objects for habitual seeking

Nature Communications ◽

10.1038/s41467-021-22335-5 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Joonyoung Kang ◽

Hyeji Kim ◽

Seong Hwan Hwang ◽

Minjun Han ◽

Sue-Hyun Lee ◽

...

Keyword(s):

Single Unit ◽

Ventral Striatum ◽

Long Term Memory ◽

Response Patterns ◽

Neural Representations ◽

Habitual Behavior ◽

Value Changes ◽

Update Process

AbstractThe ventral striatum (VS) is considered a key region that flexibly updates recent changes in reward values for habit learning. However, this update process may not serve to maintain learned habitual behaviors, which are insensitive to value changes. Here, using fMRI in humans and single-unit electrophysiology in macaque monkeys we report another role of the primate VS: that the value memory subserving habitual seeking is stably maintained in the VS. Days after object-value associative learning, human and monkey VS continue to show increased responses to previously rewarded objects, even when no immediate reward outcomes are expected. The similarity of neural response patterns to each rewarded object increases after learning among participants who display habitual seeking. Our data show that long-term memory of high-valued objects is retained as a single representation in the VS and may be utilized to evaluate visual stimuli automatically to guide habitual behavior.

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Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3

10.21203/rs.3.rs-345804/v1 ◽

2021 ◽

Author(s):

András Ecker ◽

Bence Bagi ◽

Eszter Vértes ◽

Orsolya Steinbach-Németh ◽

Mária Karlócai ◽

...

Keyword(s):

Place Cells ◽

Data Driven ◽

Long Term Memory ◽

Term Memory ◽

Sharp Wave ◽

Synaptic Interactions ◽

Network States ◽

Area Ca3 ◽

Reversed Order

Abstract Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated (``replayed'), either in the same or reversed order, during bursts of activity (sharp wave-ripples; SWRs) that occur in sleep and awake rest. SWR-associated replay is thought to be critical for the creation and maintenance of long-term memory. In order to identify the cellular and network mechanisms of SWRs and replay, we constructed and simulated a data-driven model of area CA3 of the hippocampus. Our results show that the chain-like structure of recurrent excitatory interactions established during learning not only determines the content of replay, but is essential for the generation of the SWRs as well. We find that bidirectional replay requires the interplay of the experimentally confirmed, temporally symmetric plasticity rule, and cellular adaptation. Our model provides a unifying framework for diverse phenomena involving hippocampal plasticity, representations, and dynamics, and suggests that the structured neural codes induced by learning may have greater influence over cortical network states than previously appreciated.

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A novel role for cortical acetylcholine in object memory updating

10.1101/2020.02.08.940064 ◽

2020 ◽

Author(s):

Kristen H. Jardine ◽

Cassidy E. Wideman ◽

Chelsea MacGregor ◽

Cassandra Sgarbossa ◽

Dean Orr ◽

...

Keyword(s):

Information Integration ◽

Contextual Information ◽

Memory Storage ◽

Aging Brain ◽

Long Term Memory ◽

Dependent Manner ◽

Memory Updating ◽

Cholinergic Mechanism ◽

Object Memory

AbstractReactivated long-term memories can become labile and sensitive to modification. Memories in this destabilized state can be weakened or strengthened, but there is limited research characterizing the mechanisms underlying retrieval-induced qualitative updates (i.e., information integration). We have previously implicated cholinergic transmission in object memory destabilization. Here we present a novel rodent paradigm developed to assess the role of this cholinergic mechanism in qualitative memory updating. The post-reactivation object memory modification (PROMM) task exposes rats to contextual information following object memory reactivation. Subsequent object exploratory performance suggests that the contextual information is integrated with the original memory in a reactivation- and time-dependent manner. This effect is blocked by interference with M1 muscarinic receptors and several downstream signals in perirhinal cortex. These findings therefore demonstrate a hitherto unacknowledged cognitive function for acetylcholine with important implications for understanding the dynamic nature of long-term memory storage in the normal and aging brain.

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The Flexibility of Episodic Long-Term Memory-Guided Attention and the Impact of Reinstating Context

SURG Journal ◽

10.21083/surg.v11i0.5357 ◽

2019 ◽

Vol 11 ◽

Author(s):

Diana Segal ◽

Lindsay Plater ◽

Naseem Al-Aidroos ◽

Chris Fiacconi

Keyword(s):

Contextual Information ◽

Spatial Location ◽

Grocery Store ◽

Attention Capture ◽

Sufficient Evidence ◽

Long Term Memory ◽

Sources Of Information ◽

Term Memory ◽

The Impact

While it may seem that salient visual events, like the flashing lights on an ambulance, can automatically capture our attention, capture is actually under our control. Depending on our current internal goals, we adopt attentional control settings (ACSs) that specify what stimuli in the environment capture our attention. It has been shown that ACSs can be defined based on long-term episodic memory representations. For example, when searching for the items on your grocery list, an ACS can be specified based on your long-term memory of the list, such that your attention will be drawn to those items, and only those items. Importantly, episodic memories incorporate contextual information that can enhance recall when reinstated (e.g., you will remember your grocery list better if it was memorized at the grocery store rather than at home). Here we asked whether reinstating context can enhance the establishment of long-term memory ACSs. Participants memorized two sets of 15 images of objects in a particular context (i.e., a coloured box in a particular spatial location), that they then searched for, inducing an episodic-based ACS for those objects. During the search task, this encoding context was either reinstated, or not. We found that individuals are able to flexibly switch between ACSs and sources of information. However, we did not find sufficient evidence for the effect of context on the establishment of ACSs or their flexibility. This study extends our understanding of the factors that influence memory-guided attention, and the impact of contextual reinstatement on the formation of ACSs.

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Interplay between somatic and dendritic inhibition promotes the emergence and stabilization of place fields

10.1101/483875 ◽

2018 ◽

Author(s):

Victor Pedrosa ◽

Claudia Clopath

Keyword(s):

Firing Rate ◽

Place Cell ◽

Place Cells ◽

Place Field ◽

Ca1 Neurons ◽

Hippocampal Ca1 ◽

Place Fields ◽

Cell Stability ◽

Cell Firing ◽

Novel Environments

AbstractDuring exploration of novel environments, place fields are rapidly formed in hippocampal CA1 neurons. Place cell firing rate increases in early stages of exploration of novel environments but returns to baseline levels in familiar environments. However, although similar in amplitude and width, place fields in familiar environments are more stable than in novel environments. We propose a computational model of the hippocampal CA1 network, which describes the formation, the dynamics and the stabilization of place fields. We show that although somatic disinhibition is sufficient to form place cells, dendritic inhibition along with synaptic plasticity is necessary for stabilization. Our model suggests that place cell stability is due to large excitatory synaptic weights and large dendritic inhibition. We show that the interplay between somatic and dendritic inhibition balances the increased excitatory weights, so that place cells return to their baseline firing rate after exploration. Our model suggests that different types of interneurons are essential to unravel the mechanisms underlying place field plasticity. Finally, we predict that artificial induced dendritic events can shift place fields even after place field stabilization.

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