Coordinated hippocampal-thalamic-cortical communication crucial for engram dynamics underneath systems consolidation

Tomé, Douglas Feitosa; Sadeh, Sadra; Clopath, Claudia

doi:10.1038/s41467-022-28339-z

Cited by 18 publications

(9 citation statements)

References 95 publications

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“…However, a biologically detailed thalamocortical neural network model using a Hebbian learning rule has been developed to engage with these dynamics and provides important insights into how they may contribute to memory consolidation ( 54 – 56 ). We view this model and others that make more direct contact with lower level neural mechanisms ( 90 ) as complementary to our approach. Having these models at different levels of abstraction is useful in creating the full bridge from individual neurons to dynamics across systems to higher-level behavioral phenomena—for example, our use of a rate code allows for easier simulation of more complex tasks, and may help our framework scale to larger networks.…”

Section: Discussionmentioning

confidence: 97%

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Singh

Norman

Schapiro

2022

Proc. Natl. Acad. Sci. U.S.A.

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How do we build up our knowledge of the world over time? Many theories of memory formation and consolidation have posited that the hippocampus stores new information, then “teaches” this information to the neocortex over time, especially during sleep. But it is unclear, mechanistically, how this actually works—How are these systems able to interact during periods with virtually no environmental input to accomplish useful learning and shifts in representation? We provide a framework for thinking about this question, with neural network model simulations serving as demonstrations. The model is composed of hippocampus and neocortical areas, which replay memories and interact with one another completely autonomously during simulated sleep. Oscillations are leveraged to support error-driven learning that leads to useful changes in memory representation and behavior. The model has a non–rapid eye movement (NREM) sleep stage, where dynamics between the hippocampus and neocortex are tightly coupled, with the hippocampus helping neocortex to reinstate high-fidelity versions of new attractors, and a REM sleep stage, where neocortex is able to more freely explore existing attractors. We find that alternating between NREM and REM sleep stages, which alternately focuses the model’s replay on recent and remote information, facilitates graceful continual learning. We thus provide an account of how the hippocampus and neocortex can interact without any external input during sleep to drive useful new cortical learning and to protect old knowledge as new information is integrated.

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Section: Discussionmentioning

confidence: 97%

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Singh

Norman

Schapiro

2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Note that, these connections are not of the same nature. Excitatory functional connections from HPC to PFC are mainly modulated by intermediate regions (for example, the thalamus Tomé et al, 2022). In this case, the strength of the connections W HP C−P F C reflect the coupling strength of hippocampal and PFC oscillatory activity.…”

Section: Multi-region Recurrent Neural Networkmentioning

confidence: 99%

Memory’s gatekeeper: the role of PFC in the encoding of familiar events

Guerreiro,

Clopath

2024

Preprint

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Theoretical models conventionally portray the consolidation of memories as a slow process that unfolds during sleep. According to the classical Complementary Learning Systems (CLS) theory (as presented in J. McClelland et al., 1995), the hippocampus (HPC) rapidly changes its connectivity during wakefulness to encode ongoing events and create memory ensembles that are later transferred to the prefrontal cortex (PFC) during sleep. However, recent experimental studies challenge this notion by showing that new information consistent with prior knowledge can be rapidly consolidated in PFC during wakefulness, and that PFC lesions disrupt the encoding of familiar events in the HPC. These results challenge the widely accepted view that consolidation is a slow process that unfolds during sleep and highlight the role of PFC during the initial stages of memory encoding. The contributions of the PFC to memory encoding have therefore largely been overlooked. Moreover, most theoretical frameworks assume random and uncorrelated patterns representing memories, disregarding the correlations between our experiences. To address this shortcomings, we developed a HPC-PFC network model that simulates interactions between the HPC and PFC during the encoding of a memory (awake stage), and subsequent consolidation (sleeping stage) to examine the contributions of each region to the consolidation of novel and familiar memories. Our results show that the PFC network uses stored memory "schemas" consolidated during previous experiences to identify inputs that evoke familiar patterns of activity, quickly integrated it in its network, and gate which components are encoded in the HPC. More specifically, the PFC uses GABAergic long-range projections to inhibit HPC neurons representing input components correlated with a previously stored memory "schema", eliciting sparse hippocampal activity during exposure to familiar events, as it has been experimentally observed.

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“…However, the consistency of this interaction is not always reliable, and not every time an SWR ends up finishing an UP state. It is important to discuss that it is possible that other brain circuits, such as the thalamus, may be required to be included in this process to increase the probability of this coordination (Tomé, Sadeh, and Clopath 2022). In addition, an alternative hypothesis be that SWRs and replays, such as those that propagate along the hippocampal longitudinal axis, may have a stronger impact on cortical Down states of the RTC or PFC during certain memory-related processes, particularly during the reactivation of long and extended experiences (Davidson, Kloosterman, and Wilson 2009;Yamamoto and Tonegawa 2017).…”

Section: Down States Of the Rtc Are Strongly Coordinated To Hippocamp...mentioning

confidence: 99%

Hippocampal memory reactivation during sleep is correlated with specific cortical states of the Retrosplenial and Prefrontal Cortices

Feliciano‐Ramos¹,

Penagos²,

Galazo³

et al. 2023

Preprint

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Episodic memories are thought to be stabilized through the coordination of cortico-hippocampal activity during sleep. However, the timing and mechanism of this coordination remain unknown. To investigate this, we studied the relationship between hippocampal reactivation and slow-wave sleep UP and Down states of the retrosplenial cortex (RTC) and prefrontal cortex (PFC). We found that hippocampal reactivation are strongly correlated with specific cortical states. Reactivation occurred during sustained cortical UP states or during the transition from UP to Down state. Interestingly, sustained UP states from the PFC were more coordinated with memory reactivation in the hippocampus, whereas hippocampal reactivation was biased to occur during the cortical UP to Down state transition of the RTC. Reactivation usually occurred within 150-200 ms of a cortical UP-state onset, indicating that a build-up of excitation during cortical UP-state activity influences the probability of memory reactivation in CA1. Conversely, CA1 reactivation occurred 30-50 ms before the onset of a cortical Down state, suggesting that memory reactivation affects Down state initiation in RTC and PFC, but the effect in RTC was more robust. Our findings provide evidence that supports and highlights the complexity of bidirectional communication between cortical regions and the hippocampus during sleep.

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Coordinated hippocampal-thalamic-cortical communication crucial for engram dynamics underneath systems consolidation

Cited by 18 publications

References 95 publications

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Memory’s gatekeeper: the role of PFC in the encoding of familiar events

Hippocampal memory reactivation during sleep is correlated with specific cortical states of the Retrosplenial and Prefrontal Cortices

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