The entorhinal cognitive map is attracted to goals Boccara, Charlotte N; Nardin, Michele; Stella, Federico ...
Science (American Association for the Advancement of Science),
03/2019, Volume:
363, Issue:
6434
Journal Article
Peer reviewed
Open access
Grid cells with their rigid hexagonal firing fields are thought to provide an invariant metric to the hippocampal cognitive map, yet environmental geometrical features have recently been shown to ...distort the grid structure. Given that the hippocampal role goes beyond space, we tested the influence of nonspatial information on the grid organization. We trained rats to daily learn three new reward locations on a cheeseboard maze while recording from the medial entorhinal cortex and the hippocampal CA1 region. Many grid fields moved toward goal location, leading to long-lasting deformations of the entorhinal map. Therefore, distortions in the grid structure contribute to goal representation during both learning and recall, which demonstrates that grid cells participate in mnemonic coding and do not merely provide a simple metric of space.
Memory consolidation is thought to depend on the reactivation of waking hippocampal firing patterns during sleep. Following goal learning, the reactivation of place cell firing can represent goals ...and predicts subsequent memory recall. However, it is unclear whether reactivation promotes the recall of the reactivated memories only or triggers wider reorganization. We trained animals to locate goals at fixed locations in two different environments. Following learning, by performing online assembly content decoding, the reactivation of only one environment was disrupted, leading to recall deficit in that environment. The place map of the disrupted environment was destabilized but re-emerged once the goal was relearned. These data demonstrate that sleep reactivation facilitates goal-memory retrieval by strengthening memories that enable the selection of context-specific hippocampal maps. However, sleep reactivation may not be needed for the stabilization of place maps considering that the map of the disrupted environment re-emerged after the retraining of goals.
•Online decoding allows selective disruption of reactivated memory traces•Content-related reactivation disruption in sleep led to specific recall impairment•Disrupted spatial memory representations re-emerge in the same form after relearning•Reactivation may facilitate the selection of correct representation after learning
Gridchyn et al. examine how the content of reactivated sleep activity influences memory recall. By disrupting the reactivation of specific place cell patterns, it shows recall impairment for spatial memories represented by the disrupted patterns, without impacting other, undisrupted memories.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Hippocampal activity patterns representing movement trajectories are reactivated in immobility and sleep periods, a process associated with memory recall, consolidation, and decision making. It is ...thought that only fixed, behaviorally relevant patterns can be reactivated, which are stored across hippocampal synaptic connections. To test whether some generalized rules govern reactivation, we examined trajectory reactivation following non-stereotypical exploration of familiar open-field environments. We found that random trajectories of varying lengths and timescales were reactivated, resembling that of Brownian motion of particles. The animals’ behavioral trajectory did not follow Brownian diffusion demonstrating that the exact behavioral experience is not reactivated. Therefore, hippocampal circuits are able to generate random trajectories of any recently active map by following diffusion dynamics. This ability of hippocampal circuits to generate representations of all behavioral outcome combinations, experienced or not, may underlie a wide variety of hippocampal-dependent cognitive functions such as learning, generalization, and planning.
•Hippocampal replay can represent Brownian diffusion-like random trajectories•Reactivated trajectories cover positions over wide ranges of spatiotemporal scales•Replay event statistics are incompatible with actual behavioral trajectories•Expression dynamics of replayed assemblies was linked to specific oscillatory bands
Stella et al. examine the dynamical properties of reactivated spatial trajectories in the hippocampus following non-stereotypical exploration and find that reactivated trajectories are governed by a Brownian diffusion process that occur at varying lengths and timescales, without directly reflecting behavior.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
The hippocampus is an important brain circuit for spatial memory and the spatially selective spiking of hippocampal neuronal assemblies is thought to provide a mnemonic representation of space. We ...found that remembering newly learnt goal locations required NMDA receptor-dependent stabilization and enhanced reactivation of goal-related hippocampal assemblies. During spatial learning, place-related firing patterns in the CA1, but not CA3, region of the rat hippocampus were reorganized to represent new goal locations. Such reorganization did not occur when goals were marked by visual cues. The stabilization and successful retrieval of these newly acquired CA1 representations of behaviorally relevant places was NMDAR dependent and necessary for subsequent memory retention performance. Goal-related assembly patterns associated with sharp wave/ripple network oscillations, during both learning and subsequent rest periods, predicted memory performance. Together, these results suggest that the reorganization and reactivation of assembly firing patterns in the hippocampus represent the formation and expression of new spatial memory traces.
Full text
Available for:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, UILJ, UKNU, UL, UM, UPUK
Hippocampus is needed for both spatial working and reference memories. Here, using a radial eight-arm maze, we examined how the combined demand on these memories influenced CA1 place cell ...assemblies while reference memories were partially updated. This was contrasted with control tasks requiring only working memory or the update of reference memory. Reference memory update led to the reward-directed place field shifts at newly rewarded arms and to the gradual strengthening of firing in passes between newly rewarded arms but not between those passes that included a familiar-rewarded arm. At the maze center, transient network synchronization periods preferentially replayed trajectories of the next chosen arm in reference memory tasks but the previously visited arm in the working memory task. Hence, reference memory demand was uniquely associated with a gradual, goal novelty-related reorganization of place cell assemblies and with trajectory replay that reflected the animal’s decision of which arm to visit next.
•Place cells gradually move their firing fields toward newly learned rewards•Task-contingent firing is influenced by goal novelty during reference memory update•In reference memory tasks, trajectory replay predicts future arm at decision point•In the pure working memory task, trajectory replay encodes previously visited arm
Xu et al. examine how the combined demand on spatial working and reference memory influences place cell assemblies and find that their gradual reorganization is linked to goal novelty and that their replay at decision points predicts future arm choice.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
In the hippocampus, cell assemblies forming mnemonic representations of space are thought to arise as a result of changes in functional connections of pyramidal cells. We have found that CA1 ...interneuron circuits are also reconfigured during goal-oriented spatial learning through modification of inputs from pyramidal cells. As learning progressed, new pyramidal assemblies expressed in theta cycles alternated with previously established ones, and eventually overtook them. The firing patterns of interneurons developed a relationship to new, learning-related assemblies: some interneurons associated their activity with new pyramidal assemblies while some others dissociated from them. These firing associations were explained by changes in the weight of monosynaptic inputs received by interneurons from new pyramidal assemblies, as these predicted the associational changes. Spatial learning thus engages circuit modifications in the hippocampus that incorporate a redistribution of inhibitory activity that might assist in the segregation of competing pyramidal cell assembly patterns in space and time.
► Interneuron firing reorganizes as pyramidal assemblies flicker during spatial learning ► Interneurons form dynamic firing associations to newly established assemblies ► Changes in pyramidal cell connections to interneurons explain firing associations ► Pyramidal cell-interneuron coupling changes are activity dependent and map specific
Dupret et al. show that CA1 hippocampal interneuron circuits undergo plastic changes during spatial learning, enabling them to develop firing associations with newly established pyramidal cell assemblies. These learning-related circuit modifications may assist in the segregation of competing pyramidal assemblies.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
The execution of cognitive functions requires coordinated circuit activity across different brain areas that involves the associated firing of neuronal assemblies. Here, we tested the circuit ...mechanism behind assembly interactions between the hippocampus and the medial prefrontal cortex (mPFC) of adult rats by recording neuronal populations during a rule-switching task. We identified functionally coupled CA1-mPFC cells that synchronized their activity beyond that expected from common spatial coding or oscillatory firing. When such cell pairs fired together, the mPFC cell strongly phase locked to CA1 theta oscillations and maintained consistent theta firing phases, independent of the theta timing of their CA1 counterpart. These functionally connected CA1-mPFC cells formed interconnected assemblies. While firing together with their CA1 assembly partners, mPFC cells fired along specific theta sequences. Our results suggest that upregulated theta oscillatory firing of mPFC cells can signal transient interactions with specific CA1 assemblies, thus enabling distributed computations.
Display omitted
•mPFC spatial coding lags behind the hippocampus with a behavior-dependent delay•CA1-mPFC cells synchronize independently from common place coding or oscillations•Enhanced mPFC theta phase locking signals interaction with specific CA1 assembles•Interacting CA1-mPFC assemblies can exhibit independent theta sequences
Nardin et al. identify functionally coupled hippocampal CA1-medial prefrontal cortex (mPFC) assemblies. During the synchronized activity of an assembly, mPFC cells enhance their phase locking to CA1 theta oscillations and fire along specific theta sequences. Thus, theta sequential firing of mPFC cells can signal transient interactions with CA1 assembly partners.
Full text
Available for:
GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Hippocampal neurons encode a cognitive map of space. These maps are thought to be updated during learning and in response to changes in the environment through activity-dependent synaptic plasticity. ...Here we examine how changes in activity influence spatial coding in rats using halorhodopsin-mediated, spatially selective optogenetic silencing. Halorhoposin stimulation leads to light-induced suppression in many place cells and interneurons; some place cells increase their firing through disinhibition, whereas some show no effect. We find that place fields of the unaffected subpopulation remain stable. On the other hand, place fields of suppressed place cells were unstable, showing remapping across sessions before and after optogenetic inhibition. Disinhibited place cells had stable maps but sustained an elevated firing rate. These findings suggest that place representation in the hippocampus is constantly governed by activity-dependent processes, and that disinhibition may provide a mechanism for rate remapping.
Sharp wave/ripple (SWR, 150–250 Hz) hippocampal events have long been postulated to be involved in memory consolidation. However, more recent work has investigated SWRs that occur during active ...waking behaviour: findings that suggest that SWRs may also play a role in cell assembly strengthening or spatial working memory. Do such theories of SWR function apply to animal learning? This review discusses how general theories linking SWRs to memory-related function may explain circuit mechanisms related to rodent spatial learning and to the associated stabilization of new cognitive maps.
Full text
Available for:
BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Abstract
The mammalian hippocampal formation (HF) plays a key role in several higher brain functions, such as spatial coding, learning and memory. Its simple circuit architecture is often viewed as a ...trisynaptic loop, processing input originating from the superficial layers of the entorhinal cortex (EC) and sending it back to its deeper layers. Here, we show that excitatory neurons in layer 6b of the mouse EC project to all sub-regions comprising the HF and receive input from the CA1, thalamus and claustrum. Furthermore, their output is characterized by unique slow-decaying excitatory postsynaptic currents capable of driving plateau-like potentials in their postsynaptic targets. Optogenetic inhibition of the EC-6b pathway affects spatial coding in CA1 pyramidal neurons, while cell ablation impairs not only acquisition of new spatial memories, but also degradation of previously acquired ones. Our results provide evidence of a functional role for cortical layer 6b neurons in the adult brain.
PDF
