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| Open AccessMultidimensional memory topography in the medial parietal cortex identified from neuroimaging of thousands of daily memory videos
Autobiographical memories are associated with activity in the hippocampus and the parietal cortex. Here the authors characterise the neural substrates for retrieving autobiographical memories from a large dataset, and identify a topography within the medial parietal cortex that reflects memory content, age, and memory strength.
- Wilma A. Bainbridge
- & Chris I. Baker
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| Open AccessInducing forgetting of unwanted memories through subliminal reactivation
Classical forgetting methods typically re-expose people to reminders of their unwanted memories. Here, the authors disrupt unpleasant memories by subliminally reactivating them as participants suppress retrieval of unrelated neutral memories, avoiding the need for conscious exposure.
- Zijian Zhu
- , Michael C. Anderson
- & Yingying Wang
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| Open AccessAversive memory formation in humans involves an amygdala-hippocampus phase code
The amygdala facilitates memory encoding in the hippocampus. Here the authors show, using simultaneous intracranial recordings from these regions, that emotional memory encoding is mediated by the amygdala theta phase to which hippocampal gamma activity and neuronal firing is coupled.
- Manuela Costa
- , Diego Lozano-Soldevilla
- & Bryan A. Strange
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| Open AccessΔFosB accumulation in hippocampal granule cells drives cFos pattern separation during spatial learning
In mice, reactivation of neurons that express cFos during fear conditioning induces a behavioural response. Here the authors show that cFos expression in mouse dentate gyrus shifts every day to different neurons, even during highly consistent spatial navigation, and suggest this clock-like selection mechanism may aid the encoding of episodic memories.
- Paul J. Lamothe-Molina
- , Andreas Franzelin
- & Thomas G. Oertner
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| Open AccessSalience memories formed by value, novelty and aversiveness jointly shape object responses in the prefrontal cortex and basal ganglia
How object salience is encoded in the cortex and basal ganglia remains incompletely understood. Here, the authors show that individual prefrontal cortex neurons are jointly sensitive to the memory of value, aversiveness, novelty, and recency of objects, while the substantia nigra reticulata filters out novelty and recency signals but amplifies value and aversive memories.
- Ali Ghazizadeh
- & Okihide Hikosaka
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| Open AccessHemisphere-specific spatial representation by hippocampal granule cells
Lateralization of hippocampal function has been observed in CA1-3, but the extent to which there is lateralization in the dentate gyrus is less clear. Using 2-photon calcium imaging of granule cells over five days in mice, the authors explore differences in spatial encoding between the left and right dentate gyrus.
- Thibault Cholvin
- & Marlene Bartos
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Article
| Open AccessBrainstem networks construct threat probability and prediction error from neuronal building blocks
The prevailing view of threat computation is a division of labor in which the forebrain signals threat and the brainstem organizes behavior. Using neuropixels, the authors show that brainstem neurons organize into a functional network to signal threat.
- Jasmin A. Strickland
- & Michael A. McDannald
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| Open AccessPerception and memory have distinct spatial tuning properties in human visual cortex
Neural activity from perception is thought to be reactivated during memory recall. Here, the authors show that memory reactivation in visual cortex exhibits different tuning properties from those observed during perception.
- Serra E. Favila
- , Brice A. Kuhl
- & Jonathan Winawer
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Article
| Open AccessFlexibility of functional neuronal assemblies supports human memory
Neuronal assemblies remain understudied in human data. Here, the authors show that gamma phase-locked neuronal firing sequences comprise assemblies in human single unit recordings, and their ability to incorporate new neurons over time facilitates memory.
- Gray Umbach
- , Ryan Tan
- & Bradley Lega
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Article
| Open AccessA neural theory for counting memories
It is unclear how the brain keeps track of the number of times different events are experienced. Here, a neural circuit is proposed for this problem inspired by a classic solution in computer science, and evidence of this circuit is shown in the fruit fly brain.
- Sanjoy Dasgupta
- , Daisuke Hattori
- & Saket Navlakha
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| Open AccessBehaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility
Cross-species research is key to fully understanding brain function. Here, the authors present the ferret as a species for hippocampal research and show that, in stark contrast to rats, ferrets have robust theta oscillations during immobility.
- Soraya L. S. Dunn
- , Stephen M. Town
- & Daniel Bendor
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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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Article
| Open AccessInsular cortical circuits as an executive gateway to decipher threat or extinction memory via distinct subcortical pathways
Ensembles of fear and extinction memories compete and interact to drive opposing behaviors. Here the authors identified insular cortical circuits as an executive gateway that decipher between fear and extinction memories via distinct subcortical pathways.
- Qi Wang
- , Jia-Jie Zhu
- & Tian-Le Xu
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| Open AccessReactivating hippocampal-mediated memories during reconsolidation to disrupt fear
The hippocampus is a brain region critically involved in memory. In this study, the authors demonstrate that reactivating hippocampal neurons associated with positive memories can disrupt a fear response in mice.
- Stephanie L. Grella
- , Amanda H. Fortin
- & Steve Ramirez
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Article
| Open AccessSmall, correlated changes in synaptic connectivity may facilitate rapid motor learning
How animals are able to rapidly adapt their behaviour to changing environmental demands remains poorly understood. Here, the authors use a modelling approach to show that synaptic plasticity in motor cortex may underlie rapid motor learning, demonstrating that small, correlated connectivity changes that preserve neural covariance are highly effective in driving behavioural adaptation.
- Barbara Feulner
- , Matthew G. Perich
- & Claudia Clopath
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| Open AccessStriatal dopamine dissociates methylphenidate effects on value-based versus surprise-based reversal learning
The mechanisms underpinning the variability in methylphenidate’s effects on cognition remain unclear. Here, the authors show that such effects reflect changes in striatal dopamine-related output gating of task-relevant cortical signals, and that these changes depend on baseline dopamine synthesis capacity.
- Ruben van den Bosch
- , Britt Lambregts
- & Roshan Cools
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| Open AccessA direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory
The mammalian hippocampal formation plays a key role in several higher brain functions. Here, the authors show that excitatory neurons in layer 6b of the mouse EC project to all sub-regions comprising the hippocampal formation and receive input from the CA1, thalamus and claustrum.
- Yoav Ben-Simon
- , Karola Kaefer
- & Peter Jonas
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Article
| Open AccessSocial incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity
Social experiences influence future decision making. The authors here establish a method for quantifying this phenomenon in mice and identify an amygdalo-frontal-striatal circuit controlling how social context shapes decisions.
- Henry W. Kietzman
- , Gracy Trinoskey-Rice
- & Shannon L. Gourley
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| Open AccessCingulate-motor circuits update rule representations for sequential choice decisions
The anterior cingulate cortex allows an animal to update its behaviour when the environment changes. In this work, the authors identify a pathway from cingulate to secondary motor cortex, critical for updating motor rules following behavioural errors.
- Daigo Takeuchi
- , Dheeraj Roy
- & Susumu Tonegawa
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Article
| Open AccessPACAP-PAC1R modulates fear extinction via the ventromedial hypothalamus
The PACAP-PAC1R neuropeptide system regulates neuroendocrine stress responses. Here the authors demonstrate a role for PACAP-PAC1R in ventromedial hypothalamus in modulating fear extinction.
- E. R. Velasco
- , A. Florido
- & R. Andero
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| Open AccessNoise correlations in neural ensemble activity limit the accuracy of hippocampal spatial representations
CA1 neurons encode an animal's position within the environment. Here the authors identified in hippocampal neuronal activity a detrimental type of noise that limits accuracy of spatial position, relative to body size.
- Omer Hazon
- , Victor H. Minces
- & Pablo E. Jercog
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| Open AccessPredicting memory from the network structure of naturalistic events
Naturalistic experiences often have complex structure, consisting of multiple inter-related events. Here, the authors show that the semantic and causal interconnectedness of events in narratives positively predicts memory performance and neural responses associated with memory encoding and recall.
- Hongmi Lee
- & Janice Chen
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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 AccessA synaptic signal for novelty processing in the hippocampus
Memory formation and recall are complementary processes within the hippocampus. Here the authors demonstrate a synaptic signal of novelty in the hippocampus and provide a computational framework for how such a novelty-driven switch may enable flexible encoding of new memories while preserving stable retrieval of familiar ones.
- Ruy Gómez-Ocádiz
- , Massimiliano Trippa
- & Christoph Schmidt-Hieber
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| Open AccessSex-specific regulation of inhibition and network activity by local aromatase in the mouse hippocampus
Using a combination of molecular, genetic, functional and behavioural tools, this study describes the impact of brain synthesized estrogen in inhibitory neuronal function, network oscillations and hippocampal dependent memory.
- Alicia Hernández-Vivanco
- , Nuria Cano-Adamuz
- & Pablo Méndez
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| Open AccessDopamine encodes real-time reward availability and transitions between reward availability states on different timescales
Dopamine in the ventral striatum conveys a complex reward-associated signal. This study demonstrates how dopamine reflects sustained reward availability, and rapidly signals unexpected changes in availability.
- Abigail Kalmbach
- , Vanessa Winiger
- & Eleanor H. Simpson
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| Open AccessExisting function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task
Using an optical brain computer interface in mice, here the authors demonstrate that new skill acquisition is not inherently disruptive to existing function. These findings suggest neural networks are robust to perturbations associated with integrating new information.
- Brian B. Jeon
- , Thomas Fuchs
- & Sandra J. Kuhlman
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| Open AccessHippocampal representations switch from errors to predictions during acquisition of predictive associations
Successfully exploiting the regularities in our environment requires balancing the encoding of new information with the retrieval of stored associations. Here, the authors show that the hippocampus switches from representing novel information (errors) to representing predictions as learning proceeds.
- Fraser Aitken
- & Peter Kok
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Article
| Open AccessMolecular encoding and synaptic decoding of context during salt chemotaxis in C. elegans
The nematode C. elegans moves around to find an optimal environment. This work demonstrates how it can detect and move towards a previously learned salinity using the salt-sensing neuron ASER.
- Shingo Hiroki
- , Hikari Yoshitane
- & Yuichi Iino
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| Open AccessThe representation of context in mouse hippocampus is preserved despite neural drift
Recent work has shown that the tuning of hippocampal place cells changes unexpectedly across weeks, a phenomenon known as neural drift. Keinath et al. show that this drift occurs in a particular way, one which preserves the representation of context.
- Alexandra T. Keinath
- , Coralie-Anne Mosser
- & Mark P. Brandon
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| Open AccessAn energizing role for motivation in information-seeking during the early phase of the COVID-19 pandemic
Information-seeking behavior in humans is often viewed as irrational rather than utility maximizing. Here the authors describe data obtained in Spring 2020 showing that participants’ concern about COVID-19 was related not only to their drive to seek information about the virus, but also to their curiosity about other more general topics.
- Yaniv Abir
- , Caroline B. Marvin
- & Daphna Shohamy
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| Open AccessInformation normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment
Prior experience is used by the brain to guide adaptive behaviour during decision making. Here, the authors show that mice also selectively use information learned through recent and longer-term experience beyond just prior actions and reward to guide adaptive behaviour.
- Drew C. Schreiner
- , Christian Cazares
- & Christina M. Gremel
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| Open AccessAngular and linear speed cells in the parahippocampal circuits
It remains unclear how the hippocampal region integrates position and self-motion information to update spatial representations. Here, the authors report grid and head direction cells as well as cells encoding self-motion parameters such as angular head velocity and speed, and find conjunctive representations of these different parameters.
- Davide Spalla
- , Alessandro Treves
- & Charlotte N. Boccara
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| Open AccessBrain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions
Where memories are located in our brains is not well understood. In this paper, the authors demonstrate that memories are spread out throughout multiple brain regions.
- Dheeraj S. Roy
- , Young-Gyun Park
- & Susumu Tonegawa
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| Open AccessFixational drift is driven by diffusive dynamics in central neural circuitry
Between saccades, our eyes undergo random movements called fixational drift, but what drives this motion has remained elusive. In this paper, the authors demonstrate that a central neural circuit within the oculomotor system drives fixational drift.
- Nadav Ben-Shushan
- , Nimrod Shaham
- & Yoram Burak
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| Open AccessFlexible auditory training, psychophysics, and enrichment of common marmosets with an automated, touchscreen-based system
The authors present a cage-based stand-alone platform for autonomous, standardized, and unsupervised training and testing of visuo-auditory-cued behaviours of common marmosets. The experiments do not require dietary restriction or social separation.
- A. Calapai
- , J. Cabrera-Moreno
- & M. Jeschke
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| Open AccessAcquiring new memories in neocortex of hippocampal-lesioned mice
Hippocampal lesioned mice form new memories. Here, the authors show the lateral entorhinal cortex modulates learning-induced cortical long-range gamma synchrony in a hippocampal-dependent manner and artificially induced cortical gamma synchrony across cortical areas improved memory encoding in hippocampal lesioned mice.
- Wenhan Luo
- , Di Yun
- & Ji-Song Guan
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| Open AccessLower novelty-related locus coeruleus function is associated with Aβ-related cognitive decline in clinically healthy individuals
Older individuals exhibiting diminished function of the locus coeruleus while learning new information show faster cognitive decline that is typical for Alzheimer’s disease.
- Prokopis C. Prokopiou
- , Nina Engels-Domínguez
- & Heidi I. L. Jacobs
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| Open AccessMultiplexed action-outcome representation by striatal striosome-matrix compartments detected with a mouse cost-benefit foraging task
The role that the striatum plays in tracking the association between actions and combinations of rewarding and aversive outcomes remains unclear. Here, by using both calcium imaging in mice and reinforcement learning models, the authors find that individual striatal neurons can encode associations between actions and multiple, sometimes conflicting, outcomes.
- Bernard Bloem
- , Rafiq Huda
- & Ann M. Graybiel
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| Open AccessDe novo inter-regional coactivations of preconfigured local ensembles support memory
The authors show that fear-memory-related cell-ensembles in the amygdala, hippocampus, and prefrontal cortex are inter-regionally co-activated in post-learning sleep. The co-activations are hosted by fast network oscillations and re-appear during recall.
- Hiroyuki Miyawaki
- & Kenji Mizuseki
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Article
| Open AccessInhibition allocates spikes during hippocampal ripples
The sequences of neuronal spikes during hippocampal sharp-wave ripples are important for memory storage. Here the authors show that inhibitory neurons activated before sharp-wave ripples regulate the orders of spikes during sharp-wave ripples.
- Asako Noguchi
- , Roman Huszár
- & Yuji Ikegaya
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Article
| Open AccessNeuronal activity in sensory cortex predicts the specificity of learning in mice
The neural mechanisms underpinning the specificity of fear memories remains poorly understood. Here, the authors highlight how neural activity prior to fear learning impacts fear memory specificity.
- Katherine C. Wood
- , Christopher F. Angeloni
- & Maria N. Geffen
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Article
| Open AccessAcetylcholine deficiency disrupts extratelencephalic projection neurons in the prefrontal cortex in a mouse model of Alzheimer’s disease
Short-term memory deficits are associated with prefrontal cortex dysfunction in Alzheimer’s disease. Here, the authors assessed extratelencephalic projection (ET) neurons and found reduced ET neural activity in the medial prefrontal cortex (mPFC) and showed ET neurons received fewer cholinergic inputs from the basal forebrain in 5×FAD mice which led to object recognition memory deficits.
- Qingtao Sun
- , Jianping Zhang
- & Qingming Luo
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Article
| Open AccessBrain-wide visual habituation networks in wild type and fmr1 zebrafish
Habituation is a process in which animals stop responding to repetitive stimuli, and habituation is altered in autism and other conditions. Here, the authors describe visual habituation networks across the zebrafish brain, and find that fmr1 mutants show slower brain-wide and behavioural habituation.
- Emmanuel Marquez-Legorreta
- , Lena Constantin
- & Ethan K. Scott
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Article
| 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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Article
| Open AccessHippocampal ensembles represent sequential relationships among an extended sequence of nonspatial events
It remains unclear how hippocampal activity supports the temporal organization of our experiences. In this paper, the authors recorded from rats performing an odor sequence task and show that hippocampal ensembles represent the sequential relations among nonspatial events at different timescales.
- Babak Shahbaba
- , Lingge Li
- & Norbert J. Fortin
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| Open AccessEvent boundaries shape temporal organization of memory by resetting temporal context
Our memory is temporally organized, but our internal clock can be distorted. The authors demonstrate how environmental changes (termed event boundaries) affect memory for event order, and provide a computational model to explain these effects.
- Yi Pu
- , Xiang-Zhen Kong
- & Lucia Melloni
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| Open AccessA neural circuit linking learning and sleep in Drosophila long-term memory
Learning enhances sleep across species. The authors identify a neural circuit in Drosophila that mediates the learning-induced sleep and ensures that only long or more intense learning experiences are consolidated to long-term memory.
- Zhengchang Lei
- , Kristin Henderson
- & Krystyna Keleman
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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