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Ventral tegmental area dopamine projections to the hippocampus trigger long-term potentiation and contextual learning
How the hippocampus selects relevant events that are worth remembering is debated. Here, authors show midbrain dopamine neurons projecting to the hippocampus provide a teaching signal triggering NeoHebbian LTP and contextual learning.
- Fares J. P. Sayegh
- , Lionel Mouledous
- & Lionel Dahan
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| Open Access
Spontaneous persistent activity and inactivity in vivo reveals differential cortico-entorhinal functional connectivity
Cortico-entorhinal interactions remain poorly understood. Here, the authors demonstrate that a model of interacting networks predicts spontaneous persistent activity and inactivity in the medial, but not lateral, entorhinal cortex in vivo.
- Krishna Choudhary
- , Sven Berberich
- & Mayank R. Mehta
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| Open Access
Intracellular magnesium optimizes transmission efficiency and plasticity of hippocampal synapses by reconfiguring their connectivity
How synapses at dendrites are organized to optimize information processing remains elusive. Here, the authors found that intracellular magnesium optimizes transmission, plasticity, and coding capacity of synapses by reconfiguring their connectivity at dendrites.
- Hang Zhou
- , Guo-Qiang Bi
- & Guosong Liu
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Article
| Open Access
A 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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| Open Access
Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations
Current approaches possibly cannot unambiguously distinguish the unique contributions of feedback inhibition versus feedforward inhibition to oscillatory events. Here authors show that a loss of CA1 pyramidal cell transmission, resulting in feedback inhibition reduction, leads to spatially triggered high-frequency oscillatory events; these events were like place cells in their spatial extent and localized to small regions in CA1.
- Chinnakkaruppan Adaikkan
- , Justin Joseph
- & Thomas J. McHugh
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| Open Access
Activity-dependent compartmentalization of dendritic mitochondria morphology through local regulation of fusion-fission balance in neurons in vivo
The mechanisms regulating mitochondrial architecture in neurons remain unclear. The authors report that in dendrites, mitochondria structure is specified by the CAMKK2-AMPK pathway through compartment-specific and activity-dependent levels of fission.
- Daniel M. Virga
- , Stevie Hamilton
- & Tommy L. Lewis Jr
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| Open Access
Gamma oscillatory complexity conveys behavioral information in hippocampal networks
Specific gamma frequency oscillations are supposed to differentially route information within the hippocampal formation. Here, the authors show that while hippocampal gamma oscillations are more diverse than previously reported, this variability is modulated by behavior and learning.
- Vincent Douchamps
- , Matteo di Volo
- & Romain Goutagny
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| Open Access
T-DOpE probes reveal sensitivity of hippocampal oscillations to cannabinoids in behaving mice
Neural activity is regulated by synapse-neuromodulator interactions, necessitating optoelectro-pharmacological investigations. Here, authors implement their multi-modal probe to show focal infusion of synthetic cannabinoid disrupts CA1 oscillations.
- Jongwoon Kim
- , Hengji Huang
- & Xiaoting Jia
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| Open Access
Environment 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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| Open Access
A developmental increase of inhibition promotes the emergence of hippocampal ripples
The developmental trajectory of hippocampal ripples, the electrical signature of long term memory storage, is poorly understood. Here, the authors show that their delayed appearance is mechanistically linked to the maturation of inhibition.
- Irina Pochinok
- , Tristan M. Stöber
- & Ileana L. Hanganu-Opatz
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Article
| Open Access
Subfield-specific interneuron circuits govern the hippocampal response to novelty in male mice
Hippocampal GABAergic neurons are thought to play a role in processing memories. Here, the authors show that functions of parvalbumin and somatostatin expressing interneurons in mice depend on novelty and differ between hippocampal subfields.
- Thomas Hainmueller
- , Aurore Cazala
- & Marlene Bartos
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Article
| Open Access
Latent representations in hippocampal network model co-evolve with behavioral exploration of task structure
How mechanisms of single-cell plasticity lead to task-dependent cognitive maps remains unclear. Here, the authors show that this model of hippocampus shows that cooperation between local plasticity and reinforcement learning of behavior can lead to task-specific latent representations.
- Ian Cone
- & Claudia Clopath
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Article
| Open Access
Distinguishing examples while building concepts in hippocampal and artificial networks
While the hippocampus is well-known to store specific memories, it can also learn common features that are shared across individual memories. Here, the authors show how this ability arises from dual input pathways and how it can inspire better machine learning methods.
- Louis Kang
- & Taro Toyoizumi
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Article
| Open Access
Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval
How brain regions communicate to support the learning and recall of rich memories is not fully understood. Using recordings of electrical activity deep within the brains of human patients, the authors discovered a role for the theta rhythm in allowing this bidirectional dialogue across brain regions to happen.
- Sandra Gattas
- , Myra Sarai Larson
- & Michael A. Yassa
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| Open Access
The role of experience in prioritizing hippocampal replay
While memory consolidation involves repeated reactivation of past memory traces, it is not fully understood how the brain prioritizes memories for long-term storage during sleep. Here the authors recorded from hippocampal place cells in rats, and find that a novel experience with a longer duration is prioritized for consolidation.
- Marta Huelin Gorriz
- , Masahiro Takigawa
- & Daniel Bendor
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| Open Access
Cortical 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 Access
Hippocampal 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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| Open Access
Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus
How fearful events are represented in the hippocampus remains unclear. Here, the authors describe aversive stimulus-triggered single neuron and population responses as well as alterations of the spatial code in the dorsal hippocampal CA1 region.
- Albert M. Barth
- , Marta Jelitai
- & Viktor Varga
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| Open Access
A 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 Access
Dynamic 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 Access
Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear
The thalamic nucleus reuniens coordinates oscillations between the hippocampus and medial prefrontal cortex during emotional memory retrieval. Here the authors show that theta-paced optogenetic stimulation of this network can suppress the retrieval of aversive memories and prevent fear relapse after extinction.
- Michael S. Totty
- , Tuğçe Tuna
- & Stephen Maren
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| Open Access
Neurofunctional underpinnings of individual differences in visual episodic memory performance
The neural basis of individual differences in episodic memory performance is not well understood. Here, the authors show in a large fMRI dataset that activity of the hippocampus, orbitofrontal cortex and posterior cingulate cortex accounts for individual variability in memory performance.
- Léonie Geissmann
- , David Coynel
- & Dominique J. F. de Quervain
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| Open Access
Acetylcholine modulates the temporal dynamics of human theta oscillations during memory
Memory loss is a known result of cholinergic dysfunction, yet the neural basis for this effect remains unknown. Here, the authors demonstrate that the way cholinergic blockade disrupts memory is by impairing the amplitude and timing of theta oscillations.
- Tamara Gedankien
- , Ryan Joseph Tan
- & Bradley Lega
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| Open Access
Backbone spiking sequence as a basis for preplay, replay, and default states in human cortex
Sequential neural spiking activity is a potential substrate for learning and memory across species. Here, the authors showed spiking in the human cortex forms an average backbone sequence, and flexibility around this backbone is associated with cognition.
- Alex P. Vaz
- , John H. Wittig Jr.
- & Kareem A. Zaghloul
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| Open Access
Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice
The ability to recognize an individual and retrieve related information is crucial for social animals. Here, the authors employ a new social recognition paradigm to show that dorsal CA1 neurons distinguish individual mice and encode associated reward information.
- Eunji Kong
- , Kyu-Hee Lee
- & Doyun Lee
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| Open Access
Single-neuron mechanisms of neural adaptation in the human temporal lobe
Behavioural adaptation from semantic priming is accompanied by reduced neural activity in bulk-tissue measurements, but the underlying single neuron mechanisms remain unclear. Here, the authors leverage simultaneous intracranial EEG and single neuron spiking recordings in the human medial temporal lobe to unveil differential sharpening and fatiguing mechanisms across different temporal lobe areas.
- Thomas P. Reber
- , Sina Mackay
- & Florian Mormann
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| Open Access
Cross-stage neural pattern similarity in the hippocampus predicts false memory derived from post-event inaccurate information
The neural processes underlying the misinformation effect, where post-event information can alter memory, are not well understood. Here, the authors show that during the memory test phase, misinformation competes with original information in the hippocampus to produce false memory.
- Xuhao Shao
- , Ao Li
- & Bi Zhu
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| Open Access
Flexible reuse of cortico-hippocampal representations during encoding and recall of naturalistic events
How the brain builds memories from the complex, dynamic experiences that make up everyday life remains poorly understood. Here, the authors show that memories for lifelike events are supported by stable representations of people, contexts, and situations that can be flexibly recombined into unique, specific instances.
- Zachariah M. Reagh
- & Charan Ranganath
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| Open Access
Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes
How temporal coordination of neurons in the hippocampus contributes to memory function is not well understood. Here the authors show that abolishing hippocampal theta oscillations lead to impaired working and episodic memory while leaving spatiotemporal codes intact.
- Guillaume Etter
- , Suzanne van der Veldt
- & Sylvain Williams
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| Open Access
Hippocampus as a sorter and reverberatory integrator of sensory inputs
How the hippocampus sorts and integrates multiple sensory inputs during learning remains unclear. Here, the authors found that the hippocampus uses reverberatory activity to link conditioned and unconditioned stimuli and to avoid crosstalk during sensory inputs.
- Masanori Nomoto
- , Emi Murayama
- & Kaoru Inokuchi
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| Open Access
Neural circuit dynamics of drug-context associative learning in the mouse hippocampus
Drug-associated contexts are a strong trigger for relapse to substance use. Here, the authors report that a subpopulation of neurons in the hippocampus of mice specifically encode drug-associated contextual information.
- Yanjun Sun
- & Lisa M. Giocomo
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| Open Access
Hippocampal convergence during anticipatory midbrain activation promotes subsequent memory formation
Motivational states play a key role in memory formation. Here, the authors show that curiosity engages reward circuitry to promote a hippocampal state conducive to the formation of new memories.
- Jia-Hou Poh
- , Mai-Anh T. Vu
- & R. Alison Adcock
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| Open Access
Reward 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 Access
Aversive 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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Article
| Open Access
ΔFosB 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 Access
Hemisphere-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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| Open Access
Flexibility 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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| Open Access
Behaviourally 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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| Open Access
Schemas 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 Access
Reactivating 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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| Open Access
Noise 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 Access
A 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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Article
| Open Access
Sex-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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Article
| Open Access
Hippocampal 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 Access
The 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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Article
| Open Access
Angular 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 Access
Acquiring 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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Article
| Open Access
De 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 Access
Hippocampal 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
Hippocampal sharp-wave ripples correlate with periods of naturally occurring self-generated thoughts in humans