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| Open AccessA hippocampus-accumbens code guides goal-directed appetitive behavior
The dorsal hippocampus plays an important role for spatial memory, but how its outputs guide behavior is not fully understood. Here, the authors show that nucleus accumbens-specific hippocampal projection neurons carry a highly conjunctive code of spatial and action information that directs spatial reward memory-guided appetitive behaviors.
- Oliver Barnstedt
- , Petra Mocellin
- & Stefan Remy
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Article
| Open AccessA consistent map in the medial entorhinal cortex supports spatial memory
The medial entorhinal cortex (MEC) is hypothesized to function as a cognitive map for memory-guided navigation. Here, the authors demonstrate that the establishment of a spatially consistent MEC map across learning correlates with, and is necessary for, successful spatial memory.
- Taylor J. Malone
- , Nai-Wen Tien
- & Yi Gu
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| Open AccessEnvironment geometry alters subiculum boundary vector cell receptive fields in adulthood and early development
How neural responses to boundaries develop in the subiculum remains unknown. Here authors show that the receptive fields of Boundary Vector Cells (neurons signalling vector displacement to boundaries) are altered by environment geometry, with directional tunings aligning with square arena walls, including during development.
- Laurenz Muessig
- , Fabio Ribeiro Rodrigues
- & Thomas J. Wills
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Article
| Open AccessCortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue
The mechanisms of episodic memory are not well understood. Here, the authors show that the reactivation of non-spatial information precedes the reactivation of spatial information, and that both are correlated with hippocampal sharp-wave ripples.
- HaoRan Chang
- , Ingrid M. Esteves
- & Bruce L. McNaughton
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| Open AccessHippocampal firing fields anchored to a moving object predict homing direction during path-integration-based behavior
The hippocampus contributes to path integration, but the firing patterns supporting this function are unknown. Here, the authors found that the activity of hippocampal neurons during a path integration task predicted the animal’s homing direction.
- Maryam Najafian Jazi
- , Adrian Tymorek
- & Kevin Allen
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Article
| Open AccessStriatum-projecting prefrontal cortex neurons support working memory maintenance
Lesions of dorsomedial, but not dorsolateral, striatum are associated with working memory impairments. Here, the authors investigate the role of a projection from medial prefrontal cortex to dorsomedial striatum in the maintenance of information during a working memory task in mice.
- Maria Wilhelm
- , Yaroslav Sych
- & Fritjof Helmchen
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Article
| Open AccessA thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination
The role of the Nucleus Reuniens (NR)-CA1 pathway in contextual fear conditioning remains unknown. Here, the authors show that the NR-CA1 pathway transmits a signal that actively suppresses fear memory retrieval in CA1 during fearful behavior.
- Heather C. Ratigan
- , Seetha Krishnan
- & Mark E. J. Sheffield
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| Open AccessDynamic neural representations of memory and space during human ambulatory navigation
Here the authors show in freely moving human participants that deep brain oscillations in the medial temporal lobe flexibly encode both memory and spatial information, depending on the current cognitive task demands.
- Sabrina L. L. Maoz
- , Matthias Stangl
- & Nanthia Suthana
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| Open AccessMapping the spatial transcriptomic signature of the hippocampus during memory consolidation
Transcriptional events are critical for hippocampus-dependent long-term memory storage. Here, the authors utilize spatial transcriptomics to elucidate localized gene expression patterns across hippocampal subregions during memory consolidation.
- Yann Vanrobaeys
- , Utsav Mukherjee
- & Snehajyoti Chatterjee
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Article
| Open AccessAn astrocytic signaling loop for frequency-dependent control of dendritic integration and spatial learning
How glial cells like astrocytes shape complex brain functions remains unclear. Here, the authors identified an astrocyte-mediated excitatory signaling loop between neurons and their own dendritic signal integration that supports spatial memory.
- Kirsten Bohmbach
- , Nicola Masala
- & Christian Henneberger
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| Open AccessReward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal
How expectations of reward influence spatial memories remains unclear. Here, the authors reveal a dopamine pathway to the hippocampus that increases activity with proximity to expected rewards, thus stabilizing spatial representations of trajectories that lead to rewards.
- Seetha Krishnan
- , Chad Heer
- & Mark E. J. Sheffield
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Article
| 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 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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| 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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Article
| 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 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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Article
| 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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Article
| 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 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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Article
| 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 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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Article
| Open AccessBNIP3L/NIX-mediated mitophagy protects against glucocorticoid-induced synapse defects
Stress-induced glucocorticoids cause mitochondrial damage in neurons, but they are not cleared by mitophagy. Here, the authors show that glucocorticoids inhibit NIX-dependent basal mitophagy, contributing to neurodegeneration in a mouse model that can be reversed by pretreatment with a NIX enhancer.
- Gee Euhn Choi
- , Hyun Jik Lee
- & Ho Jae Han
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Article
| Open AccessPerineuronal nets stabilize the grid cell network
Perineuronal nets may stabilize synaptic connections. Here, the authors show that removal of perineuronal nets disrupts both the temporal and spatial organization of grid cell firing.
- Ane Charlotte Christensen
- , Kristian Kinden Lensjø
- & Torkel Hafting
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| Open AccessLTD is involved in the formation and maintenance of rat hippocampal CA1 place-cell fields
LTP and LTD are involved in shaping hippocampal place field representations. Here, the authors show that de novo pathway-specific hippocampal LTD changes dynamics and stability of newly formed place fields, regulating acquisition and maintenance of novel spatial information in adult rats.
- Donovan M. Ashby
- , Stan B. Floresco
- & Yu Tian Wang
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Article
| Open AccessGrid cells are modulated by local head direction
Neurons with grid firing fields are thought to play important roles in spatial cognition. Here, the authors show that in contrast to assumptions underlying current models and analyses, grid fields are modulated by local head direction; this suggests different mechanisms and new roles for grid firing.
- Klara Gerlei
- , Jessica Passlack
- & Matthew F. Nolan
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| Open AccessBehavior-dependent directional tuning in the human visual-navigation network
Our brain derives a sense of direction from visual inputs. Here, the authors combine 7T-fMRI with predictive modeling of virtual navigation to show that the strength, width and topology of directional coding in the human brain reflect ongoing memory-guided behavior.
- Matthias Nau
- , Tobias Navarro Schröder
- & Christian F. Doeller
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Article
| Open AccessDG–CA3 circuitry mediates hippocampal representations of latent information
Keinath et al. show that information about the recent past is represented in the hippocampus through changes in firing rates in the absence of task demands. This representation is eliminated when DG–CA3 circuitry is inhibited.
- Alexandra T. Keinath
- , Andrés Nieto-Posadas
- & Mark P. Brandon
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Article
| Open AccessSources of path integration error in young and aging humans
Path integration abilities, important for spatial navigation, vary widely across individuals and deteriorate in old age. This work shows that path integration errors in general, as well as age-related path integration deficits, are mainly caused by accumulating noise in people’s velocity estimation.
- Matthias Stangl
- , Ingmar Kanitscheider
- & Thomas Wolbers
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| Open AccessPrecise coupling of the thalamic head-direction system to hippocampal ripples
Thalamic head direction (HD) cells are necessary to establish spatial maps in the hippocampus. Here, the authors show that HD cells tuned to a particular direction are coupled to individual hippocampal ripple events during sleep, suggesting an influence of the replay of specific trajectories during sleep memory consolidation.
- Guillaume Viejo
- & Adrien Peyrache
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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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| 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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| 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
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Article
| Open AccessA human memory circuit derived from brain lesions causing amnesia
Memory is hypothesised to depend on different brain regions that interact in a network. Here, the authors use case studies of stroke patients with amnesia from the literature to identify brain regions that are part of this network.
- Michael A. Ferguson
- , Chun Lim
- & Michael D. Fox
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Article
| Open AccessLocus coeruleus-CA1 projections are involved in chronic depressive stress-induced hippocampal vulnerability to transient global ischaemia
Depression and transient ischaemic attacks are tightly regulated but the neural circuits underlying depression-modulated ischaemic injury are not known. Here, the authors show that the locus coeruleus-CA1 pathway is involved in depression-associated ischaemia susceptibility.
- Qian Zhang
- , Dian Xing Hu
- & Bo Tian
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Article
| Open AccessNeuronal representation of environmental boundaries in egocentric coordinates
The hippocampus represents an allocentric map of space, however, motor movements used for navigation are defined in an egocentric framework. Here, the authors report that dorsomedial striatal neurons exhibit an egocentric representation of the boundaries in the environment.
- James R. Hinman
- , G. William Chapman
- & Michael E. Hasselmo
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| Open AccessHeading direction with respect to a reference point modulates place-cell activity
Place cells are neurons in the hippocampus which encode an animal’s location in space. Here, in mice, the authors show that place cell activity is also modulated by the heading-direction of the animal relative to a particular “reference point” that can be either within or outside their enclosure.
- P. E. Jercog
- , Y. Ahmadian
- & E. R. Kandel
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Article
| Open AccessPath integration maintains spatial periodicity of grid cell firing in a 1D circular track
In an open field, the preferential firing of grid cells on a hexagonal lattice is formed by integrating external as well as self-motion cues. Here, the authors show that on a 1D circular track, path integration cues shape the spatial selectivity of grid cells while external cues determine the scale of the grid.
- Pierre-Yves Jacob
- , Fabrizio Capitano
- & Francesca Sargolini
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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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Article
| 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 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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| Open AccessPerirhinal firing patterns are sustained across large spatial segments of the task environment
Spatial navigation and memory depend on neural coding of an organism’s location as well as large-scale knowledge of the environment, but how animals organize information in task-relevant spatial segments is not well understood. Here the authors show that, in rats, perirhinal neurons perform integrative operations, globally specifying where, in the task context, an animal is located.
- Jeroen J. Bos
- , Martin Vinck
- & Cyriel M. A. Pennartz
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Article
| Open AccessHippocampal and prefrontal processing of network topology to simulate the future
The hippocampus is known to support navigation, but how it processes possible paths to aid navigation is unknown. Here Javadiet al. show that entering streets drives hippocampal activity corresponding to the number of future paths, and that prefrontal activity corresponds to path-planning demands.
- Amir-Homayoun Javadi
- , Beatrix Emo
- & Hugo J. Spiers
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| Open AccessOpposite monosynaptic scaling of BLP–vCA1 inputs governs hopefulness- and helplessness-modulated spatial learning and memory
How emotions affect memory is an open question. Here the authors establish learnt hopeful and learnt helpless mouse models, and find that posterior basolateral amygdala to ventral hippocampal CA1 monosynaptic glutamatergic inputs link emotions to spatial memory performance.
- Ying Yang
- , Zhi-Hao Wang
- & Jian-Zhi Wang
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Article
| Open AccessEarly detection of cryptic memory and glucose uptake deficits in pre-pathological APP mice
Identifying early signs of Alzheimer’s disease is important when it comes to diagnosis and treatment. Here, the authors identify subtle memory retrieval deficits and associated brain glucose uptake impairments in very young mouse models of Alzheimer’s, prior to plaque development.
- V. Beglopoulos
- , J. Tulloch
- & R. G. M. Morris