scholarly journals Distinct place cell dynamics in CA1 and CA3 encode experience in new environments

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Can Dong ◽  
Antoine D. Madar ◽  
Mark E. J. Sheffield
Keyword(s):  
Spatial Memory ◽  
Virtual Environments ◽  
Calcium Imaging ◽  
Place Cell ◽  
Place Cells ◽  
Spatial Representations ◽  
Cell Dynamics ◽  
Memory Processing ◽  
Place Fields ◽  
Spatial Memories

AbstractWhen exploring new environments animals form spatial memories that are updated with experience and retrieved upon re-exposure to the same environment. The hippocampus is thought to support these memory processes, but how this is achieved by different subnetworks such as CA1 and CA3 remains unclear. To understand how hippocampal spatial representations emerge and evolve during familiarization, we performed 2-photon calcium imaging in mice running in new virtual environments and compared the trial-to-trial dynamics of place cells in CA1 and CA3 over days. We find that place fields in CA1 emerge rapidly but tend to shift backwards from trial-to-trial and remap upon re-exposure to the environment a day later. In contrast, place fields in CA3 emerge gradually but show more stable trial-to-trial and day-to-day dynamics. These results reflect different roles in CA1 and CA3 in spatial memory processing during familiarization to new environments and constrain the potential mechanisms that support them.

scholarly journals Changing reward expectation transforms spatial encoding and retrieval in the hippocampus

2020 ◽  
Author(s):  
Seetha Krishnan ◽  
Chery Cherian ◽  
Mark. E. J. Sheffield
Keyword(s):  
Spatial Memory ◽  
Spatial Information ◽  
Place Cell ◽  
Cellular Level ◽  
Place Cells ◽  
Cell Dynamics ◽  
Spatial Encoding ◽  
Internal States ◽  
Spatial Memories ◽  
Encoding And Retrieval

SummaryInternal states of reward expectation play a central role in influencing the strength of spatial memories. At the cellular level, spatial memories are represented through the firing dynamics of hippocampal place cells. However, it remains unclear how internal states of reward expectation influence place cell dynamics and exert their effects on spatial memories. Here we show that when reward expectation is altered, the same environment becomes encoded by a distinct ensemble of place cells at all locations. Further, when reward expectation is high versus low, place cells demonstrate enhanced reliability during navigation and greater stability across days at all locations within the environment. These findings reveal that when rewards are expected, neuromodulatory circuits that represent internal reward expectation support and strengthen the encoding and retrieval of spatial information by place cells at all locations that lead to reward. This enhanced spatial memory can be used to guide future decisions about which locations are most likely to lead to rewards that are crucial for survival.

scholarly journals Distinct place cell dynamics in CA1 and CA3 encode experience in new contexts

2020 ◽  
Author(s):  
Can Dong ◽  
Mark E. J. Sheffield
Keyword(s):  
Place Cell ◽  
Place Cells ◽  
Cell Dynamics ◽  
Place Fields ◽  
Distinct Features

AbstractWe compared trial-by-trial dynamics of place cells in CA1 and CA3 in new contexts across days. We found that CA1 place fields form early but shift backwards with experience and partially remap across days. In contrast, CA3 place fields develop gradually but remain stable with experience and across days. This suggests distinct plasticity mechanisms drive the formation and dynamics of place fields in CA1 and CA3 to encode distinct features of experience.n

scholarly journals On how the dentate gyrus contributes to memory discrimination

2017 ◽  
Author(s):  
Milenna T. van Dijk ◽  
Andre A. Fenton
Keyword(s):  
Dentate Gyrus ◽  
Pattern Discrimination ◽  
Place Cell ◽  
Place Cells ◽  
Inhibitory Neurons ◽  
List Type ◽  
Principal Cells ◽  
Cell Network ◽  
Place Fields ◽  
Spatial Memories

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

scholarly journals Offline Memory Reactivation Promotes the Consolidation Of Spatially Unbiased Long-Term Cognitive Maps

2020 ◽  
Author(s):  
Andres D. Grosmark ◽  
Fraser T. Sparks ◽  
Matt J. Davis ◽  
Attila Losonczy
Keyword(s):  
Memory Consolidation ◽  
Calcium Imaging ◽  
Cognitive Maps ◽  
Place Cells ◽  
Reward Learning ◽  
Spatial Representations ◽  
Learning Behavior ◽  
Spatial Memories ◽  
Distinct Role

Spatial memories which can last a lifetime are thought to be encoded during ‘online’ periods of exploration and subsequently consolidated into stable cognitive maps through their ‘offline’ reactivation1–5. However, the mechanisms and computational principles by which offline reactivation stabilize long-lasting spatial representations remain poorly understood. Here we employed simultaneous fast calcium imaging and electrophysiology to track hippocampal place cells over weeks of online spatial reward learning behavior and offline resting. We describe that recruitment to persistent network-level offline reactivation of spatial experiences predicts cells’ future multi-day representational stability. Moreover, while representations of reward-adjacent locations are generally more stable across days, reactivation-related stabilization is, conversely, most prominent for reward-distal locations. Thus, while occurring on millisecond time-scales, offline reactivation counter-balances the observed multi-day representational reward-adjacency bias, promoting the stabilization of cognitive maps which comprehensively reflect entire underlying spatial contexts. These findings suggest that post-learning offline-related memory consolidation plays complimentary and computationally distinct role in learning as compared to online encoding.

Hippocampal Place-Cell Firing During Movement in Three-Dimensional Space

2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton
Keyword(s):  
Hippocampal Neurons ◽  
Horizontal Plane ◽  
Three Dimensional ◽  
Place Cell ◽  
Place Cells ◽  
Limbic Cortex ◽  
Head Direction ◽  
Head Direction Cells ◽  
Recording Apparatus ◽  
Place Fields

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.

scholarly journals Altered hippocampal place cell representation and theta rhythmicity following moderate prenatal alcohol exposure

2020 ◽  
Author(s):  
Ryan E. Harvey ◽  
Laura E. Berkowitz ◽  
Daniel D. Savage ◽  
Derek A. Hamilton ◽  
Benjamin J. Clark
Keyword(s):  
Spatial Memory ◽  
Prenatal Alcohol Exposure ◽  
Alcohol Exposure ◽  
Place Cell ◽  
Place Cells ◽  
Spatial Tuning ◽  
Cell Firing ◽  
Prenatal Alcohol ◽  
Ca3 Neurons ◽  
Hippocampal Place Cell

SummaryPrenatal alcohol exposure (PAE) leads to profound deficits in spatial memory and synaptic and cellular alterations to the hippocampus that last into adulthood. Neurons in the hippocampus, called place cells, discharge as an animal enters specific places in an environment, establish distinct ensemble codes for familiar and novel places, and are modulated by local theta rhythms. Spatial memory is thought to critically depend on the integrity of hippocampal place cell firing. We therefore tested the hypothesis that hippocampal place cell firing is impaired after PAE by performing in-vivo recordings from the hippocampi (CA1 and CA3) of moderate PAE and control adult rats. Our results show that hippocampal CA3 neurons from PAE rats have reduced spatial tuning. Secondly, CA1 and CA3 neurons from PAE rats are less likely to orthogonalize their firing between directions of travel on a linear track and between contexts in an open arena compared to control neurons. Lastly, reductions in the number of hippocampal place cells exhibiting significant theta rhythmicity and phase precession were observed which may suggest changes to hippocampal microcircuit function. Together, the reduced spatial tuning and sensitivity to context provides a neural systems-level mechanism to explain spatial memory impairment after moderate PAE.

scholarly journals Scopolamine Impairs Spatial Information Recorded With “Miniscope” Calcium Imaging in Hippocampal Place Cells

2021 ◽  
Vol 15 ◽  
Author(s):  
Dechuan Sun ◽  
Ranjith Rajasekharan Unnithan ◽  
Chris French
Keyword(s):  
Spatial Memory ◽  
Calcium Imaging ◽  
Memory Retrieval ◽  
Spatial Information ◽  
Place Cells ◽  
Network Activity ◽  
Memory Encoding ◽  
Neural Firing ◽  
Neural Ensemble ◽  
Hippocampal Network

The hippocampus and associated cholinergic inputs have important roles in spatial memory in rodents. Muscarinic acetylcholine receptors (mAChRs) are involved in the communication of cholinergic signals and regulate spatial memory. They have been found to impact the memory encoding process, but the effect on memory retrieval is controversial. Previous studies report that scopolamine (a non-selective antagonist of mAChR) induces cognitive deficits on animals, resulting in impaired memory encoding, but the effect on memory retrieval is less certain. We tested the effects of blocking mAChRs on hippocampal network activity and neural ensembles that had previously encoded spatial information. The activity of hundreds of neurons in mouse hippocampal CA1 was recorded using calcium imaging with a miniaturised fluorescent microscope and properties of place cells and neuronal ensemble behaviour in a linear track environment were observed. We found that the decoding accuracy and the stability of spatial representation revealed by hippocampal neural ensemble were significantly reduced after the administration of scopolamine. Several other parameters, including neural firing rate, total number of active neurons, place cell number and spatial information content were affected. Similar results were also observed in a simulated hippocampal network model. This study enhances the understanding of the function of mAChRs on spatial memory impairment.

scholarly journals Differences in reward biased spatial representations in the lateral septum and hippocampus

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hannah S Wirtshafter ◽  
Matthew A Wilson
Keyword(s):  
Spatial Information ◽  
Place Cells ◽  
Lateral Septum ◽  
Field Size ◽  
Spatial Representations ◽  
Navigation Task ◽  
Place Fields ◽  
Cross Correlations

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.

scholarly journals Reconceiving the hippocampal map as a topological template

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Yuri Dabaghian ◽  
Vicky L Brandt ◽  
Loren M Frank
Keyword(s):  
Computational Model ◽  
Spatial Cognition ◽  
Cell Activity ◽  
Place Cell ◽  
Higher Order ◽  
Place Cells ◽  
Wide Range ◽  
New Directions ◽  
Place Fields

The role of the hippocampus in spatial cognition is incontrovertible yet controversial. Place cells, initially thought to be location-specifiers, turn out to respond promiscuously to a wide range of stimuli. Here we test the idea, which we have recently demonstrated in a computational model, that the hippocampal place cells may ultimately be interested in a space's topological qualities (its connectivity) more than its geometry (distances and angles); such higher-order functioning would be more consistent with other known hippocampal functions. We recorded place cell activity in rats exploring morphing linear tracks that allowed us to dissociate the geometry of the track from its topology. The resulting place fields preserved the relative sequence of places visited along the track but did not vary with the metrical features of the track or the direction of the rat's movement. These results suggest a reinterpretation of previous studies and new directions for future experiments.

scholarly journals Impaired spatial memory codes in a mouse model of Rett syndrome

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Sara E Kee ◽  
Xiang Mou ◽  
Huda Y Zoghbi ◽  
Daoyun Ji
Keyword(s):  
Mouse Model ◽  
Spatial Memory ◽  
Rett Syndrome ◽  
Spatial Information ◽  
Memory Deficits ◽  
Place Cells ◽  
Long Time ◽  
Spatial Memories ◽  
Memory Codes

The Mecp2+/- mouse model recapitulates many phenotypes of patients with Rett syndrome (RTT), including learning and memory deficits. It is unknown, however, how the disease state alters memory circuit functions in vivo in RTT mice. Here we recorded from hippocampal place cells, which are thought to encode spatial memories, in freely moving RTT mice and littermate controls. We found that place cells in RTT mice are impaired in their experience-dependent increase of spatial information. This impairment is accompanied by an enhanced baseline firing synchrony of place cells within ripple oscillations during rest, which consequently occludes the increase in synchrony after a novel experience. Behaviorally, contextual memory is normal at short but not long time scale in RTT mice. Our results suggest that hypersynchrony interferes with memory consolidation and leads to impaired spatial memory codes in RTT mice, providing a possible circuit mechanism for memory deficits in Rett Syndrome.

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