scholarly journals Discrete Place Fields of Hippocampal Formation Interneurons

2007 ◽  
Vol 97 (6) ◽  
pp. 4152-4161 ◽  
Author(s):  
W. Bryan Wilent ◽  
Douglas A. Nitz

The spike discharge of hippocampal excitatory principal cells, also called “place cells,” is highly location specific, but the discharge of local inhibitory interneurons is thought to display relatively low spatial specificity. Whereas in other brain regions, such as sensory neocortex, the activity of interneurons is often exquisitely stimulus selective and directly determines the responses of neighboring excitatory neurons, the activity of hippocampal interneurons typically lacks the requisite specificity needed to shape the defined structure of principal cell fields. Here we show that hippocampal formation interneurons have “on” fields (abrupt increases in activity) and “off” fields (abrupt decreases in activity) that are associated with the same location-specific informational content, spatial resolution, and dependency on context as the “place fields” of CA1 principal cells. This establishes that interneurons have well-defined place fields, thus having important implications for understanding how the hippocampus represents spatial information.

2018 ◽  
Vol 119 (2) ◽  
pp. 476-489 ◽  
Author(s):  
Brian J. Gereke ◽  
Alexandra J. Mably ◽  
Laura Lee Colgin

CA1 place cells become more anticipatory with experience, an effect thought to be caused by NMDA receptor-dependent plasticity in the CA3–CA1 network. Theta (~5–12 Hz), slow gamma (~25–50 Hz), and fast gamma (~50–100 Hz) rhythms are thought to route spatial information in the hippocampal formation and to coordinate place cell ensembles. Yet, it is unknown whether these rhythms exhibit experience-dependent changes concurrent with those observed in place cells. Slow gamma rhythms are thought to indicate inputs from CA3 to CA1, and such inputs are thought to be strengthened with experience. Thus, we hypothesized that slow gamma rhythms would become more evident with experience. We tested this hypothesis using mice freely traversing a familiar circular track for three 10-min sessions per day. We found that slow gamma amplitude was reduced in the early minutes of the first session of each day, even though both theta and fast gamma amplitudes were elevated during this same period. However, in the first minutes of the second and third sessions of each day, all three rhythms were elevated. Interestingly, theta was elevated to a greater degree in the first minutes of the first session than in the first minutes of later sessions. Additionally, all three rhythms were strongly influenced by running speed in dynamic ways, with the influence of running speed on theta and slow gamma changing over time within and across sessions. These results raise the possibility that experience-dependent changes in hippocampal rhythms relate to changes in place cell activity that emerge with experience. NEW & NOTEWORTHY We show that CA1 theta, slow gamma, and fast gamma rhythms exhibit characteristic changes over time within sessions in familiar environments. These effects in familiar environments evolve across repeated sessions.


2020 ◽  
Author(s):  
Mary Ann Go ◽  
Jake Rogers ◽  
Giuseppe P. Gava ◽  
Catherine Davey ◽  
Seigfred Prado ◽  
...  

ABSTRACTThe hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of a track floating on air, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells with place fields remapping when animals entered a different environment. When animals re-entered the same environment, place fields typically remapped over a time period of multiple days, faster than in freely moving preparations, but comparable with virtual reality. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.


Author(s):  
Mary Ann Go ◽  
Jake Rogers ◽  
Giuseppe P. Gava ◽  
Catherine E. Davey ◽  
Seigfred Prado ◽  
...  

The hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of an air-floating track with proximal cues, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells despite the absence of distal visual cues. Place fields remapped when animals entered a different environment. When animals re-entered the same environment, place fields typically remapped over a time period of multiple days, faster than in freely moving preparations, but comparable with virtual reality. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hannah S Wirtshafter ◽  
Matthew A Wilson

The lateral septum (LS), which is innervated by the hippocampus, is known to represent spatial information. However, the details of place representation in the LS, and whether this place information is combined with reward signaling, remains unknown. We simultaneously recorded from rat CA1 and caudodorsal lateral septum in rat during a rewarded navigation task and compared spatial firing in the two areas. While LS place cells are less numerous than in hippocampus, they are similar to the hippocampus in field size and number of fields per cell, but with field shape and center distributions that are more skewed toward reward. Spike cross-correlations between the hippocampus and LS are greatest for cells that have reward-proximate place fields, suggesting a role for the LS in relaying task-relevant hippocampal spatial information to downstream areas, such as the VTA.


1998 ◽  
Vol 353 (1373) ◽  
pp. 1333-1340 ◽  
Author(s):  
John O'Keefe ◽  
Neil Burgess ◽  
James G. Donnett ◽  
Kathryn J. Jeffery ◽  
Eleanor A. Maguire

The hippocampal formation in both rats and humans is involved in spatial navigation. In the rat, cells coding for places, directions, and speed of movement have been recorded from the hippocampus proper and/or the neighbouring subicular complex. Place fields of a group of the hippocampal pyramidal cells cover the surface of an environment but do not appear to do so in any systematic fashion. That is, there is no topographical relation between the anatomical location of the cells within the hippocampus and the place fields of these cells in an environment. Recent work shows that place cells are responding to the summation of two or more Gaussian curves, each of which is fixed at a given distance to two or more walls in the environment. The walls themselves are probably identified by their allocentric direction relative to the rat and this information may be provided by the head direction cells. The right human hippocampus retains its role in spatial mapping as demonstrated by its activation during accurate navigation in imagined and virtual reality environments. In addition, it may have taken on wider memory functions, perhaps by the incorporation of a linear time tag which allows for the storage of the times of visits to particular locations. This extended system would serve as the basis for a spatio–temporal event or episodic memory system.


2017 ◽  
Author(s):  
Milenna T. van Dijk ◽  
Andre A. Fenton

SummaryThe dentate gyrus (DG) is crucial for behaviorally discriminating similar spatial memories, predicting that dentate gyrus place cells change (“remap”) spatial tuning (“place fields”) for memory discrimination. This prediction was never tested, although DG place cells remap across similar environments without memory tasks. We confirm this prior finding, then demonstrate that DG place fields do not remap across spatial tasks that require DG-dependent memory discrimination. Instead of remapping, place-discriminating discharge is observed transiently amongst DG place cells, particularly where memory discrimination is most necessary. The DG network signals memory discrimination by expressing distinctive sub-second network patterns of co-firing amongst principal cells at memory discrimination sites. This is accompanied by increased coupling of discharge from excitatory principal cells and inhibitory interneurons. Instead of remapping, these findings identify that memory discrimination is signaled by sub-second patterns of correlated discharge within the dentate network.eTOC blurbvan Dijk and Fenton report that dentate gyrus place cells signal memory discrimination not by remapping, but by variable sub-second patterns of coordinated place cell network discharge and enhanced discharge coupling between excitatory and inhibitory neurons, at sites of memory discrimination.HighlightsDentate gyrus-dependent memory discrimination does not require place cell remappingDentate neural correlates of pattern discrimination are transient, lasting secondsSub-second dentate network discharge correlations signal memory discriminationDentate excitatory-inhibitory coupling is increased at memory discrimination sites


2019 ◽  
Author(s):  
Mauro M. Monsalve-Mercado ◽  
Yasser Roudi

AbstractPhase precessing place cells encode spatial information on fine timescales via the timing of their spikes. This phase code has been extensively studied on linear tracks and for short runs in the open field. However, less is known about the phase code on unconstrained trajectories lasting tens of minutes, typical of open field foraging. In previous work (Monsalve-Mercado and Leibold, 2017), an analytic expression was derived for the spike-time cross-correlation between phase precessing place cells during natural foraging in the open field. This expression makes two predictions on how this phase code differs from the linear track case: cross-correlations are symmetric with respect to time, and they represent the distance between pairs of place fields in that the theta-filtered cross-correlations around zero time-lag are positive for cells with nearby fields while they are negative for those with fields further apart. Here we analyze several available open field recordings and show that these predictions hold for pairs of CA1 place cells. We also show that the relationship remains during remapping in CA1, and it is also present in place cells in area CA3. For CA1 place cells of Fmr1-null mice, which exhibit normal place fields but somewhat weaker temporal coordination with respect to theta compared to wild type, the cross-correlations still remain symmetric but the relationship to place field overlap is largely lost. The relationship discussed here describes how spatial information is communicated by place cells to downstream areas in a finer theta-timescale, relevant for learning and memory formation in behavioural tasks lasting tens of minutes in the open field.


2019 ◽  
Vol 10 (1) ◽  
Author(s):  
G. Torromino ◽  
L. Autore ◽  
V. Khalil ◽  
V. Mastrorilli ◽  
M. Griguoli ◽  
...  

AbstractThe hippocampal formation is considered essential for spatial navigation. In particular, subicular projections have been suggested to carry spatial information from the hippocampus to the ventral striatum. However, possible cross-structural communication between these two brain regions in memory formation has thus far been unknown. By selectively silencing the subiculum–ventral striatum pathway we found that its activity after learning is crucial for spatial memory consolidation and learning-induced plasticity. These results provide new insight into the neural circuits underlying memory consolidation and establish a critical role for off-line cross-regional communication between hippocampus and ventral striatum to promote the storage of complex information.


2017 ◽  
Author(s):  
Bryan C. Souza ◽  
Rodrigo Pavão ◽  
Hindiael Belchior ◽  
Adriano B.L. Tort

AbstractThe hippocampal formation is involved in navigation, and its neuronal activity exhibits a variety of spatial correlates (e.g., place cells, grid cells). The quantification of the information encoded by spikes has been standard procedure to identify which cells have spatial correlates. For place cells, most of the established metrics derive from Shannon’s mutual information (Shannon, 1948), and convey information rate in bits/sec or bits/spike (Skaggs et al., 1993; Skaggs et al., 1996). Despite their widespread use, the performance of these metrics in relation to the original mutual information metric has never been investigated. In this work, using simulated and real data, we find that the current information metrics correlate less with the accuracy of spatial decoding than the original mutual information metric. We also find that the top informative cells may differ among metrics, and show a surrogate-based normalization that yields comparable spatial information estimates. Since different information metrics may identify different neuronal populations, we discuss current and alternative definitions of spatially informative cells, which affect the metric choice.


2021 ◽  
Author(s):  
Ayaka Bota ◽  
Akihiro Goto ◽  
Suzune Tsukamoto ◽  
Alexander Schmidt ◽  
Fred Wolf ◽  
...  

In the brain, spatial information is represented by neurons that fire when an animal is at specific locations, including place cells in hippocampus and grid cells in entorhinal cortex. But how this information is processed in downstream brain regions still remains elusive. Using chronic Ca2+ imaging, we examined the activity of neurons in anterior cingulate cortex (ACC), a brain region implicated in memory consolidation, and found neurons that fire in a manner consistent with the properties of place cells. While the ACC place cells showed stability, location and context specificity similar to the hippocampal counterparts, they also have unique properties. Unlike hippocampal place cells that immediately formed upon exposure to a novel environment, ACC place cells increased over days. Also, ACC place cells tend to have additional place fields whereas typical hippocampal place cells have only one. Hippocampal activity is required for the formation of ACC place cells, but once they are established, hippocampal inactivation did not have any impact on ACC place cell firing. We thus identified features of ACC place cells that carry spatial information in a unique fashion.


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