Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus

By Annabelle C. Singer, Loren M. Frank. 2009

362 citations recorded by the source corpus.

Remembering experiences that lead to reward is essential for survival. The hippocampus is required for forming and storing memories of events and places, but the mechanisms that associate specific experiences with rewarding outcomes are not understood. Event memory storage is thought to depend on the reactivation of previous experiences during hippocampal sharp wave-ripples (SWRs). We used a novel sequence switching task that allowed us to examine the interaction between SWRs and reward. We compared SWR activity after animals traversed spatial trajectories and either received or did not receive a reward. Here we show that rat hippocampal CA3 principal cells are significantly more active during SWRs following receipt of reward. This SWR activity was further enhanced during learning and reactivated coherent elements of the paths associated with the reward location. This enhanced reactivation in response to reward could be a mechanism to bind rewarding outcomes to the experiences that precede them.

Subfields: Behavioral Neuroscience, Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neuroscience

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Citations in the corpus

Prioritized Experience Replay (2015, background): “Such an asymmetry in replay frequency was also observed in rat studies (Singer & Frank, 2009).”
Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, positive): “…prioritized experience replay was performed based on the magnitude of an experience’s temporal-difference (TD) error, which measures an agent’s learning progress and is consistent with biological findings (Singer & Frank, 2009; McNamara, Tejero-Cantero, Trouche, Campo-Urriza, & Dupret, 2014).”
Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, background): “Reverse replay during behavior seems well suited for linking recently experienced sequences to their outcome, which may promote task learnin”
Sequence Learning and the Role of the Hippocampus in Rodent Navigation (2012, positive): “com reward appears to play a critical role in modulating replay levels [58 ].”
A novel DDPG method with prioritized experience replay (2017, background): “During the learning process, instead of replaying all experiences uniformly, we tend to frequently replay experiences associated with more successful attempts and similar ideas can be referred to [9], [10].”
The content of hippocampal “replay” (2018, background): “These data are at odds with a clear enhancement of reward-based reverse replay in linear tracks (Ambrose et al., 2016; Singer & Frank, 2009).”
Selectivity in Postencoding Connectivity with High-Level Visual Cortex Is Associated with Reward-Motivated Memory (2017, background): “Additionally, recent research in rodents has shown increased “replay” of patterns of prior reward-related activity in the VTA during rest (Singer and Frank, 2009; Valdés et al., 2015), and it has been proposed that these “replay” events Table 1.”
Hippocampal Offline Reactivation Consolidates Recently Formed Cell Assembly Patterns during Sharp Wave-Ripples (2016, background): “Consistent with a role for reactivation in memory consolidation, co-firing patterns associated with spatial novelty or rewarded learning are reactivated more strongly (O’Neill et al., 2008; Singer and Frank, 2009; McNamara et al., 2014), and electrical disruption of hippocampal SWRs during sleep imp”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “The dopaminergic effects may also be related to the increased participation of CA3 pyramidal cells in SPW-Rs when rewarded in a novel environment (Singer and Frank, 2009).”