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| Open AccessFunctionally distinct high and low theta oscillations in the human hippocampus
We show that the human hippocampus exhibits two distinct theta oscillations during spatial navigation with the faster oscillation in posterior regions showing movement modulation. This result suggests a distinct feature of the human hippocampus compared to rodents, which generally show a single 8 Hz rhythm.
- Abhinav Goyal
- , Jonathan Miller
- & Joshua Jacobs
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Article
| Open AccessHDAC1 modulates OGG1-initiated oxidative DNA damage repair in the aging brain and Alzheimer’s disease
Defects in DNA repair have been linked to brain aging and neurodegenerative disorders. Here the authors reveal a role for HDAC1 in stimulating OGG1 activity to alleviate 8-oxoG lesions with implications in the aging brain and neurodegenerative diseases.
- Ping-Chieh Pao
- , Debasis Patnaik
- & Li-Huei Tsai
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Article
| Open AccessTrajectory-modulated hippocampal neurons persist throughout memory-guided navigation
Trajectory-coding neurons in the hippocampus convey important information for performing memory tasks. Here, Kinsky et al. track long-term neural activity in the hippocampus to find that trajectory-coding emerges rapidly and remains stable across long time-scales.
- Nathaniel R. Kinsky
- , William Mau
- & Michael E. Hasselmo
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| Open AccessDynamic reconfiguration of functional brain networks during working memory training
Working memory training reshapes the brain functional network reorganization. Here, the authors demonstrate an increase of the whole-brain network segregation during the n-back task, accompanied by alterations in dynamic communication between the default mode system and task-positive systems.
- Karolina Finc
- , Kamil Bonna
- & Danielle S. Bassett
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Article
| Open AccessNeuromedin U signaling regulates retrieval of learned salt avoidance in a C. elegans gustatory circuit
Learning and memory are regulated by neuropeptides. Here, the authors show that the neuropeptide CAPA-1 and its receptor NMUR-1 are required to retrieve learned salt avoidance in C. elegans. CAPA-1/NMUR-1 activation in AFD sensory neurons modulates locomotor programs to express learned avoidance.
- Jan Watteyne
- , Katleen Peymen
- & Isabel Beets
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Article
| Open AccessPrefrontal reinstatement of contextual task demand is predicted by separable hippocampal patterns
Spatial contexts are often predictive of the tasks to be performed in them (e.g., a kitchen predicts cooking). Here the authors show that the retrieval of task demand when encountering a spatial context depends on hippocampal-prefrontal interactions.
- Jiefeng Jiang
- , Shao-Fang Wang
- & Anthony D. Wagner
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Article
| Open AccessFeature-specific neural reactivation during episodic memory
Memory recollection involves reactivation of neural activity that occurred during the recalled experience. Here, the authors show that neural reactivation can be decomposed into visual-semantic features, is widely synchronized throughout the brain, and predicts memory vividness and accuracy.
- Michael B. Bone
- , Fahad Ahmad
- & Bradley R. Buchsbaum
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| Open AccessPropagation of hippocampal ripples to the neocortex by way of a subiculum-retrosplenial pathway
Communication between the hippocampus and neocortex is organized through high frequency sharp wave ripple activity. Here, the authors report ripple activity coupling between the hippocampus and granular retrosplenial cortex suggesting an involvement in communicating with the neocortex.
- Noam Nitzan
- , Sam McKenzie
- & Dietmar Schmitz
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Article
| Open AccessMouse tracking reveals structure knowledge in the absence of model-based choice
Mouse tracking can reveal people’s subjective beliefs and whether they understand the structure of a task. These data demonstrate that people often do not use this information to make good choices.
- Arkady Konovalov
- & Ian Krajbich
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Article
| Open AccessA gravity-based three-dimensional compass in the mouse brain
Head direction neurons constitute the brain’s compass, and are classically known to indicate head orientation in the horizontal plane. Here, the authors show that head direction neurons form a three-dimensional compass that can also indicate head tilt, and anchors to gravity.
- Dora E. Angelaki
- , Julia Ng
- & Jean Laurens
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Article
| Open AccessPhase-dependent amplification of working memory content and performance
Neuronal patterns during working memory show low-frequency oscillatory activity. Here, the authors demonstrate a rhythmic retention of working memory information in theta and alpha frequency ranges. Moreover, phase-locked amplification of the retained information improves working memory performance.
- Sanne ten Oever
- , Peter De Weerd
- & Alexander T. Sack
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Article
| Open AccessInterplay between midbrain and dorsal anterior cingulate regions arbitrates lingering reward effects on memory encoding
Rewarded stimuli are better encoded in memory. Here, the authors show that the average accumulation of reward over consecutive trials provides an additive, non-linear (inverted U-shape) modulation of memory encoding, paralleled by a similar recruitment of dopaminergic memory circuitry.
- Kristoffer Carl Aberg
- , Emily Elizabeth Kramer
- & Sophie Schwartz
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Article
| Open AccessExcitatory VTA to DH projections provide a valence signal to memory circuits
The neuronal pathway that signals the positive or negative value of memories is not well understood. Here, the authors report that an excitatory projection from the ventral tegmental area to the dorsal hippocampus carries the valence information, contributing, especially in females, to the recurrence of fear and to drug seeking behavior.
- Yuan Han
- , Yi Zhang
- & Jelena Radulovic
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Article
| Open AccessImpact of functional synapse clusters on neuronal response selectivity
The formation of functional synaptic clusters (FSCs) and their impact on somatic membrane potential (sVm) in vivo are poorly understood. Here, the authors develop a computational approach to show that FSCs have to form via local rather than global plasticity and be moderately large to impact sVm.
- Balázs B. Ujfalussy
- & Judit K. Makara
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Article
| Open AccessEncoding of contextual fear memory in hippocampal–amygdala circuit
Previous studies implicate the hippocampal–amygdala pathway in contextual fear conditioning, in which animals learn to associate a neutral context with an aversive stimulus and display fear responses to dangerous situations. Here the authors show that selective strengthening of hippocampal–amygdala pathway contributes to encoding adaptive fear memory for threat-predictive context.
- Woong Bin Kim
- & Jun-Hyeong Cho
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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 AccessOlfactory memory representations are stored in the anterior olfactory nucleus
Odours are powerful stimuli used by most organisms to guide behaviour. Here, the authors identify populations of neurons within the anterior olfactory nucleus (AON) which are necessary and sufficient for the behavioural expression of odour memory.
- Afif J. Aqrabawi
- & Jun Chul Kim
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Article
| Open AccessIntrinsic neuronal properties represent song and error in zebra finch vocal learning
The regulation of cellular neuronal properties distinct from synaptic plasticity has been proposed as a mechanism of functional network organization. Here, the authors show that the magnitude of five ion currents in basal ganglia projection song system forebrain neurons covary across life, rapidly and dynamically relating to learned features of individual zebra finches’ songs.
- Arij Daou
- & Daniel Margoliash
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Article
| Open AccessEarly life experiences selectively mature learning and memory abilities
The mechanisms underlying the maturation of learning and memory abilities are poorly understood. Here, authors show that episodic learning produces persistent neuronal activation, BDNF-dependent increase in excitatory synapse markers (synaptophysin and PSD-95), and significant maturation of AMPA receptor synaptic responses in the hippocampus of infant rats and mice compared to juveniles and adults.
- Benjamin Bessières
- , Alessio Travaglia
- & Cristina M. Alberini
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Article
| Open AccessPersistent activation of central amygdala CRF neurons helps drive the immediate fear extinction deficit
Learned conditioned fear associations can be weakened (extinction learning), but extinction is less effective if performed too soon after the original fear conditioning. Here, the authors show that persistent activation of CRF-expressing neurons in the central amygdala is involved in the early fear extinction deficit.
- Yong S. Jo
- , Vijay Mohan K. Namboodiri
- & Larry S. Zweifel
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| Open AccessIncreasing neurogenesis refines hippocampal activity rejuvenating navigational learning strategies and contextual memory throughout life
Ageing affects several brain areas causing a decrease in cognitive abilities and memory. We find that increasing the endogenous potential of the hippocampus to generate new neurons throughout life rejuvenates learning and memory, indicating that neural reserves can be exploited during ageing to compensate for age- or disease-related cognitive impairments.
- Gabriel Berdugo-Vega
- , Gonzalo Arias-Gil
- & Federico Calegari
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Article
| Open AccessDopamine transients do not act as model-free prediction errors during associative learning
Dopamine neurons are proposed to signal the reward prediction error in model-free reinforcement learning algorithms. Here, the authors show that when given during an associative learning task, optogenetic activation of dopamine neurons causes associative, rather than value, learning.
- Melissa J. Sharpe
- , Hannah M. Batchelor
- & Geoffrey Schoenbaum
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Article
| Open AccessControllability governs the balance between Pavlovian and instrumental action selection
Pavlovian and instrumentally driven actions often conflict when determining the best outcome. Here, the authors present an arbitration theory supported by human behavioral data where Pavlovian predictors drive action selection in an uncontrollable environment, while more flexible instrumental prediction dominates under conditions of high controllability.
- Hayley M. Dorfman
- & Samuel J. Gershman
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| Open AccessHippocampal clock regulates memory retrieval via Dopamine and PKA-induced GluA1 phosphorylation
The neural mechanisms that lead to a relative deficit in memory retrieval in the afternoon are unclear. Here, the authors show that the circadian - dependent transcription factor BMAL1 regulates retrieval through dopamine and glutamate receptor phosphorylation.
- Shunsuke Hasegawa
- , Hotaka Fukushima
- & Satoshi Kida
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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 AccessThe role of prefrontal cortex in the control of feature attention in area V4
The neural mechanisms underlying feature based attention to targets in a cluttered scene are not well understood. Here, the authors show that inactivation of the ventral prearcuate region leads to deficits in picking out a target among many stimuli as well as eliminates the feature based modulation of responses of V4 neurons.
- Narcisse P. Bichot
- , Rui Xu
- & Robert Desimone
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Article
| Open AccessA non-spatial account of place and grid cells based on clustering models of concept learning
Spatial maps in the medial temporal lobe (MTL) have been proposed to map abstract conceptual knowledge. Rather than grounding abstract knowledge in a spatial map, the authors propose a general-purpose clustering algorithm that explains how both spatial (including place and grid cells) and higher-dimensional conceptual representations arise during learning.
- Robert M. Mok
- & Bradley C. Love
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Article
| Open AccessEnsemble representations reveal distinct neural coding of visual working memory
People can easily extract task-relevant gist features from visual scenes and hold those features in working memory. Here, the authors show that this gist information is gradually abstracted from posterior to anterior regions of the brain and stably represented at the anterior region.
- Byung-Il Oh
- , Yee-Joon Kim
- & Min-Suk Kang
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Article
| Open AccessKetamine can reduce harmful drinking by pharmacologically rewriting drinking memories
Memories linking environmental cues to alcohol reward are involved in the development and maintenance of heavy drinking. Here, the authors show that a single dose of ketamine, given after retrieval of alcohol-reward memories, disrupts the reconsolidation of these memories and reduces drinking in humans.
- Ravi K. Das
- , Grace Gale
- & Sunjeev K. Kamboj
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Article
| Open AccessInterference between overlapping memories is predicted by neural states during learning
Interference from overlapping memories can cause forgetting. Here, the authors show using fMRI decoding approaches that spontaneous reactivation of older memories during new encoding leads to integration, and less interference, between overlapping items.
- Avi J. H. Chanales
- , Nicole M. Dudukovic
- & Brice A. Kuhl
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Article
| Open AccessInterplay between α2-chimaerin and Rac1 activity determines dynamic maintenance of long-term memory
Memory consolidation theory suggests that memory is maintained at a stable strength after formation. The authors show that memory is dynamically maintained at an intermediate level allowing a bidirectional regulation which is mediated by a balance between activated Rac1 and expressed α2-chimaerin.
- Li Lv
- , Yunlong Liu
- & Yi Zhong
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Article
| Open AccessOptogenetic gamma stimulation rescues memory impairments in an Alzheimer’s disease mouse model
Slow gamma oscillations are associated with memory and have been reported to be disrupted in patients with Alzheimer’s disease. Here the authors show that optogenetic stimulation of medial septum parvalbumin neurons at 40 Hz rescues memory retrieval in the J20 mouse model of Alzheimer’s disease.
- Guillaume Etter
- , Suzanne van der Veldt
- & Sylvain Williams
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Perspective
| Open AccessEvolving perspectives on the sources of the frequency-following response
The auditory frequency-following response (FFR) indexes the quality of neural sound encoding in the brain. In this Perspective, the authors discuss the potential of the FFR to provide a better understanding of sound encoding in the auditory system and its relationship to behavior.
- Emily B. J. Coffey
- , Trent Nicol
- & Nina Kraus
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Article
| Open AccessUnbalanced dendritic inhibition of CA1 neurons drives spatial-memory deficits in the Ts2Cje Down syndrome model
Exaggerated synaptic inhibition is hypothesised to be a main cause of cognitive deficits in Down syndrome models. The authors identify triplication of the kainate receptor encoding gene Grik1 as the cause of memory deficits due to a reorganization of synaptic inhibition along the CA1 dendritic tree.
- Sergio Valbuena
- , Álvaro García
- & Juan Lerma
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Article
| Open AccessTau deposition is associated with functional isolation of the hippocampus in aging
Deposition of tau protein aggregates occurs during aging and Alzheimer disease. Here, the authors show that tau burden in the anterior-temporal memory network is associated with disrupted fMRI connectivity and functional isolation of the hippocampus from other memory network components.
- Theresa M. Harrison
- , Anne Maass
- & William J. Jagust
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Article
| Open AccessMultiple associative structures created by reinforcement and incidental statistical learning mechanisms
Associative learning occurs through reinforcement mechanisms as well as incidentally through experience of statistical relationships. Here, the authors report that these two learning processes are associated with specialized anatomical regions that operate at different time scales.
- Miriam C. Klein-Flügge
- , Marco K. Wittmann
- & Matthew F. S. Rushworth
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Article
| Open AccessRevealing neural correlates of behavior without behavioral measurements
Neuronal tuning is typically measured in response to a priori defined behavioural variables of interest. Here, the authors use an unsupervised learning approach to recover neuronal tuning with respect to the recorded network activity and show that this can reveal the relevant behavioural variables.
- Alon Rubin
- , Liron Sheintuch
- & Yaniv Ziv
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Article
| Open AccessContributions of anterior cingulate cortex and basolateral amygdala to decision confidence and learning under uncertainty
The degree of subjective confidence in deciding based on ambiguous sensory cues facilitates learning. Here, the authors report distinct functions of the basolateral amygdala and anterior cingulate cortex on implicit confidence judgements as well as flexible learning under uncertain conditions in rats.
- A. Stolyarova
- , M. Rakhshan
- & A. Izquierdo
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Article
| Open AccessThe rostroventral part of the thalamic reticular nucleus modulates fear extinction
The precise role of the thalamic reticular nucleus in fear is not understood. Here, the authors report that the rostroventral part of the reticular nucleus is involved in the extinction of tone conditioned fear memory through its inhibitory projections to the dorsal midline thalamus.
- Joon-Hyuk Lee
- , Charles-Francois V. Latchoumane
- & Hee-Sup Shin
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Article
| Open AccessLong-term memory is formed immediately without the need for protein synthesis-dependent consolidation in Drosophila
New protein synthesis is known to be indispensable for the consolidation of long-term memory. Here, the authors report that an olfactory memory can be successfully recalled after 14 days without protein synthesis when the training context is also provided in addition to the conditioned odor.
- Bohan Zhao
- , Jiameng Sun
- & Yi Zhong
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Article
| Open AccessNMDA receptor-dependent plasticity in the nucleus accumbens connects reward-predictive cues to approach responses
Conditioned stimuli elicit phasic changes in nucleus accumbens (NAc) firing that invigorate approach responses to predicted rewards. Here the authors show that NAc neurons acquire cue-evoked responses during learning as a result of excitatory plasticity within the NAc.
- Mercedes Vega-Villar
- , Jon C. Horvitz
- & Saleem M. Nicola
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Article
| Open AccessDynamic regulation of interregional cortical communication by slow brain oscillations during working memory
Working memory involves a fronto-parietal brain network, but how the parts of this network are coordinated is unclear. Here, the authors show that fast brain activity at posterior sites is nested into prefrontal slow brain waves, with cognitive demand determining the slow wave phase involved.
- B. Berger
- , B. Griesmayr
- & P. Sauseng
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Article
| Open AccessEvidence for allocentric boundary and goal direction information in the human entorhinal cortex and subiculum
In rodents, cells in the medial entorhinal cortex and subiculum are known to encode the allocentric direction to nearby walls and boundaries. Here, using fMRI the authors show that this is also true in humans, with allocentric boundary direction being encoded in posterior entorhinal cortex and subiculum.
- J. P. Shine
- , J. P. Valdés-Herrera
- & T. Wolbers
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Article
| Open AccessHippocampal-neocortical interactions sharpen over time for predictive actions
In familiar environments, humans automatically anticipate the sensory consequences of their motor actions. Here, the authors show how action-based predictions arise from interactions between the hippocampus and visual cortex, and how these interactions strengthen and weaken over time.
- Nicholas C. Hindy
- , Emily W. Avery
- & Nicholas B. Turk-Browne
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Article
| Open AccessZika virus replicates in adult human brain tissue and impairs synapses and memory in mice
Here, using ex-vivo human adult cortical tissue and a mouse model, the authors investigate the functional consequences of Zika virus (ZIKV) infection in the adult brain, and show that ZIKV causes synapse damage and altered brain function that impacts cognition via activation of innate and inflammatory factors.
- Claudia P. Figueiredo
- , Fernanda G. Q. Barros-Aragão
- & Sergio T. Ferreira
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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 AccessAnti-relapse neurons in the infralimbic cortex of rats drive relapse-suppression by drug omission cues
Drug addiction is a chronic disorder and many sufferers experience relapses even after a period of successful abstinence. Here, the authors reveal a subset of neurons in the rat infralimbic cortex that suppresses relapse into cocaine or alcohol use by responding to drug-omission cues.
- Amanda Laque
- , Genna L. De Ness
- & Nobuyoshi Suto
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Article
| Open AccessWilm’s tumor 1 promotes memory flexibility
Impairments in memory flexibility are associated with neuropsychiatric disorders such as PTSD and autism. Here, the authors report that the transcriptional repressor Wilm's Tumor 1 regulates synaptic plasticity leading to weakening of memory strength and enabling memory flexibility.
- Chiara Mariottini
- , Leonardo Munari
- & Ravi Iyengar
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Article
| Open AccessMemory-guided microsaccades
Microsaccades are small-amplitude, fixational eye movements that are largely thought to be involuntary. Here, the authors demonstrate that monkeys (and humans) can be easily trained to respond to a remembered target location with a volitional microsaccade, and that a population of superior colliculus neurons is selectively associated with them.
- Konstantin F. Willeke
- , Xiaoguang Tian
- & Ziad M. Hafed