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.

scholarly journals Critical role of de novo LTD in the formation and maintenance of hippocampal CA1 place-cell fields

2019 ◽  
Author(s):  
Donovan M Ashby ◽  
Jeremy K Seamans ◽  
Yu Tian Wang
Keyword(s):  
Direct Evidence ◽  
De Novo ◽  
Critical Role ◽  
Place Field ◽  
Hippocampal Ca1 ◽  
Place Fields ◽  
Freely Moving ◽  
Novel Environments

AbstractSynaptic plasticity mechanisms may help shape hippocampal place field representations of novel environments, yet direct evidence for how this occurs is lacking. Using multi-channel recordings in freely moving rats, we demonstrate that novelty exploration results in widespread de novo long-term depression (LTD) at hippocampal CA1 synapses in a pathway-specific manner, while blockade of LTD expression impairs the maintenance of newly formed place fields. This study therefore reveals an unrecognized role for LTD in the formation and maintenance of hippocampal place fields in novel environments.

scholarly journals Medial entorhinal cortex lesions induce degradation of CA1 place cell firing stability when self-motion information is used

2020 ◽  
Vol 4 ◽  
pp. 239821282095300
Author(s):  
Pierre-Yves Jacob ◽  
Tiffany Van Cauter ◽  
Bruno Poucet ◽  
Francesca Sargolini ◽  
Etienne Save
Keyword(s):  
Entorhinal Cortex ◽  
Place Cell ◽  
Motion Information ◽  
Baseline Session ◽  
Place Field ◽  
Medial Entorhinal Cortex ◽  
Motion Cues ◽  
Place Fields ◽  
Cell Firing ◽  
Self Motion

The entorhinal–hippocampus network plays a central role in navigation and episodic memory formation. To investigate these interactions, we examined the effect of medial entorhinal cortex lesions on hippocampal place cell activity. Since the medial entorhinal cortex is suggested to play a role in the processing of self-motion information, we hypothesised that such processing would be necessary for maintaining stable place fields in the absence of environmental cues. Place cells were recorded as medial entorhinal cortex–lesioned rats explored a circular arena during five 16-min sessions comprising a baseline session with all sensory inputs available followed by four sessions during which environmental (i.e. visual, olfactory, tactile) cues were progressively reduced to the point that animals could rely exclusively on self-motion cues to maintain stable place fields. We found that place field stability and a number of place cell firing properties were affected by medial entorhinal cortex lesions in the baseline session. When rats were forced to rely exclusively on self-motion cues, within-session place field stability was dramatically decreased in medial entorhinal cortex rats relative to SHAM rats. These results support a major role of the medial entorhinal cortex in processing self-motion cues, with this information being conveyed to the hippocampus to help anchor and maintain a stable spatial representation during movement.

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.

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 Position-theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate

2019 ◽  
Author(s):  
Kathryn McClain ◽  
David Tingley ◽  
David Heeger ◽  
György Buzsáki
Keyword(s):  
Firing Rate ◽  
Spatial Information ◽  
Cell Activity ◽  
Gain Control ◽  
Place Cell ◽  
Small Subset ◽  
Running Speed ◽  
Speed Modulation ◽  
Place Fields ◽  
Theta Phase

AbstractSpiking activity of place cells in the hippocampus encodes the animal’s position as it moves through an environment. Within a cell’s place field, both the firing rate and the phase of spiking in the local theta oscillation contain spatial information. We propose a position-theta-phase (PTP) model that captures the simultaneous expression of the firing-rate code and theta-phase code in place cell spiking. This model parametrically characterizes place fields to compare across cells, time and condition, generates realistic place cell simulation data, and conceptualizes a framework for principled hypothesis testing to identify additional features of place cell activity. We use the PTP model to assess the effect of running speed in place cell data recorded from rats running on linear tracks. For the majority of place fields we do not find evidence for speed modulation of the firing rate. For a small subset of place fields, we find firing rates significantly increase or decrease with speed. We use the PTP model to compare candidate mechanisms of speed modulation in significantly modulated fields, and determine that speed acts as a gain control on the magnitude of firing rate. Our model provides a tool that connects rigorous analysis with a computational framework for understanding place cell activity.SignificanceThe hippocampus is heavily studied in the context of spatial navigation, and the format of spatial information in hippocampus is multifaceted and complex. Furthermore, the hippocampus is also thought to contain information about other important aspects of behavior such as running speed, though there is not agreement on the nature and magnitude of their effect. To understand how all of these variables are simultaneously represented and used to guide behavior, a theoretical framework is needed that can be directly applied to the data we record. We present a model that captures well-established spatial-encoding features of hippocampal activity and provides the opportunity to identify and incorporate novel features for our collective understanding.

scholarly journals Ripple Band Phase Precession of Place Cell Firing during Replay

2021 ◽  
Author(s):  
Daniel Bush ◽  
Freyja Olafsdottir ◽  
Caswell Barry ◽  
Neil Burgess
Keyword(s):  
Hippocampal Formation ◽  
Receptive Fields ◽  
Negative Relationship ◽  
Place Cell ◽  
Place Cells ◽  
Phase Coding ◽  
Equivalent Rate ◽  
Phase Precession ◽  
Cell Firing ◽  
Ripple Phase

Phase coding offers several theoretical advantages for information transmission compared to an equivalent rate code. Phase coding is shown by place cells in the rodent hippocampal formation, which fire at progressively earlier phases of the movement related 6-12Hz theta rhythm as their spatial receptive fields are traversed. Importantly, however, phase coding is independent of carrier frequency, and so we asked whether it might also be exhibited by place cells during 150-250Hz ripple band activity, when they are thought to replay information to neocortex. We demonstrate that place cells which fire multiple spikes during candidate replay events do so at progressively earlier ripple phases, and that spikes fired across all replay events exhibit a negative relationship between decoded location within the firing field and ripple phase. These results provide insights into the mechanisms underlying phase coding and place cell replay, as well as the neural code propagated to downstream neurons.

scholarly journals Mild Traumatic Brain Injury Decreases Spatial Information Content and Reduces Place Field Stability of Hippocampal CA1 Neurons

2020 ◽  
Vol 37 (2) ◽  
pp. 227-235 ◽  
Author(s):  
John I. Broussard ◽  
John B. Redell ◽  
Jing Zhao ◽  
Mark E. Maynard ◽  
Nobuhide Kobori ◽  
...  
Keyword(s):  
Traumatic Brain Injury ◽  
Brain Injury ◽  
Information Content ◽  
Mild Traumatic Brain Injury ◽  
Spatial Information ◽  
Place Field ◽  
Ca1 Neurons ◽  
Hippocampal Ca1 Neurons ◽  
Hippocampal Ca1

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 Place-cell capacity and volatility with grid-like inputs

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Man Yi Yim ◽  
Lorenzo A Sadun ◽  
Ila R Fiete ◽  
Thibaud Taillefumier
Keyword(s):  
Grid Cell ◽  
Place Cell ◽  
Place Cells ◽  
Place Field ◽  
Cell Capacity ◽  
Spatial Range ◽  
External Cues ◽  
Noise Robust ◽  
Large Response

What factors constrain the arrangement of the multiple fields of a place cell? By modeling place cells as perceptrons that act on multiscale periodic grid-cell inputs, we analytically enumerate a place cell's repertoire - how many field arrangements it can realize without external cues while its grid inputs are unique; and derive its capacity - the spatial range over which it can achieve any field arrangement. We show that the repertoire is very large and relatively noise-robust. However, the repertoire is a vanishing fraction of all arrangements, while capacity scales only as the sum of the grid periods so field arrangements are constrained over larger distances. Thus, grid-driven place field arrangements define a large response scaffold that is strongly constrained by its structured inputs. Finally, we show that altering grid-place weights to generate an arbitrary new place field strongly affects existing arrangements, which could explain the volatility of the place code.

scholarly journals Robotic and neuronal simulation of the hippocampus and rat navigation

1997 ◽  
Vol 352 (1360) ◽  
pp. 1535-1543 ◽  
Author(s):  
Neil Burgess ◽  
James G. Donnett ◽  
Kathryn J. Jeffery ◽  
John O–keefe
Keyword(s):  
Short Range ◽  
Place Cell ◽  
Place Cells ◽  
Proximity Data ◽  
Heading Direction ◽  
Cell Firing ◽  
Synaptic Changes ◽  
External Signals ◽  
Good Agreement

The properties of hippocampal place cells are reviewed, with particular attention to the nature of the internal and external signals that support their firing. A neuronal simulation of the firing of place cells in open–field environments of varying shape is presented. This simulation is coupled with an existing model of how place–cell firing can be used to drive navigation and is tested by implementation as a miniature mobile robot. The sensors on the robot provide visual, odometric and short–range proximity data, which are combined to estimate the distance of the walls of the enclosure from the robot and the robot's current heading direction. These inputs drive the hippocampal simulation, in which the robot's location is represented as the firing of place cells. If a goal location is encountered, learning occurs in connections from the concurrently active place cells to a set of ‘goal cells’, which guide subsequent navigation, allowing the robot to return to an unmarked location. The system shows good agreement with actual place–cell firing, and makes predictions regarding the firing of cells in the subiculum, the effect of blocking long–term synaptic changes, and the locus of search of rats after deformation of their environment.

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