@article{14656, abstract = {Although much is known about how single neurons in the hippocampus represent an animal's position, how circuit interactions contribute to spatial coding is less well understood. Using a novel statistical estimator and theoretical modeling, both developed in the framework of maximum entropy models, we reveal highly structured CA1 cell-cell interactions in male rats during open field exploration. The statistics of these interactions depend on whether the animal is in a familiar or novel environment. In both conditions the circuit interactions optimize the encoding of spatial information, but for regimes that differ in the informativeness of their spatial inputs. This structure facilitates linear decodability, making the information easy to read out by downstream circuits. Overall, our findings suggest that the efficient coding hypothesis is not only applicable to individual neuron properties in the sensory periphery, but also to neural interactions in the central brain.}, author = {Nardin, Michele and Csicsvari, Jozsef L and Tkačik, Gašper and Savin, Cristina}, issn = {1529-2401}, journal = {The Journal of Neuroscience}, number = {48}, pages = {8140--8156}, publisher = {Society of Neuroscience}, title = {{The structure of hippocampal CA1 interactions optimizes spatial coding across experience}}, doi = {10.1523/JNEUROSCI.0194-23.2023}, volume = {43}, year = {2023}, } @unpublished{10077, abstract = {Although much is known about how single neurons in the hippocampus represent an animal’s position, how cell-cell interactions contribute to spatial coding remains poorly understood. Using a novel statistical estimator and theoretical modeling, both developed in the framework of maximum entropy models, we reveal highly structured cell-to-cell interactions whose statistics depend on familiar vs. novel environment. In both conditions the circuit interactions optimize the encoding of spatial information, but for regimes that differ in the signal-to-noise ratio of their spatial inputs. Moreover, the topology of the interactions facilitates linear decodability, making the information easy to read out by downstream circuits. These findings suggest that the efficient coding hypothesis is not applicable only to individual neuron properties in the sensory periphery, but also to neural interactions in the central brain.}, author = {Nardin, Michele and Csicsvari, Jozsef L and Tkačik, Gašper and Savin, Cristina}, booktitle = {bioRxiv}, publisher = {Cold Spring Harbor Laboratory}, title = {{The structure of hippocampal CA1 interactions optimizes spatial coding across experience}}, doi = {10.1101/2021.09.28.460602}, year = {2021}, } @article{7684, author = {Gridchyn, Igor and Schönenberger, Philipp and O'Neill, Joseph and Csicsvari, Jozsef L}, issn = {10974199}, journal = {Neuron}, number = {2}, pages = {291--300.e6}, publisher = {Elsevier}, title = {{Assembly-specific disruption of hippocampal replay leads to selective memory deficit}}, doi = {10.1016/j.neuron.2020.01.021}, volume = {106}, year = {2020}, } @article{5828, abstract = {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.}, author = {Xu, Haibing and Baracskay, Peter and O'Neill, Joseph and Csicsvari, Jozsef L}, issn = {10974199}, journal = {Neuron}, number = {1}, pages = {119--132.e4}, publisher = {Elsevier}, title = {{Assembly responses of hippocampal CA1 place cells predict learned behavior in goal-directed spatial tasks on the radial eight-arm maze}}, doi = {10.1016/j.neuron.2018.11.015}, volume = {101}, year = {2019}, } @article{6194, abstract = {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.}, author = {Boccara, Charlotte N. and Nardin, Michele and Stella, Federico and O'Neill, Joseph and Csicsvari, Jozsef L}, issn = {1095-9203}, journal = {Science}, number = {6434}, pages = {1443--1447}, publisher = {American Association for the Advancement of Science}, title = {{The entorhinal cognitive map is attracted to goals}}, doi = {10.1126/science.aav4837}, volume = {363}, year = {2019}, } @article{6338, abstract = {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.}, author = {Stella, Federico and Baracskay, Peter and O'Neill, Joseph and Csicsvari, Jozsef L}, journal = {Neuron}, pages = {450--461}, publisher = {Elsevier}, title = {{Hippocampal reactivation of random trajectories resembling Brownian diffusion}}, doi = {10.1016/j.neuron.2019.01.052}, volume = {102}, year = {2019}, } @article{1132, abstract = {The hippocampus is thought to initiate systems-wide mnemonic processes through the reactivation of previously acquired spatial and episodic memory traces, which can recruit the entorhinal cortex as a first stage of memory redistribution to other brain areas. Hippocampal reactivation occurs during sharp wave-ripples, in which synchronous network firing encodes sequences of places.We investigated the coordination of this replay by recording assembly activity simultaneously in the CA1 region of the hippocampus and superficial layers of the medial entorhinal cortex. We found that entorhinal cell assemblies can replay trajectories independently of the hippocampus and sharp wave-ripples. This suggests that the hippocampus is not the sole initiator of spatial and episodic memory trace reactivation. Memory systems involved in these processes may include nonhierarchical, parallel components.}, author = {O'Neill, Joseph and Boccara, Charlotte and Stella, Federico and Schönenberger, Philipp and Csicsvari, Jozsef L}, issn = {00368075}, journal = {Science}, number = {6321}, pages = {184 -- 188}, publisher = {American Association for the Advancement of Science}, title = {{Superficial layers of the medial entorhinal cortex replay independently of the hippocampus}}, doi = {10.1126/science.aag2787}, volume = {355}, year = {2017}, } @article{1334, abstract = {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.}, author = {Schönenberger, Philipp and O'Neill, Joseph and Csicsvari, Jozsef L}, journal = {Nature Communications}, publisher = {Nature Publishing Group}, title = {{Activity dependent plasticity of hippocampal place maps}}, doi = {10.1038/ncomms11824}, volume = {7}, year = {2016}, } @article{1279, abstract = {During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory inputdriven neuronal firing patterns are replayed. Such replay is thought to be important for plasticity- related processes and consolidation of memory traces. It has previously been shown that the electrical stimulation-induced disruption of SWR events interferes with learning in rodents in different experimental paradigms. On the other hand, the cognitive map theory posits that the plastic changes of the firing of hippocampal place cells constitute the electrophysiological counterpart of the spatial learning, observable at the behavioral level. Therefore, we tested whether intact SWR events occurring during the sleep/rest session after the first exploration of a novel environment are needed for the stabilization of the CA1 code, which process requires plasticity. We found that the newly-formed representation in the CA1 has the same level of stability with optogenetic SWR blockade as with a control manipulation that delivered the same amount of light into the brain. Therefore our results suggest that at least in the case of passive exploratory behavior, SWR-related plasticity is dispensable for the stability of CA1 ensembles.}, author = {Kovács, Krisztián and O'Neill, Joseph and Schönenberger, Philipp and Penttonen, Markku and Rangel Guerrero, Dámaris K and Csicsvari, Jozsef L}, journal = {PLoS One}, number = {10}, publisher = {Public Library of Science}, title = {{Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus}}, doi = {10.1371/journal.pone.0164675}, volume = {11}, year = {2016}, } @article{2860, abstract = {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.}, author = {Dupret, David and O'Neill, Joseph and Csicsvari, Jozsef L}, journal = {Neuron}, number = {1}, pages = {166 -- 180}, publisher = {Elsevier}, title = {{Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning}}, doi = {10.1016/j.neuron.2013.01.033}, volume = {78}, year = {2013}, } @article{2958, abstract = {The activity of hippocampal pyramidal cells reflects both the current position of the animal and information related to its current behavior. Here we investigated whether single hippocampal neurons can encode several independent features defining trials during a memory task. We also tested whether task-related information is represented by partial remapping of the place cell population or, instead, via firing rate modulation of spatially stable place cells. To address these two questions, the activity of hippocampal neurons was recorded in rats performing a conditional discrimination task on a modified T-maze in which the identity of a food reward guided behavior. When the rat was on the central arm of the maze, the firing rate of pyramidal cells changed depending on two independent factors: (1) the identity of the food reward given to the animal and (2) the previous location of the animal on the maze. Importantly, some pyramidal cells encoded information relative to both factors. This trial-type specific and retrospective coding did not interfere with the spatial representation of the maze: hippocampal cells had stable place fields and their theta-phase precession profiles were unaltered during the task, indicating that trial-related information was encoded via rate remapping. During error trials, encoding of both trial-related information and spatial location was impaired. Finally, we found that pyramidal cells also encode trial-related information via rate remapping during the continuous version of the rewarded alternation task without delays. These results suggest that hippocampal neurons can encode several task-related cognitive aspects via rate remapping.}, author = {Allen, Kevin and Rawlins, J Nick and Bannerman, David and Csicsvari, Jozsef L}, journal = {Journal of Neuroscience}, number = {42}, pages = {14752 -- 14766}, publisher = {Society for Neuroscience}, title = {{Hippocampal place cells can encode multiple trial-dependent features through rate remapping}}, doi = {10.1523/JNEUROSCI.6175-11.2012}, volume = {32}, year = {2012}, }