Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory

By T. Dugladze, D. Schmitz, Miles A. Whittington, Imre Vida, T. Gloveli. Science, 2012

879 citations recorded by the source corpus.

Spatial Memory Perturbation The hippocampus is important for learning and memory. However, it is not clear which patterns of neural activity in the hippocampus support specific mnemonic functions. Jadhav et al. (p. 1454, published online 3 May) developed a real-time analysis system to detect and selectively interrupt a certain type of hippocampal neuronal network event—sharp-wave ripples—during learning. In awake animals, loss of sharp-wave ripples and associated memory replay activity caused a learning deficit specific to spatial working memory but had no effect on reference memory. This learning deficit was present despite the preservation of place-field representations and replay activity during rest. The neuronal “replay” of past experience may allow animals to retrieve specific memories and use them to guide behavior. The hippocampus is critical for spatial learning and memory. Hippocampal neurons in awake animals exhibit place field activity that encodes current location, as well as sharp-wave ripple (SWR) activity during which representations based on past experiences are often replayed. The relationship between these patterns of activity and the memory functions of the hippocampus is poorly understood. We interrupted awake SWRs in animals learning a spatial alternation task. We observed a specific learning and performance deficit that persisted throughout training. This deficit was associated with awake SWR activity, as SWR interruption left place field activity and post-experience SWR reactivation intact. These results provide a link between awake SWRs and hippocampal memory processes, which suggests that awake replay of memory-related information during SWRs supports learning and memory-guided decision-making.

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

View Paper: https://www.semanticscholar.org/paper/eb4f496dce54d0ab163779972872df2747c58e08

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Citations in the corpus

Navigating cognition: Spatial codes for human thinking (2018, background): “learning and planning (115) and the disruption of sequences during sharp-wave ripples impairs successful performance (116).”
Memory consolidation. (2015, background): “This work has hinted at the possibility that replay during sleep is important for consolidation processes, whereas awake replay is more associated with spatial working memory and navigational planning (Girardeau et al. 2009; Ego-Stengel and Wilson 2010; Jadhav et al. 2012; Pfeiffer and Foster 2013).”
Interplay of hippocampus and prefrontal cortex in memory (2013, positive): “Consistent with this expectation, hippocampal neural ensembles have been shown to replay place cell firing sequences during sleep and quiet waking periods following learning in rodents [20], and blocking this replay prevents subsequent memory retrieval [21].”
The content of hippocampal “replay” (2018, background): “…slow-wave sleep, quiet rest, grooming, and eating/drinking (Buzs aki, 1986, 2015), and disruption in their expression results in significant memory impairments (Ego-Stengel & Wilson, 2010; Girardeau et al., 2009; Jadhav et al., 2012; Nakashiba et al., 2009; Nokia et al., 2012; Wang et al., 2015a).”
The Role of Hippocampal Replay in Memory and Planning (2018, background): “When sharp wave ripples were disrupted at non-decision points performance was preserved (right) [120].”
Integrating memories to guide decisions (2015, background): “However, although hippocampal preplay appears to support correct navigational performance on simple spatial tasks [26,27], it has not so far been studied while animals were performing behavioral tasks that specifically require or demonstrate integrative, model-based decisions.”
Switching between internal and external modes: A multiscale learning principle (2017, background): “Disrupting these ripples disrupts learning (Jadhav, Kemere, German, & Frank 2012).”
Replay Comes of Age. (2017, background): “…these with the actual future behaviors and the outcomes of those behaviors to learn a model of the animal’s own behavior, although studies demonstrating the necessity and correlation of replay to performance in choice tasks would seem to contradict this ( Jadhav et al. 2012, Singer et al. 2013).”
Neuromodulation of brain states. (2012, positive): “Selective interruption of hippocampal ripple events during wakefulness impairs spatial learning (Jadhav et al., 2012), similar to the effect of ripple disruption during sleep (Ego-Stengel and Wilson, 2010; Girardeau et al., 2009).”