scholarly journals Phencyclidine discoordinates hippocampal network activity but not place fields

2017 ◽  
Author(s):  
Hsin-Yi Kao ◽  
Dino Dvořák ◽  
EunHye Park ◽  
Jana Kenney ◽  
Eduard Kelemen ◽  
...  
Keyword(s):  
Cognitive Impairment ◽  
Spatial Cognition ◽  
Local Field ◽  
Gamma Oscillations ◽  
Place Cell ◽  
Place Cells ◽  
Spatial Knowledge ◽  
Network Activity ◽  
Cognitive Behavior ◽  
Place Fields

ABSTRACTWe used the psychotomimetic phencyclidine (PCP) to investigate the relationships between cognitive behavior, coordinated neural network function and information processing within the hippocampus place cell system. We report in rats that PCP (5mg/kg i.p.) impairs a well-learned hippocampus-dependent place avoidance behavior in rats that requires cognitive control, even when PCP is injected directly into dorsal hippocampus. PCP increases 60-100 Hz medium gamma oscillations in hippocampus CA1 and these increases correlate with the cognitive impairment caused by systemic PCP administration. PCP discoordinates theta-modulated medium and slow gamma oscillations in CA1 local field potentials (LFP) such that medium gamma oscillations become more theta-organized than slow gamma oscillations. CA1 place cell firing fields are preserved under PCP but the drug discoordinates the sub-second temporal organization of discharge amongst place cells. This discoordination causes place cell ensemble representations of a familiar space to cease resembling pre-PCP representations, despite preserved place fields. These findings point to the cognitive impairments caused by PCP arising from neural discoordination. PCP disrupts the timing of discharge with respect to the sub-second timescales of theta and gamma oscillations in the LFP. Because these oscillations arise from local inhibitory synaptic activity, these findings point to excitation-inhibition discoordination as the root of PCP-induced cognitive impairment.SIGNIFICANCE STATEMENTHippocampal neural discharge is temporally coordinated on timescales of theta and gamma oscillations in the local field potential, and the discharge of a subset of pyramidal neurons called “place cells” is spatially organized such that discharge is restricted to locations called a cell’s “place field.” Because this temporal coordination and spatial discharge organization is thought to represent spatial knowledge, we used the psychotomimetic phencyclidine (PCP) to disrupt cognitive behavior and assess the importance of neural coordination and place fields for spatial cognition. PCP impaired the judicious use of spatial information and discoordinated hippocampal discharge, without disrupting firing fields. These findings dissociate place fields from spatial cognitive behavior and suggest that hippocampus discharge coordination is crucial to spatial cognition.

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.

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 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 Coordinated learning of grid cell and place cell spatial and temporal properties: multiple scales, attention and oscillations

2014 ◽  
Vol 369 (1635) ◽  
pp. 20120524 ◽  
Author(s):  
Stephen Grossberg ◽  
Praveen K. Pilly
Keyword(s):  
Entorhinal Cortex ◽  
Multiple Scales ◽  
Spatial Scales ◽  
Grid Cell ◽  
Neural Model ◽  
Gamma Oscillations ◽  
Place Cell ◽  
Place Cells ◽  
Grid Cells ◽  
Map Learning

A neural model proposes how entorhinal grid cells and hippocampal place cells may develop as spatial categories in a hierarchy of self-organizing maps (SOMs). The model responds to realistic rat navigational trajectories by learning both grid cells with hexagonal grid firing fields of multiple spatial scales, and place cells with one or more firing fields, that match neurophysiological data about their development in juvenile rats. Both grid and place cells can develop by detecting, learning and remembering the most frequent and energetic co-occurrences of their inputs. The model's parsimonious properties include: similar ring attractor mechanisms process linear and angular path integration inputs that drive map learning; the same SOM mechanisms can learn grid cell and place cell receptive fields; and the learning of the dorsoventral organization of multiple spatial scale modules through medial entorhinal cortex to hippocampus (HC) may use mechanisms homologous to those for temporal learning through lateral entorhinal cortex to HC (‘neural relativity’). The model clarifies how top-down HC-to-entorhinal attentional mechanisms may stabilize map learning, simulates how hippocampal inactivation may disrupt grid cells, and explains data about theta, beta and gamma oscillations. The article also compares the three main types of grid cell models in the light of recent data.

scholarly journals A neuronal code for space in hippocampal coactivity dynamics independent of place fields

2021 ◽  
Author(s):  
Eliott R J Levy ◽  
Eun Hye Park ◽  
William T Redman ◽  
André A Fenton
Keyword(s):  
Action Potentials ◽  
Place Cell ◽  
Place Cells ◽  
Neural Code ◽  
Cell Pair ◽  
Environmental Space ◽  
Place Fields ◽  
Cell Firing ◽  
Neuronal Code ◽  
Ensemble Activity

Hippocampus CA1 place cells express a spatial neural code by discharging action potentials in cell-specific locations (′place fields′), but their discharge timing is also coordinated by multiple mechanisms, suggesting an alternative ′ensemble cofiring′ neural code, potentially distinct from place fields. We compare the importance of these distinct information representation schemes for encoding environments. Using miniature microscopes, we recorded the ensemble activity of mouse CA1 principal neurons expressing GCaMP6f across a multi-week experience of two distinct environments. We find that both place fields and ensemble coactivity relationships are similarly reliable within environments and distinctive between environments. Decoding the environment from cell-pair coactivity relationships is effective and improves after removing cell-specific place tuning. Ensemble decoding relies most crucially on anti-coactive cell pairs distributed across CA1 and is independent of place cell firing fields. We conclude that ensemble cofiring relationships constitute an advantageous neural code for environmental space, independent of place fields.

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 A computational grid-to-place-cell transformation model indicates a synaptic driver of place cell impairment in early-stage Alzheimer’s Disease

2021 ◽  
Vol 17 (6) ◽  
pp. e1009115
Author(s):  
Natalie Ness ◽  
Simon R. Schultz
Keyword(s):  
Alzheimer’S Disease ◽  
Alzheimer's Disease ◽  
Cognitive Impairment ◽  
Cell Transformation ◽  
Pyramidal Cells ◽  
Place Cell ◽  
Transformation Model ◽  
Synaptic Dysfunction ◽  
Place Fields ◽  
Environmental Representation

Alzheimer’s Disease (AD) is characterized by progressive neurodegeneration and cognitive impairment. Synaptic dysfunction is an established early symptom, which correlates strongly with cognitive decline, and is hypothesised to mediate the diverse neuronal network abnormalities observed in AD. However, how synaptic dysfunction contributes to network pathology and cognitive impairment in AD remains elusive. Here, we present a grid-cell-to-place-cell transformation model of long-term CA1 place cell dynamics to interrogate the effect of synaptic loss on network function and environmental representation. Synapse loss modelled after experimental observations in the APP/PS1 mouse model was found to induce firing rate alterations and place cell abnormalities that have previously been observed in AD mouse models, including enlarged place fields and lower across-session stability of place fields. Our results support the hypothesis that synaptic dysfunction underlies cognitive deficits, and demonstrate how impaired environmental representation may arise in the early stages of AD. We further propose that dysfunction of excitatory and inhibitory inputs to CA1 pyramidal cells may cause distinct impairments in place cell function, namely reduced stability and place map resolution.

scholarly journals Coordinated emergence of hippocampal replay and theta sequences during post-natal development

2018 ◽  
Author(s):  
Laurenz Muessig ◽  
Michal Lasek ◽  
Isabella Varsavsky ◽  
Francesca Cacucci ◽  
Thomas J Wills
Keyword(s):  
Cell Activity ◽  
Place Cell ◽  
Place Cells ◽  
Network Activity ◽  
Recent Experience ◽  
Sequence Generation ◽  
Late Emergence ◽  
Current Location ◽  
Cell Firing ◽  
Dependent Learning

Hippocampal place cells encode an animal's current position in space during exploration. During subsequent sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial firing fields during locomotion show a greater tendency to co-fire ("reactivation") and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated ("replay"). Reactivation and replay are thought to be network mechanisms underlying memory consolidation. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signalling positions behind to those signalling positions ahead of an animal's current location. These "theta sequences" have been linked to spatial planning. Here we demonstrate that, before weaning (post-natal day 21, P21), offline place cell activity reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration ("theta sequences") and subsequent sleep ("replay"), emerge gradually after weaning in a coordinated fashion, possibly due to a protracted decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals, appearing around weaning in rats and slowly maturing thereafter. In contrast, spatially localised firing can be observed at least one week earlier (albeit with reduced spatial tuning/stability). By examining the emergence of hippocampal reactivation, replay, and theta sequences during development, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.

scholarly journals Interplay between somatic and dendritic inhibition promotes the emergence and stabilization of place fields

2018 ◽  
Author(s):  
Victor Pedrosa ◽  
Claudia Clopath
Keyword(s):  
Firing Rate ◽  
Place Cell ◽  
Place Cells ◽  
Place Field ◽  
Ca1 Neurons ◽  
Hippocampal Ca1 ◽  
Place Fields ◽  
Cell Stability ◽  
Cell Firing ◽  
Novel Environments

AbstractDuring exploration of novel environments, place fields are rapidly formed in hippocampal CA1 neurons. Place cell firing rate increases in early stages of exploration of novel environments but returns to baseline levels in familiar environments. However, although similar in amplitude and width, place fields in familiar environments are more stable than in novel environments. We propose a computational model of the hippocampal CA1 network, which describes the formation, the dynamics and the stabilization of place fields. We show that although somatic disinhibition is sufficient to form place cells, dendritic inhibition along with synaptic plasticity is necessary for stabilization. Our model suggests that place cell stability is due to large excitatory synaptic weights and large dendritic inhibition. We show that the interplay between somatic and dendritic inhibition balances the increased excitatory weights, so that place cells return to their baseline firing rate after exploration. Our model suggests that different types of interneurons are essential to unravel the mechanisms underlying place field plasticity. Finally, we predict that artificial induced dendritic events can shift place fields even after place field stabilization.

Sign in / Sign up

Export Citation Format

Share Document