Post-learning Hippocampal Replay Selectively Reinforces Spatial Memory for Highly Rewarded Locations

Michon, Frédéric; Sun, Jyh-Jang; Kim, Chae Young; Ciliberti, Davide; Kloosterman, Fabian

doi:10.1016/j.cub.2019.03.048

Cited by 76 publications

(113 citation statements)

References 48 publications

(67 reference statements)

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“…Moreover, experiment involving manipulations, for example of particular aspects of an experience or directly of brain activity, benefits from the ability to compare the effects with internal controls from the same animals, between or within the same experimental sessions. The dual reward-place association paradigm is suitable for neuronal recordings and manipulations (Michon et al 2019) : the use of radial arms enables to render the behavior of the animals more stereotypical, the training can be repeated over weeks by every day changing the locations to be learned and it allows the use of internal controls between and within sessions.…”

Section: Discussionmentioning

confidence: 99%

“…We developed a novel paradigm to study the selective retention of memories in rodents in which the retention of two, concomitantly acquired, food-place associations is assessed every day. This behavioral paradigm was successfully used to confirm the improved memory retention of experiences associated with larger reward size, and further, to demonstrate the causal role of post-learning hippocampal replay in the reward-related enhancement of memory consolidation (Michon et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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A Dual Reward-Place Association Task to Study the Preferential Retention of Relevant Memories in Rats

Michon

Sun

Kim

et al. 2020

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Memories of past events and common knowledge are critical to flexibly adjust one’s future behavior based on prior experiences. The formation and the transformation of these memories into a long-lasting form are supported by a dialog between the coordinated activity of population of neurons in the cortex and the hippocampus. Not all experiences are remembered equally well nor for equally long. It has been demonstrated experimentally in humans that memory strength positively depends on the behavioral relevance of the associated experience. Behavioral paradigms testing the selective retention of memory in rodents would enable to further investigate the neuronal mechanisms at play. We developed a novel paradigm to follow the repeated acquisition and retrieval of two contextually distinct, yet concurrently occurring, food-place associations in rats. We demonstrated the use of this paradigm by varying the amount of reward associated with the two locations. After delays of 2h or 20h, rats showed better memory performance for experiences associated with larger amount of reward. This effect depends on the level of spatial integration required to retrieve the associated location. Thus, this paradigm is suited to study the preferential retention of relevant experiences in rats.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A Dual Reward-Place Association Task to Study the Preferential Retention of Relevant Memories in Rats

Michon

Sun

Kim

et al. 2020

Preprint

Self Cite

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“…4A). This simple learning effect, while often not considered as previous knowledge effect, does affect session performance and thus, must be considered even in experiments which just focus on each session individually, as seen in most electrophysiological experiments (Lopes-Dos-Santos et al, 2018;Michon et al, 2019;Roux et al, 2017).…”

Section: Previous Knowledge Effectsmentioning

confidence: 99%

The HexMaze: A previous knowledge and schema task for mice

Bokeria¹,

Eichler²,

Brincker³

et al. 2018

Preprint

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New information is rarely learned in isolation, instead most of what we experience can be incorporated into or uses previous knowledge networks in some form. However, most rodent laboratory tasks assume the animal to be naïve with no previous experience influencing the results. Previous knowledge in form of a schema can facilitate knowledge acquisition and accelerate systems consolidation: memories become more rapidly hippocampal independent and instead rely more on the prefrontal cortex. Here, we developed a new spatial navigation task where food locations are learned in a large, gangway maze -the HexMaze. Analysing performance across sessions as well as on specific trials, we can show simple memory effects as well as multiple effects of previous knowledge accelerating both online learning and performance increases over offline periods. Importantly, we are the first to show that schema build-up is dependent on how much time passes, not how often the animal is trained.

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“…At a molecular level, synaptic, 'tagging' for information prioritised for storage, protein synthesis and synaptic modifications occur within hours of encountering information (14,15). The dopaminergic connection between midbrain and hippocampus may selectively bias long-term memory storage by altering synaptic tagging or the protein synthesis involved in synaptic tagging (15)(16)(17).…”

Section: Introductionmentioning

confidence: 99%

“…As well as prospectively prioritising, or tagging, memories for later replay during sleep, dopamine may directly act during sleep per se (18). As engram storage evolves, newly acquired memories are spontaneously repeated (17); sleep affords an optimal neurophysiological state during which to enact this process -although replay occurs during wake too (19). Patterns of activation within hippocampal neuronal assemblies are selectively replayed during sharp wave ripples which are, in turn, temporally coupled to sleep spindles and slow oscillations, prominent during non-REM sleep (20)(21)(22)(23)(24).…”

Section: Introductionmentioning

confidence: 99%

Dopamine-gated memory selection during slow wave sleep

Isotalus

Carr

Averill

et al. 2020

Preprint

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The human brain selectively stores knowledge of the world to optimise future behaviour, automatically rehearsing, contextualising or discarding information to create a robust record of experiences. Storage or forgetting evolves over time, particularly during sleep. We sought to test how dopamine shaped long term memory formation before and during sleep. We administered dopamine (L-DOPA tablet) during learning, re-learning, consolidation or retrieval of word lists in two independent double-blind randomised placebo-controlled cross-over studies of healthy older adults (study 1 n = 35, study 2 n = 32). During consolidation, nocturnal dopamine accelerated forgetting for words presented once, but did not affect words presented twice from forgetting. Overnight dopamine increased total slow wave sleep duration by approximately 11%. The effect of dopamine on memory correlated with increased spindle amplitude, which was maximised near slow oscillation peaks, suggesting dopamine-dependent memory processing modulates spindles dependent on slow-oscillation phase. Pharmaceutical modification of slow wave sleep holds great promise for improving old age – potential benefits could include cognitive enhancement and Alzheimer’s prevention.

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Post-learning Hippocampal Replay Selectively Reinforces Spatial Memory for Highly Rewarded Locations

Abstract: Highlights d Rats show stronger memory for highly rewarded locations d Disruption of hippocampal SWRs only affects memory for highly rewarded locations d Hippocampal replay events are biased to trajectories associated with high reward

Cited by 76 publications

References 48 publications

A Dual Reward-Place Association Task to Study the Preferential Retention of Relevant Memories in Rats

A Dual Reward-Place Association Task to Study the Preferential Retention of Relevant Memories in Rats

The HexMaze: A previous knowledge and schema task for mice

Dopamine-gated memory selection during slow wave sleep

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