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| Open AccessGut microbiome drives individual memory variation in bumblebees
Whether gut microbes drive cognitive differences in natural populations of animals remains unknown. Here, Li et al. demonstrate a causal link between increased symbiotic Lactobacillus Firm-5 species (L. apis) and improved long-term memory in bumblebees.
- Li Li
- , Cwyn Solvi
- & Wei Zhao
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| Open AccessMid-lateral cerebellar complex spikes encode multiple independent reward-related signals during reinforcement learning
The role of complex spikes in reinforcement learning is still unclear. Here, the authors show that complex spikes carry multiple context based, cell type specific and learning dependent signals that are independent of changes in any motor kinematics and unlikely to instruct the concurrent simple spike activity during reinforcement learning.
- Naveen Sendhilnathan
- , Anna Ipata
- & Michael E. Goldberg
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| Open AccessAn engram of intentionally forgotten information
The authors used intracranial EEG recordings from patients with epilepsy to show that successful intentional forgetting is due to a selective modification of item-specific top-down connections and not simply a degradation of the memory traces.
- Sanne Ten Oever
- , Alexander T. Sack
- & Nikolai Axmacher
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| Open AccessPartially overlapping spatial environments trigger reinstatement in hippocampus and schema representations in prefrontal cortex
The authors examine how we differentiate highly similar places from each other. They provide evidence for complementary neural mechanisms in the human hippocampus and prefrontal cortex involved in processing interfering and common elements important to remembering places that we have visited.
- Li Zheng
- , Zhiyao Gao
- & Arne D. Ekstrom
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| Open AccessConcept neurons in the human medial temporal lobe flexibly represent abstract relations between concepts
It is unclear how distinct concepts are processed in the brain. Here, the authors recorded from concept cells in human subjects with epilepsy and found that a subset of concept cells responded to non-preferred concepts if those non-preferred concepts required comparison to a preferred concept.
- Marcel Bausch
- , Johannes Niediek
- & Florian Mormann
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| Open AccessOrexin-A and endocannabinoids are involved in obesity-associated alteration of hippocampal neurogenesis, plasticity, and episodic memory in mice
The authors show that adult hippocampal neurogenesis is altered in the dentate gyrus of obese mice with subsequent inhibition of long-term potentiation and impairment of pattern separation. Inhibition of orexin-A action at orexin-1 receptors rescued both impairments in obese mice.
- Nicola Forte
- , Serena Boccella
- & Luigia Cristino
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| Open AccessLateralization of CA1 assemblies in the absence of CA3 input
Bilaterally projecting CA3 inputs may be crucial for integrating the left and right CA1 during memory but this has not been directly examined. Here, the authors show that projections from bilateral CA3 play a key role in the cross-hemispheric coordination of CA1 spatial coding.
- Hefei Guan
- , Steven J. Middleton
- & Thomas J. McHugh
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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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| Open AccessContext value updating and multidimensional neuronal encoding in the retrosplenial cortex
Goal-directed behaviors require the brain to integrate information across many task-related dimensions. Here, the authors use a virtual context discrimination paradigm in mice to demonstrate the capacity for neurons in the retrosplenial cortex to exhibit multidimensional encoding across learning.
- Weilun Sun
- , Ilseob Choi
- & Alexander Dityatev
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Article
| Open AccessDynamics of history-dependent perceptual judgment
Identical physical inputs can evoke non-identical percepts. Here, the authors investigate the sources of such variability and find that rats and humans, trained to judge tactile vibration strength, express a robust sequential effect that could be modeled as the trial-by-trial incorporation of sensory history.
- I. Hachen
- , S. Reinartz
- & M. E. Diamond
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| Open AccessIntegrating pheromonal and spatial information in the amygdalo-hippocampal network
Male and female mice need to generate spatial maps that integrate vomeronasal signals of territory owners in the hippocampus-dependent memory. The authors show that vomeronasal information influences learning-related activity in the hippocampus via the amygdaloid PMCo, lateral entorhinal cortex, and dorsal CA1.
- María Villafranca-Faus
- , Manuel Esteban Vila-Martín
- & Vicent Teruel-Martí
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| Open AccessOpposing roles for striatonigral and striatopallidal neurons in dorsolateral striatum in consolidating new instrumental actions
New instrumental learning occurs through an unexpected delivery of a rewarding stimulus or the withdrawal of a punishing stimulus. The authors show that D1 receptor-expressing medium spiny neurons (MSNs) in the anterior dorsolateral striatum encode newly learned instrumental actions whereas D2 MSNs promote the expression of habitual actions.
- Alexander C. W. Smith
- , Sietse Jonkman
- & Paul J. Kenny
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| Open AccessAbrupt hippocampal remapping signals resolution of memory interference
When two memories are similar, their encoding and retrieval can be disrupted by each other. Here the authors show that memory interference is resolved through abrupt remapping of activity patterns in the human hippocampal CA3 and dentate gyrus.
- Guo Wanjia
- , Serra E. Favila
- & Brice A. Kuhl
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| Open AccessTheta-phase dependent neuronal coding during sequence learning in human single neurons
Previous work has shown that in rodents phase precession – the phase of action potentials relative to the theta oscillation – is associated with the representation of sequential locations. Here the authors demonstrate that phase precession also occurs in the human hippocampus using single neuron and LFP recordings.
- Leila Reddy
- , Matthew W. Self
- & Pieter R. Roelfsema
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| Open AccessWorking memory representations in visual cortex mediate distraction effects
The relative roles of visual, parietal, and frontal cortex in working memory have been actively debated. Here, the authors show that distraction impacts visual working memory representations in primary visual areas, indicating that these regions play a key role in the maintenance of working memory.
- Grace E. Hallenbeck
- , Thomas C. Sprague
- & Clayton E. Curtis
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| Open AccessCognitive functions and underlying parameters of human brain physiology are associated with chronotype
How being a “morning person” or “evening person” affects human cognition and brain physiology is not well understood. Here the authors show evidence of an association of chronotype with cognitive functions and related physiological parameters.
- Mohammad Ali Salehinejad
- , Miles Wischnewski
- & Michael A. Nitsche
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| Open AccessMemory and decision making interact to shape the value of unchosen options
Making a decision requires one to differentiate between choice options, committing to one and leaving the other behind. Here, the authors show that decision-making paradoxically binds options together, such that the outcome of the choice ends up changing the value of both the chosen and the unchosen options, in opposite directions.
- Natalie Biderman
- & Daphna Shohamy
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| Open AccessRemote control of neural function by X-ray-induced scintillation
Scintillators emit visible luminescence when irradiated with X-rays and may enable remote optogenetic control of neurons deep in the brain. The authors inject an inorganic scintillator to activate and inhibit midbrain dopamine neurons in freely moving mice by X-ray irradiation to modulate place preference behavior.
- Takanori Matsubara
- , Takayuki Yanagida
- & Takayuki Yamashita
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| Open AccessDistinct cortical systems reinstate the content and context of episodic memories
People can search for memories based on their content or context, defined as when and where they were formed. Here, the authors use direct brain recordings to provide evidence in line with the idea that separable neural systems retrieve these two types of information and predict whether recall is organized by time or content.
- James E. Kragel
- , Youssef Ezzyat
- & Michael J. Kahana
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| Open AccessAgeing is associated with disrupted reinforcement learning whilst learning to help others is preserved
Evidence suggests older adults engage in more prosocial behaviours compared to younger people. Here the authors investigate prosocial reinforcement learning rates in young and older adults.
- Jo Cutler
- , Marco K. Wittmann
- & Patricia L. Lockwood
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| Open AccessParallel processing of working memory and temporal information by distinct types of cortical projection neurons
Intratelencephalic and pyramidal tract neurons are two major types of cortical excitatory neurons that project to cortical and subcortical structures. The authors show that in the prefrontal cortex the two populations have different roles for the maintenance of working memory and for tracking the passage of time.
- Jung Won Bae
- , Huijeong Jeong
- & Min Whan Jung
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| 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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Article
| Open AccessSynaptic plasticity-dependent competition rule influences memory formation
Cellular activity level at the time of learning is thought to be a critical factor to determine which neurons are recruited to encode memory. Here, the authors show that competitive synaptic plasticity mechanisms influence which neurons will encode a fear memory.
- Yire Jeong
- , Hye-Yeon Cho
- & Jin-Hee Han
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| Open AccessPreference uncertainty accounts for developmental effects on susceptibility to peer influence in adolescence
People often change their preferences to conform with others. Using a longitudinal design, the authors show that such conformity decreases over the course of adolescence and that this reduction in conformity is accompanied by a decreasing degree of uncertainty about what to like.
- Andrea M. F. Reiter
- , Michael Moutoussis
- & Raymond J. Dolan
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| Open AccessThe functional organization of excitatory synaptic input to place cells
Hippocampal place cells contribute to navigation and memory formation. Here, the authors use in vivo glutamate imaging to reveal patterns of excitatory input received by place cell dendrites and find more spatially tuned and functionally organized inputs arriving in the place field.
- Michael D. Adoff
- , Jason R. Climer
- & Daniel A. Dombeck
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| Open AccessSaturated free fatty acids and association with memory formation
Changes in poly-unsaturated free fatty acids (FFAs) have been associated with LTP. Here, using lipidomics analysis the authors characterise FFA changes in the rat brain associated with fear conditioning, and demonstrate that increases in saturated FFAs represent the major change.
- Tristan P. Wallis
- , Bharat G. Venkatesh
- & Frédéric A. Meunier
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| Open AccessHippocampal place cell sequences differ during correct and error trials in a spatial memory task
Here the authors compare place cell sequence coding during correct and error trials in a spatial memory task. Sequences coded paths that were longer and more temporally compressed during correct trials and developed a bias to replay paths to a goal location during rest periods of correct but not error trials.
- Chenguang Zheng
- , Ernie Hwaun
- & Laura Lee Colgin
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| Open AccessFeature-specific reaction times reveal a semanticisation of memories over time and with repeated remembering
Consolidation theories posit that memories gradually change in nature over time. Here the authors use a simple, feature-based reaction time task to show that with time and repeated remembering, access to conceptual features is preserved over perceptual detail, reflecting this qualitative change.
- Julia Lifanov
- , Juan Linde-Domingo
- & Maria Wimber
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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 AccessDistinct place cell dynamics in CA1 and CA3 encode experience in new environments
To understand how spatial representations emerge and evolve across hippocampal subfields, we compared trial-to-trial dynamics of place cells in CA1 and CA3 in new environments and across days. CA1 place fields form early, shift backwards and partially remap across days whereas in CA3 they develop gradually and are more stable, suggesting distinct functional roles in representing space.
- Can Dong
- , Antoine D. Madar
- & Mark E. J. Sheffield
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| Open AccessNet decrease in spine-surface GluA1-containing AMPA receptors after post-learning sleep in the adult mouse cortex
The synaptic mechanisms of how sleep benefits cognitive functions are not well characterised. Here, the authors show that sleep leads to an overall net decrease in spine-surface GluA1-containing AMPA receptors and that this is correlated with changes in performance after sleep.
- Daisuke Miyamoto
- , William Marshall
- & Chiara Cirelli
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| Open AccessNon-invasive, opsin-free mid-infrared modulation activates cortical neurons and accelerates associative learning
Neurostimulant drugs or magnetic/electrical stimulation techniques have shown limited effects on learning capabilities of healthy subjects. The authors show that, without introducing an exogeneous gene, mid-infrared light can modulate firing activity of neurons in vivo and accelerate learning in mice.
- Jianxiong Zhang
- , Yong He
- & Xiaowei Chen
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| Open AccessBidirectional propagation of low frequency oscillations over the human hippocampal surface
New microgrid recordings on the human hippocampal surface reveal that oscillations travel in reversing directions. The route of travel at a given moment was related to behavior and topographic patterns of activity strength, suggesting directions may be biomarkers of hippocampal cognitive processes.
- Jonathan K. Kleen
- , Jason E. Chung
- & Edward F. Chang
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| Open AccessA network linking scene perception and spatial memory systems in posterior cerebral cortex
Navigation requires integration of visual information with spatial memory representations. Steel et al. describe a new network of brain areas that facilitates the interaction between these perceptual and mnemonic neural systems.
- Adam Steel
- , Madeleine M. Billings
- & Caroline E. Robertson
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| Open AccessHigh-frequency head impact causes chronic synaptic adaptation and long-term cognitive impairment in mice
Repeated head impact exposure can cause memory and behavioural impairments but the physiological changes in the brain are not well understood. Here, the authors reveal synaptic adaptations as a potential mechanism for early abnormal behavioural events observed after mild and high-frequency head impact.
- Stephanie S. Sloley
- , Bevan S. Main
- & Mark P. Burns
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| Open AccessLearning with reinforcement prediction errors in a model of the Drosophila mushroom body
Dopamine neurons in the mushroom body help Drosophila learn to approach rewards and avoid punishments. Here, the authors propose a model in which dopaminergic learning signals encode reinforcement prediction errors by utilising feedback reinforcement predictions from mushroom body output neurons.
- James E. M. Bennett
- , Andrew Philippides
- & Thomas Nowotny
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| Open AccessSex differences in fear memory consolidation via Tac2 signaling in mice
The Tachykinin 2 (Tac2) pathway in the central amygdala is sufficient and necessary for modulating fear memory consolidation. The authors show that silencing Tac2 neurons in the amygdala of male mice reduces fear expression, while fear expression in female mice is increased when manipulations are made during proestrus.
- A. Florido
- , E. R. Velasco
- & R. Andero
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| Open AccessSingle cell plasticity and population coding stability in auditory thalamus upon associative learning
How thalamic sensory relays participate in plasticity upon associative fear learning and stable long-term sensory coding remains unknown. The authors show that auditory thalamus neurons exhibit heterogeneous plasticity patterns after learning while population level encoding of auditory stimuli remains stable across days.
- James Alexander Taylor
- , Masashi Hasegawa
- & Jan Gründemann
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| Open AccessClone-structured graph representations enable flexible learning and vicarious evaluation of cognitive maps
Higher-order sequence learning using a structured graph representation - clone-structured cognitive graphs (CSCG) – can explain how the hippocampus learns cognitive maps. CSCG provides novel explanations for transferable schemas and transitive inference in the hippocampus, and for how place cells, splitter cells, lap-cells and a variety of phenomena emerge from the same set of fundamental principles.
- Dileep George
- , Rajeev V. Rikhye
- & Miguel Lázaro-Gredilla
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| Open AccessAutonomous Purkinje cell activation instructs bidirectional motor learning through evoked dendritic calcium signaling
Plastic reweighting of parallel fiber synaptic strength is a mechanism for the acquisition of cerebellum-dependent motor learning. Here, the authors found that optogenetic activation of PCs generates dendritic Ca2+ signals that induce plasticity in vitro and instruct learned changes to coincident eye movements in vivo.
- Audrey Bonnan
- , Matthew M. J. Rowan
- & Jason M. Christie
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| Open AccessVarying demands for cognitive control reveals shared neural processes supporting semantic and episodic memory retrieval
Making sense of the world around us often requires flexible access to information from both semantic and episodic memory systems. Here, the authors show that controlled retrieval from functionally distinct long-term memory stores is supported by shared neural processes in the human brain.
- Deniz Vatansever
- , Jonathan Smallwood
- & Elizabeth Jefferies
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| Open AccessNeural alignment predicts learning outcomes in students taking an introduction to computer science course
Learning and remembering new information is a major challenge for students of all levels. Here, the authors show that “neural alignment” across brains is associated with learning success of STEM concepts in a real-life college course and predicts learning outcomes.
- Meir Meshulam
- , Liat Hasenfratz
- & Uri Hasson
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| Open AccessAdult-born neurons immature during learning are necessary for remote memory reconsolidation in rats
The role of adult hippocampal neurogenesis in memory reconsolidation is unclear. Here, the authors show that memory retrieval activates both immature and mature adult-born neurons. However, only adult-born neurons immature during learning are required for remote memory reconsolidation in rats.
- Marie Lods
- , Emilie Pacary
- & Sophie Tronel
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| Open AccessDynamics of fMRI patterns reflect sub-second activation sequences and reveal replay in human visual cortex
Non-invasive measurement of fast neural activity with spatial precision in humans is difficult. Here, the authors show how fMRI can be used to detect sub-second neural sequences in a localized fashion and report fast replay of images in visual cortex that occurred independently of the hippocampus.
- Lennart Wittkuhn
- & Nicolas W. Schuck
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Article
| Open AccessA neural m6A/Ythdf pathway is required for learning and memory in Drosophila
Epitranscriptomic modifications can regulate learning and memory. Here, the authors provide proteomic and functional analysis of N6-methyladenosine (m6A)-binding proteins in D. melanogaster and unveil behavioral and regulatory defects for m6A/Ythdf mutants.
- Lijuan Kan
- , Stanislav Ott
- & Eric C. Lai
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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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Article
| Open AccessDopaminergic mechanism underlying reward-encoding of punishment omission during reversal learning in Drosophila
Unexpected omission of aversive outcome is encoded as reward via activation of reward-encoding dopaminergic neurons in animals. The authors identify the Drosophila neural circuit through which reward-encoding dopaminergic neurons are activated when an olfactory cue is no longer paired with punishment.
- Li Yan McCurdy
- , Preeti Sareen
- & Michael N. Nitabach
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| Open AccessFrontotemporal coordination predicts working memory performance and its local neural signatures
Here, the authors show that beta-band coordination between prefrontal and temporal cortex predicts working memory performance. Moreover, inferior temporal neurons exhibits greater memory activity when coordination between these areas is high, suggesting that this interaction supports object memory maintenance.
- Ehsan Rezayat
- , Mohammad-Reza A. Dehaqani
- & Behrad Noudoost
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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