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| Open AccessHippocampal projections to the anterior olfactory nucleus differentially convey spatiotemporal information during episodic odour memory
Hippocampus is necessary for integrating the context with sensory cues to retrieve memory for unique episodes. Here, the authors show that inhibiting topographically organized projections from hippocampus to the anterior olfactory nucleus independently impairs spatial and temporal odour memory recall.
- Afif J. Aqrabawi
- & Jun Chul Kim
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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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| Open AccessAn effect of serotonergic stimulation on learning rates for rewards apparent after long intertrial intervals
Serotonin (5-HT) plays many important roles in reward, punishment, patience and beyond, and optogenetic stimulation of 5-HT neurons has not crisply parsed them. The authors report a novel analysis of a reward-based decision-making experiment, and show that 5-HT stimulation increases the learning rate, but only on a select subset of choices.
- Kiyohito Iigaya
- , Madalena S. Fonseca
- & Peter Dayan
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| Open AccessLateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation
Theta oscillations are implicated in memory formation. Here, the authors show that low-theta oscillations in the hippocampus are differentially modulated between each hemisphere, with oscillations in the left increasing when successfully learning object–location pairs and in the right during spatial navigation.
- Jonathan Miller
- , Andrew J. Watrous
- & Joshua Jacobs
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| Open AccessFinding influential nodes for integration in brain networks using optimal percolation theory
Complex networks can be used to model brain networks. Here the authors identify the essential nodes in a model of a brain network and then validate these predictions by means of in vivo pharmacogenetic interventions. They find that the nucleus accumbens is a central region for brain integration.
- Gino Del Ferraro
- , Andrea Moreno
- & Hernán A. Makse
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| Open AccessSpecific hippocampal representations are linked to generalized cortical representations in memory
Memory representations in cortex and hippocampus are reactivated during sharp-wave ripple (SWR) events. Here, the authors show that, in a familiar environment, this activity preferentially links spatially selective hippocampal cells and task general PFC representations, pointing to a potential neural mechanism for generalization of individual experiences.
- Jai Y. Yu
- , Daniel F. Liu
- & Loren M. Frank
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| Open AccessAn ensemble code in medial prefrontal cortex links prior events to outcomes during learning
Prefrontal cortex is involved in flexibly learning the correct behavioural strategies but the neural correlates of this process are not well understood. Here the authors show that reinforcement for a correct decision at behavioural transitions evokes ensemble firing patterns related to prior events.
- Silvia Maggi
- , Adrien Peyrache
- & Mark D. Humphries
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| Open AccessEarly deprivation disruption of associative learning is a developmental pathway to depression and social problems
Early childhood deprivation such as institutionalization can greatly affect early development. Here, the authors study children who were raised in institutions but later randomly placed in foster care vs. not, to understand how early-life deprivation affects associative learning in adolescence.
- Margaret A. Sheridan
- , Katie A. McLaughlin
- & Charles A. Nelson
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Article
| Open AccessGut vagal sensory signaling regulates hippocampus function through multi-order pathways
Feeding-relevant vagal signaling occurs between the gastrointestinal tract and the brain, but it is unclear if this pathway influences cognitive processes. This study shows that endogenous gastrointestinal derived vagal sensory signaling promotes hippocampal-dependent memory function via a multi-order brainstem–septal pathway.
- Andrea N. Suarez
- , Ted M. Hsu
- & Scott E. Kanoski
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| Open AccessReward probability and timing uncertainty alter the effect of dorsal raphe serotonin neurons on patience
Activation of serotonin neurons in the dorsal raphe nucleus promotes patience in waiting for future rewards. Here the authors show that this effect is maximal for high probability reward or high temporal reward uncertainty suggesting that it boosts the prior probability of reward.
- Katsuhiko Miyazaki
- , Kayoko W. Miyazaki
- & Kenji Doya
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Article
| Open AccessKnowledge acquisition is governed by striatal prediction errors
Trial and error learning requires the brain to generate expectations and match them to outcomes, yet whether this occurs for semantic learning is unclear. Here, authors show that the brain encodes the degree to which new factual information violates expectations, which in turn determines whether information is encoded in long-term memory.
- Alex Pine
- , Noa Sadeh
- & Avi Mendelsohn
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| Open AccessOlfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior
Nasal airflow and olfactory bulb activity are linked to oscillations in cortical areas. This study shows olfactory input and respiration are correlated with oscillation in the prefrontal cortex during freezing behavior in mice, and attenuation of olfactory inputs can increase behavioral freezing.
- Andrew H. Moberly
- , Mary Schreck
- & Minghong Ma
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Article
| Open AccessPharmacologically induced amnesia for learned fear is time and sleep dependent
Emotional memory can change when retrieved, yet the conditions under which this can occur are not fully described. Here, authors show that taking a pill of propranolol taken during a specific time window can change the expression of fear memory in a person, and that sleep is necessary to forget learned fear.
- Merel Kindt
- & Marieke Soeter
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| Open AccessTime-dependent memory transformation along the hippocampal anterior–posterior axis
Detailed memories are transformed into gist-like memories over time. Here, the authors report that this change is linked to a time-dependent reorganization within the hippocampus, such that anterior activity supporting memory specificity declines over time while posterior activity patterns carrying gist representations remain more stable.
- Lisa C. Dandolo
- & Lars Schwabe
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Article
| Open AccessLinear and inverted U-shaped dose-response functions describe estrogen effects on hippocampal activity in young women
While estrogen is known to change hippocampal activity in animals, it is not known if this effect extends to humans. Here, authors vary the doses of estrogen in young women and show that the effects on hippocampal activity can be described by linear and inverted-U shaped dose-response functions.
- Janine Bayer
- , Jan Gläscher
- & Tobias Sommer
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Article
| Open AccessA neuronal basis for fear discrimination in the lateral amygdala
When perceiving new stimuli, organisms need to distinguish between threats versus harmless stimuli. Here, the authors find a set of cells in the lateral amygdala that is required to discriminate or generalize new auditory stimuli based on similarity to previously fear-associate sounds.
- Anna Grosso
- , Giulia Santoni
- & Benedetto Sacchetti
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| Open AccessInhibitory gain modulation of defense behaviors by zona incerta
Zona incerta (ZI) is an inhibitory subthalamic nucleus with diverse connectivity yet its functional importance has not been extensively studied. Here the authors report that ZI receives mPFC input and can modulate both innate and learned defensive behaviors via its inhibitory projection to the PAG.
- Xiao-lin Chou
- , Xiyue Wang
- & Huizhong Whit Tao
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Article
| Open AccessFunctional architecture of reward learning in mushroom body extrinsic neurons of larval Drosophila
The mushroom body of Drosophila integrates sensory information with past experience to guide behaviour. Here, the authors provide an atlas of the input and output neurons of the stage 3 larval mushroom body at the single-cell level, and analyse their function in learned and innate behaviours.
- Timo Saumweber
- , Astrid Rohwedder
- & Bertram Gerber
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| Open AccessFlexibility in motor timing constrains the topology and dynamics of pattern generator circuits
Human speech and bird song requires the generation of precisely timed motor patterns. The authors show that zebra finches can learn to independently modify the duration of individual song segments and find that synfire chain networks are ideally suited to implement such flexible motor timing.
- Cengiz Pehlevan
- , Farhan Ali
- & Bence P. Ölveczky
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| Open AccessAn olfactory virtual reality system for mice
Odor-guided spatial behaviours are difficult to study due to the challenge of controlling chemical concentrations in space and time. Here the authors present a precise odor delivery system to generate a olfactory virtual landscape that engages hippocampal place cells in mice.
- Brad A. Radvansky
- & Daniel A. Dombeck
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| Open AccessClosed-loop stimulation of temporal cortex rescues functional networks and improves memory
Memory lapses can occur due to ineffective encoding, but it is unclear if targeted brain stimulation can improve memory performance. Here, authors use a closed-loop system to decode and stimulate periods of ineffective encoding, showing that stimulation of lateral temporal cortex can enhance memory.
- Youssef Ezzyat
- , Paul A. Wanda
- & Michael J. Kahana
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| Open AccessHotspots of dendritic spine turnover facilitate clustered spine addition and learning and memory
Structural remodeling of dendritic spines is thought to be a mechanism of memory storage. Here, the authors look at how spine turnover and clustering predict future learning and memory performance, and see that a genetically modified mouse with enhanced spine turnover has enhanced learning.
- Adam C. Frank
- , Shan Huang
- & Alcino J. Silva
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Article
| Open AccessGamma and beta bursts during working memory readout suggest roles in its volitional control
Previously, the authors have shown that working memory can be maintained by brief gamma oscillation bursts. Here, the authors use a new task to further demonstrate the dynamics of gamma and beta oscillations in working memory readout, independent of behavioral response.
- Mikael Lundqvist
- , Pawel Herman
- & Earl K. Miller
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| Open AccessCA1 and CA3 differentially support spontaneous retrieval of episodic contexts within human hippocampal subfields
Computational studies have hinted that hippocampal subfields represent information differently. Here, the authors show that when retrieving items that share an episodic context, subfield CA1 represent similarities between items whereas CA2/3/dentate gyrus represents item-unique features.
- Halle R. Dimsdale-Zucker
- , Maureen Ritchey
- & Charan Ranganath
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| Open AccessChronic alcohol exposure disrupts top-down control over basal ganglia action selection to produce habits
Drug dependence shifts the balance in action selection away from goal-directed to habitual responding. Here, the authors report that chronic passive exposure to alcohol leads to suppression of orbitofrontal cortex inputs to dorsomedial striatum resulting in downregulation of goal-directed behavior.
- Rafael Renteria
- , Emily T. Baltz
- & Christina M. Gremel
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| Open AccessThe interhemispheric CA1 circuit governs rapid generalisation but not fear memory
Previous work has documented a slow form of memory generalization although a rapid one is demanded. Here the authors elucidate the role of the interhemispheric CA1-CA1 projection in a form of rapid generalization of contextual fear memory via gradual potentiation of these synapses over 24 h.
- Heng Zhou
- , Gui-Jing Xiong
- & Lin Xu
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| Open AccessHippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task
Theta- and gamma-frequency oscillatory synchrony correlates with spatial working memory performance. Here the authors report increases in theta-gamma cross-frequency coupling as a compensatory mechism associated with better working memory performance in models of cognitive dysfunction in mice.
- Makoto Tamura
- , Timothy J. Spellman
- & Joshua A. Gordon
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Article
| Open AccessIncreased striatal activity in adolescence benefits learning
Adolescence is associated with negative behaviors that are related to enhanced reward-related striatal activity, but it is unclear whether this activity could also be beneficial. Here, authors report longitudinal data showing that enhanced striatal activity is related with increased learning ability.
- S. Peters
- & E. A. Crone
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| Open AccessVocal learning promotes patterned inhibitory connectivity
Complex motor behaviors such as birdsong are learned through practice and are thought to depend on specific excitatory connectivity in premotor circuits. Here the authors show that song learning in Bengalese Finches is associated with enrichment of inhibitory network connectivity that can affect specific song features.
- Mark N. Miller
- , Chung Yan J. Cheung
- & Michael S. Brainard
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Article
| Open AccessInhibiting Rho kinase promotes goal-directed decision making and blocks habitual responding for cocaine
Action-outcome learning requires the prelimbic prefrontal cortex. Here the authors report that fasudil, a Rho kinase inhibitor, reduces dendritic spine densities on prelimbic neurons in an activity-dependent manner, stimulating goal-directed actions, and reducing habitual responding for cocaine.
- Andrew M. Swanson
- , Lauren M. DePoy
- & Shannon L. Gourley
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Article
| Open AccessIngestion of artificial sweeteners leads to caloric frustration memory in Drosophila
While non-caloric artificial sweeteners (NAS) are used as food additives, it’s unclear whether animals perceive NAS as positive or negative percept. Here, Musso and colleagues show in Drosophila that NAS is a negative percept, encoded in a new type of memory.
- Pierre-Yves Musso
- , Aurélie Lampin-Saint-Amaux
- & Thomas Preat
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| Open AccessChanges in cortical network connectivity with long-term brain-machine interface exposure after chronic amputation
Previous studies have shown short-term plasticity in single neurons or local field potentials during brain-machine interface (BMI) training. Here the authors report long-term changes in functional connectivity of motor cortex neuronal ensemble activity as chronically amputated monkeys learn to operate a BMI.
- Karthikeyan Balasubramanian
- , Mukta Vaidya
- & Nicholas G. Hatsopoulos
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| Open AccessWidespread theta synchrony and high-frequency desynchronization underlies enhanced cognition
Synchronous neural activity is related with memory encoding and retrieval, but it is not clear whether this happens across the whole brain. Here, authors use intracranial recordings to show that gamma networks are largely asynchronous, desynchronizing while theta synchronizes during memory encoding and retrieval.
- E. A. Solomon
- , J. E. Kragel
- & M. J. Kahana
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| Open AccessShort-term reward experience biases inference despite dissociable neural correlates
Making a good decision often requires the weighing of relative short-term rewards against long-term benefits, yet how the brain does this is not understood. Here, authors show that long-term beliefs are biased by reward experience and that dissociable brain regions facilitate both types of learning.
- Adrian G. Fischer
- , Sacha Bourgeois-Gironde
- & Markus Ullsperger
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Article
| Open AccessActivity-dependent expression of Channelrhodopsin at neuronal synapses
Changes to subsets of dendritic spines are thought to be important for memory formation. Here, the authors develop a hybrid RNA/protein tool that allows for optogenetic stimulation of single synapses that have been tagged in an activity-dependent manner
- Francesco Gobbo
- , Laura Marchetti
- & Antonino Cattaneo
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| Open AccessNeuronal hyperactivity due to loss of inhibitory tone in APOE4 mice lacking Alzheimer’s disease-like pathology
The APOE4 allele is the leading risk factor for late-onset Alzheimer’s disease, but how it might contribute to the disease is not clear. Here the authors show that a mouse expressing the human APOE4 allele displays hyperactivity in the entorhinal cortex due to a decreased inhibitory tone, which may in part explain accelerated Alzheimer’s pathology in APOE4 carriers.
- Tal Nuriel
- , Sergio L. Angulo
- & Karen E. Duff
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| Open AccessSupramammillary glutamate neurons are a key node of the arousal system
Supramammillary nucleus (SuM) neurons have been studied in the context of REM sleep but their possible role in mediating wakefulness is not known. Here the authors elucidate the distinct functional contributions of three subpopulations in the SuM on electrographical and behavioral arousal in mice using genetically targeted approaches.
- Nigel P. Pedersen
- , Loris Ferrari
- & Patrick M. Fuller
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| Open AccessNeuronal baseline shifts underlying boundary setting during free recall
Though people are easily able to recall items in a category without mentioning a wrong exemplar, the mechanism underlying this ability is unknown. Here, authors use intracranial recordings to show that this ability is likely due to a selective increase in baseline neuronal activity in category-specific regions.
- Yitzhak Norman
- , Erin M. Yeagle
- & Rafael Malach
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| Open AccessHippocampal GABA enables inhibitory control over unwanted thoughts
It is not fully understood how intrusive or unwanted memories are regulated. Here the authors show that hippocampal GABA concentrations, and coupling between the dorsolateral prefrontal cortex and hippocampus, predict how well subjects can suppress unwanted memories when presented with a reminder.
- Taylor W. Schmitz
- , Marta M. Correia
- & Michael C. Anderson
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| 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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Article
| Open AccessPrior preferences beneficially influence social and non-social learning
People often assume that other people share their preferences, but how exactly this bias manifests itself in learning and decision-making is unclear. Here, authors show that a person's own preferences influence learning in both social and non-social situations, and that this bias improves performance.
- Tor Tarantola
- , Dharshan Kumaran
- & Benedetto De Martino
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Article
| Open AccessCortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents
Different stages of sleep, marked by particular electroencephalographic (EEG) signatures, have been linked to memory consolidation, but underlying mechanisms are poorly understood. Here, the authors show that dendritic calcium synchronisation correlates with spindle-rich sleep phases.
- Julie Seibt
- , Clément J. Richard
- & Matthew E. Larkum
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Article
| Open AccessReinforcement determines the timing dependence of corticostriatal synaptic plasticity in vivo
Spike timing dependent plasticity (STDP) has been studied extensively in slices but whether such pairings can induce plasticity in vivo is not known. Here the authors report an experimental paradigm that achieves bidirectional corticostriatal STDP in vivo through modulation by behaviourally relevant reinforcement signals, mediated by dopamine and adenosine signaling.
- Simon D. Fisher
- , Paul B. Robertson
- & John N.J. Reynolds
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Article
| Open AccessSparse orthogonal population representation of spatial context in the retrosplenial cortex
Neurons in the retrosplenial cortex (RSC) encode spatial and navigational signals. Here the authors use calcium imaging to show that, similar to the hippocampus, RSC neurons also encode place cell-like activity in a sparse orthogonal representation, partially anchored to the allocentric cues on the linear track.
- Dun Mao
- , Steffen Kandler
- & Vincent Bonin
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Article
| Open AccessHIPP neurons in the dentate gyrus mediate the cholinergic modulation of background context memory salience
Intra-hippocampal circuits are essential for associating a background context with behaviorally salient stimuli and involve cholinergic modulation at SST+ interneurons. Here the authors show that the salience of the background context memory is modulated through muscarinic activation of NPY+ hilar perforant path associated interneurons and NPY signaling in the dentate gyrus.
- Syed Ahsan Raza
- , Anne Albrecht
- & Oliver Stork
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Article
| Open AccessAutism-like behaviours and enhanced memory formation and synaptic plasticity in Lrfn2/SALM1-deficient mice
Lrfn2/SALM1 is a synaptic adhesion molecule, and is known to interact with PSD-95. Here the authors show that Lrfn2 regulates excitatory synapse maturation and maintenance, and that Lrfn2 knockout mice exhibit autism-like behaviours as well as enhanced learning and memory.
- Naoko Morimura
- , Hiroki Yasuda
- & Jun Aruga
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Article
| Open AccessRefinement of learned skilled movement representation in motor cortex deep output layer
Motor learning induces structural and functional reorganization in upper layers of motor cortex. Here the authors show that neuronal ensembles in the output layer 5b exhibit temporal dynamics during skilled learning that progressively becomes well-aligned to movement in a dopamine dependent manner.
- Qian Li
- , Ho Ko
- & Wing-Ho Yung
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Article
| Open AccessReactivation of associative structure specific outcome responses during prospective evaluation in reward-based choices
How the brain evaluates options to make a reward-based choice is unclear. Here, authors show that, prior to choice, neural activity patterns to the potential outcomes are reactivated in macaque orbitofrontal cortex, in a way that reflects the unique event sequences leading up to the outcomes.
- Maya Zhe Wang
- & Benjamin Y. Hayden
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Article
| Open AccessNeuronal population coding of perceived and memorized visual features in the lateral prefrontal cortex
Neurons in the lateral prefrontal cortex are known to encode visual features as well as maintain them in working memory. Here the authors report that LPFC neurons encode both perceived and memorized visual features in diverse combinations and the population activity reliably decodes as well as differentiates between these two representations.
- Diego Mendoza-Halliday
- & Julio C. Martinez-Trujillo