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| Open AccessContext memory formed in medial prefrontal cortex during infancy enhances learning in adulthood
Early life experience contributes to behaviour in later life. Here the authors show in rats, that the infant brain, during a critical period, forms lasting memories of the spatial context of experiences; in adulthood, these memories involving medial prefrontal cortex improve spatial abilities in similar contexts.
- María P. Contreras
- , Marta Mendez
- & Marion Inostroza
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| Open AccessEarly excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight
The role neurochemistry plays in encoding newly-acquired motor skills remains unclear. Here, the authors use multimodal imaging to show that early inhibitory and excitatory changes promote overnight behavioral, structural, and connectivity-related gains.
- Tamir Eisenstein
- , Edna Furman-Haran
- & Assaf Tal
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| Open AccessAwake ripples enhance emotional memory encoding in the human brain
The neural dynamics of emotional memory consolidation are not well understood. Here, the authors analyse intracranial recordings from human participants after emotional memory encoding, showing that ripple-locked activity in the amygdala and hippocampus is predictive of subsequent memory.
- Haoxin Zhang
- , Ivan Skelin
- & Jack J. Lin
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| Open AccessRespiration modulates sleep oscillations and memory reactivation in humans
The memory function of sleep relies on the coordination of slow oscillations and spindles. Here the authors show that respiration is associated with the emergence and interplay of these sleep rhythms, and that this coupling is linked to memory reactivation.
- Thomas Schreiner
- , Marit Petzka
- & Bernhard P. Staresina
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| Open AccessCA3 hippocampal synaptic plasticity supports ripple physiology during memory consolidation
Memory consolidation requires hippocampal ripples. Here the authors show that AMPA receptor mobilisation at CA3 recurrent synapses is required for ripple-dependent rule consolidation.
- Hajer El Oussini
- , Chun-Lei Zhang
- & Yann Humeau
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| Open AccessCortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue
The mechanisms of episodic memory are not well understood. Here, the authors show that the reactivation of non-spatial information precedes the reactivation of spatial information, and that both are correlated with hippocampal sharp-wave ripples.
- HaoRan Chang
- , Ingrid M. Esteves
- & Bruce L. McNaughton
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| Open AccessTime-dependent memory transformation in hippocampus and neocortex is semantic in nature
Memories are transformed over time. Here, the authors show that this transformation is semantic in nature and linked to transformed event representations in neocortex and increased pattern reinstatement in the posterior hippocampus, while they find no credible evidence for a perceptual transformation.
- Valentina Krenz
- , Arjen Alink
- & Lars Schwabe
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Article
| Open AccessLocating causal hubs of memory consolidation in spontaneous brain network in male mice
How long-lasting memory is formed remains incompletely understood. Here, using fMRI and hub silencing, the authors discovered causal network hubs that are instrumental in consolidating memory and contributing to network reorganization.
- Zengmin Li
- , Dilsher Athwal
- & Kai-Hsiang Chuang
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| Open AccessSystems consolidation induces multiple memory engrams for a flexible recall strategy in observational fear memory in male mice
In observational contextual fear conditioning (OCFC), animals learn to fear the context in which they witnessed a demonstrator’s aversive experience. Here, the authors show that recall of OCFC relies on different brain areas, depending on recency of the experience and the observer’s current context.
- Joseph I. Terranova
- , Jun Yokose
- & Takashi Kitamura
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| Open AccessFunctional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation
Thalamic spindle activities may support memory consolidation. Here the authors show that optogenetically-evoked somatosensory thalamic spindle-like activity enhances memory performance in male rats.
- Xunda Wang
- , Alex T. L. Leong
- & Ed X. Wu
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Article
| Open AccessMemory for nonadjacent dependencies in the first year of life and its relation to sleep
Grammar learning requires memory for temporally organised, rule-based patterns in speech. Here, the authors use event-related potentials to show that 6 to 8 month-old infants can form memory of dependencies between nonadjacent elements in sentences of an unknown language, regardless of whether they nap or stay awake after encoding.
- Manuela Friedrich
- , Matthias Mölle
- & Angela D. Friederici
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Article
| Open AccessSleep-like unsupervised replay reduces catastrophic forgetting in artificial neural networks
Artificial neural networks are known to perform well on recently learned tasks, at the same time forgetting previously learned ones. The authors propose an unsupervised sleep replay algorithm to recover old tasks synaptic connectivity that may have been damaged after new task training.
- Timothy Tadros
- , Giri P. Krishnan
- & Maxim Bazhenov
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Article
| Open AccessSchemas provide a scaffold for neocortical integration of new memories over time
It remains unclear how past experiences shape how new information is acquired and represented in the brain. Here, the authors provide data suggesting that past experiences influence neocortical integration and the organization of new overlapping memories across time.
- Sam Audrain
- & Mary Pat McAndrews
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| Open AccessThalamo-hippocampal pathway regulates incidental memory capacity in mice
Incidental memory is affected by retention delay, and by memory load. Here the authors show that female and male mice process high memory load through different activation of thalamic-cortical pathways, that makes their incidental memory resistant to distraction and to memory decay, respectively.
- G. Torromino
- , V. Loffredo
- & E. De Leonibus
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| Open AccessCoordinated hippocampal-thalamic-cortical communication crucial for engram dynamics underneath systems consolidation
Systems consolidation refers to the reorganization of memory engrams across brain regions. The authors present a biologically-plausible computational model that shows that hippocampal-thalamic-cortical activity is crucial for systems consolidation, making testable predictions for experimental neuroscience.
- Douglas Feitosa Tomé
- , Sadra Sadeh
- & Claudia Clopath
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| Open AccessBreathing coordinates cortico-hippocampal dynamics in mice during offline states
Using large-scale recordings from cortical and subcortical brain regions in behaving mice, the authors reveal the presence of a respiratory corollary discharge in mice, that modulates neural activity across these circuits and couples hippocampal sharp-wave ripples and cortical DOWN/UP state transitions.
- Nikolaos Karalis
- & Anton Sirota
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| Open AccessNoradrenergic arousal after encoding reverses the course of systems consolidation in humans
Memories are assumed to undergo a time-dependent systems consolidation, during which hippocampal contributions to memory decrease while neocortical contributions increase. Here, the authors show that noradrenergic arousal after encoding may reverse this course of systems consolidation in humans
- Valentina Krenz
- , Tobias Sommer
- & Lars Schwabe
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Article
| Open AccessReward biases spontaneous neural reactivation during sleep
Sleep is known to promote memory consolidation, but the extent to which this is dependent on the memory’s relevance remains unclear. Here, the authors use a brain decoding approach to show that neural representations of rewarded experiences undergo a privileged reactivation during sleep, favouring their consolidation.
- Virginie Sterpenich
- , Mojca K. M. van Schie
- & Sophie Schwartz
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| Open AccessEndogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes
Sleep after learning helps to strengthen new memories. Here, the authors link this memory benefit to the reactivation of learning experiences when two endogenous sleep rhythms—slow oscillations and sleep spindles—coincide.
- Thomas Schreiner
- , Marit Petzka
- & Bernhard P. Staresina
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| Open AccessCausal role for sleep-dependent reactivation of learning-activated sensory ensembles for fear memory consolidation
Learning-activated engram neurons play a critical role in memory recall but the role of these neurons in offline memory consolidation is unclear. The authors show that sleep-associated reactivation of learning-activated sensory neurons is necessary for memory consolidation.
- Brittany C. Clawson
- , Emily J. Pickup
- & Sara J. Aton
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| Open AccessTravelling spindles create necessary conditions for spike-timing-dependent plasticity in humans
Sleep spindles during non-rapid eye movement are important for memory consolidation and require specific neuronal firing conditions in non-human mammals. Here, the authors show these conditions are present in humans, potentially facilitating spike-timing-dependent plasticity.
- Charles W. Dickey
- , Anna Sargsyan
- & Eric Halgren
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| Open AccessRpd3/CoRest-mediated activity-dependent transcription regulates the flexibility in memory updating in Drosophila
The flexibility of memory updating may be determined in the initial memory consolidation process. Here, the authors show the proteomic changes of the transcriptional repressor complexes required for initial memory consolidation and influencing the flexibility of future memory updating.
- Mai Takakura
- , Reiko Nakagawa
- & Yukinori Hirano
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| Open AccessInhibitory neurotransmission drives endocannabinoid degradation to promote memory consolidation
Endocannabinoid levels are controlled by the fine balance between their synthesis and degradation. Here, the authors show that memory formation through fear conditioning selectively accelerates the degradation of endocannabinoids in the cerebellum via a lasting increase in GABA release.
- Christophe J. Dubois
- , Jessica Fawcett-Patel
- & Siqiong June Liu
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Article
| Open AccessZeta Inhibitory Peptide attenuates learning and memory by inducing NO-mediated downregulation of AMPA receptors
Zeta inhibitory peptide (ZIP) impairs the maintenance of acquired memories. ZIP is known as an inhibitor of PKMζ. Here, the authors unveil how ZIP impairs memory maintenance acting as an arginine donor, facilitating NO-dependent down-regulation of AMPARs, independently of its action on PKMζ.
- Alexey Bingor
- , Tomer Haham
- & Rami Yaka
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Article
| Open AccessSleep-dependent memory consolidation in infants protects new episodic memories from existing semantic memories
In infants, superiority of semantic over episodic memory formation has been postulated. Here, authors show that both types of memory coexist in one-year-olds, with consolidation during sleep affecting whether an experienced event is recognized as a detailed episode or as general semantic knowledge.
- Manuela Friedrich
- , Matthias Mölle
- & Jan Born
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Article
| Open AccessOffline ventral subiculum-ventral striatum serial communication is required for spatial memory consolidation
Spatial information is passed from the hippocampus via the subiculum to the ventral striatum. Here, the authors show that inhibiting this projection after spatial learning disrupts learning induced plasticity and spatial memory consolidation.
- G. Torromino
- , L. Autore
- & A. Mele
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Article
| Open AccessClosed-loop control of gamma oscillations in the amygdala demonstrates their role in spatial memory consolidation
Gamma oscillations have been proposed to underlie many cognitive and memory processes, but it has proven difficult to directly test this by manipulating them. Here, in rats, the authors show that manipulation of gamma oscillations in the amygdala affects memory consolidation.
- Vasiliki Kanta
- , Denis Pare
- & Drew B. Headley
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Article
| Open AccessBidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
How are memories transferred from short-term to long-term storage? Here, the authors show that during deep (NREM) sleep, the prefrontal cortex initiates rapid, bidirectional interactions to trigger information transfer from the hippocampus to the neocortex.
- Randolph F. Helfrich
- , Janna D. Lendner
- & Robert T. Knight
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Article
| Open AccessRetroactive and graded prioritization of memory by reward
Rewarding events are prioritized in memory, but to support adaptive decision-making memory should also be prioritized for the events leading up to a reward. Here, the authors show that reward retroactively prioritizes memory for proximal, neutral events that precede the reward.
- Erin Kendall Braun
- , G. Elliott Wimmer
- & Daphna Shohamy
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Article
| Open AccessDopamine-dependent prefrontal reactivations explain long-term benefit of fear extinction
The success of extinction learning is not predictive of long-term retrieval of an extinction memory. Using fMRI to study consolidation of fear extinction in human subjects, the authors show that reactivation in the ventromedial prefrontal cortex during memory retrieval predicts extinction memory retrieval, and that increasing dopaminergic signaling increases the number of these activations.
- A. M. V. Gerlicher
- , O. Tüscher
- & R. Kalisch
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Article
| Open AccessTime units for learning involving maintenance of system-wide cFos expression in neuronal assemblies
Learning often involves multiple exposures and trials, but it is not known whether those are treated independently, or integrated during dedicated time windows. Here, Chowdhury and Caroni show mice learn new associations during 5 h time windows, where related experiences are integrated in a process requiring coordinated cFos-activated neuronal assemblies.
- Ananya Chowdhury
- & Pico Caroni
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| Open AccessElectrophysiological mechanisms of human memory consolidation
It is believed that fast “ripple” oscillations in the hippocampus play a role in consolidation, a process by which memory traces are stabilized. Here, the authors show that ripples occuring during non-REM sleep trigger “replay” of brain activity associated with previously experienced stimuli.
- Hui Zhang
- , Juergen Fell
- & Nikolai Axmacher
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| Open AccessHuman hippocampal replay during rest prioritizes weakly learned information and predicts memory performance
The hippocampus is known to 'replay' experiences and memories during rest periods, but it is unclear how particular memories are prioritized for replay. Here, the authors show that information that is remembered less well is replayed more often, suggesting that weaker memories are selected for replay.
- Anna C. Schapiro
- , Elizabeth A. McDevitt
- & Kenneth A. Norman
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| Open AccessInfralimbic cortex is required for learning alternatives to prelimbic promoted associations through reciprocal connectivity
Prelimbic (PL) and infralimbic (IL) cortical areas are known to have complementary roles in learning and decision making. Here the authors report reciprocal connectivity between the two areas and elucidate their functional impact on different aspects of learning.
- Arghya Mukherjee
- & Pico Caroni
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Article
| Open AccessLow frequency transcranial electrical stimulation does not entrain sleep rhythms measured by human intracranial recordings
Transcranial alternating current stimulation (tACS) has been proposed to enhance neural rhythms supporting memory. Here, the authors leverage human intracranial recordings to show that low-frequency tACS does not entrain key rhythms in non-REM sleep or resting wakefulness.
- Belen Lafon
- , Simon Henin
- & Anli A. Liu
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| Open AccessDecoding material-specific memory reprocessing during sleep in humans
Neuronal learning activity is reactivated during sleep but the dynamics of this reactivation in humans are still poorly understood. Here the authors show that memory processing occurs during all stages of sleep in humans but that reprocessing of memory content in REM and non-REM sleep has different effects on later memory performance.
- M. Schönauer
- , S. Alizadeh
- & S. Gais
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| Open AccessParvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation
Episodic memory consolidation requires activity in hippocampal area CA1. Here the authors report that pharmacogenetic inhibition of CA1 PV+ interneuron firing after fear learning blocks memory consolidation and disrupts associated enhancement in network oscillations and stabilization of functional connectivity patterns.
- Nicolette Ognjanovski
- , Samantha Schaeffer
- & Sara J. Aton
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| Open AccessMemory consolidation reconfigures neural pathways involved in the suppression of emotional memories
As memories consolidate over time, they become resistant to change, though how this impacts the volitional suppression of memories is not known. Liu and colleagues show that, after overnight consolidation, aversive memories exhibit distributed prefrontal representations and are harder to suppress.
- Yunzhe Liu
- , Wanjun Lin
- & Shaozheng Qin
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Article
| Open AccessSCOP/PHLPP1β mediates circadian regulation of long-term recognition memory
Learning and memory are subject to circadian variation, though the molecular mechanisms behind this are unclear. Here, the authors show SCOP, a regulator of hippocampal memory, undergoes circadian changes in CA1 membrane raft dynamics and contributes to time-dependent changes in long-term memory.
- Kimiko Shimizu
- , Yodai Kobayashi
- & Yoshitaka Fukada
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| Open AccessCellular tagging as a neural network mechanism for behavioural tagging
Short-term memories (STM) can become long-term memories when occurring alongside novel experiences. Here, the authors investigate the neural mechanisms behind such 'behavioural tagging' and find STM neural populations are preferentially incorporated into the ensembles encoding novel experiences.
- Masanori Nomoto
- , Noriaki Ohkawa
- & Kaoru Inokuchi
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pT305-CaMKII stabilizes a learning-induced increase in AMPA receptors for ongoing memory consolidation after classical conditioning
The protein kinase CaMKII modulates synaptic plasticity and learning in both vertebrate and invertebrate organisms. In this study, the authors demonstrate a role for autophosphorylated CaMKII (pT305-CaMKII) in maintaining memory consolidation after classical conditioning in the invertebrate species Lymnaea.
- Souvik Naskar
- , Huimin Wan
- & György Kemenes
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| Open AccessSusceptibility of memory consolidation during lapses in recall
Memory lapses during memory consolidation are periods when the memory becomes briefly inaccessible after its formation. Marra and colleagues study memory lapses in the mollusc Lymnaea, and find that only during these lapses is consolidation of memories susceptible to interruption by external disturbances.
- Vincenzo Marra
- , Michael O’Shea
- & Ildikó Kemenes
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Dynamic histone marks in the hippocampus and cortex facilitate memory consolidation
Changes in gene expression in the hippocampus and the cortex are pivotal for memory consolidation. Gräff and colleagues use a recognition task in mice to show that epigenetic post-translational modifications are rapidly activated in the hippocampus after learning, but induced with a delay in the cortex.
- Johannes Gräff
- , Bisrat T. Woldemichael
- & Isabelle M. Mansuy