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 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.

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 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 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 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.

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 Neural dynamics indicate parallel integration of environmental and self-motion information by place and grid cells

2019 ◽  
Author(s):  
Dmitri Laptev ◽  
Neil Burgess
Keyword(s):  
Path Integration ◽  
Temporal Dynamics ◽  
Hippocampal Formation ◽  
Place Cell ◽  
Place Cells ◽  
Motion Information ◽  
Grid Cells ◽  
Attractor Network ◽  
Cell Firing ◽  
Self Motion

AbstractPlace cells and grid cells in the hippocampal formation are thought to integrate sensory and self-motion information into a representation of estimated spatial location, but the precise mechanism is unknown. We simulated a parallel attractor system in which place cells form an attractor network driven by environmental inputs and grid cells form an attractor network performing path integration driven by self-motion, with inter-connections between them allowing both types of input to influence firing in both ensembles. We show that such a system is needed to explain the spatial patterns and temporal dynamics of place cell firing when rats run on a linear track in which the familiar correspondence between environmental and self-motion inputs is changed (Gothard et al., 1996b; Redish et al., 2000). In contrast, the alternative architecture of a single recurrent network of place cells (performing path integration and receiving environmental inputs) cannot reproduce the place cell firing dynamics. These results support the hypothesis that grid and place cells provide two different but complementary attractor representations (based on self-motion and environmental sensory inputs respectively). Our results also indicate the specific neural mechanism and main predictors of hippocampal map realignment and make predictions for future studies.

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 Variable place–cell coupling to a continuously viewed stimulus: evidence that the hippocampus is part of a perceptual system

1997 ◽  
Vol 352 (1360) ◽  
pp. 1505-1513 ◽  
Author(s):  
Alexander Rotenberg ◽  
Robert U. Muller
Keyword(s):  
Nervous System ◽  
Neural Activity ◽  
Angular Position ◽  
Place Cell ◽  
Place Cells ◽  
Perceptual System ◽  
Original Position ◽  
Cell Coupling ◽  
Mapping System ◽  
Cell Firing

A key feature of perception is that the interpretation of a single, continuously available stimulus can change from time to time. This aspect of perception is well illustrated by the use of ambiguous figures that can be seen in two different ways. When people view such a stimulus they almost universally describe what they are seeing as jumping between two states. If it is agreed that this perceptual phenemonon is causally linked to the activity of nerve cells, the state jumps would have to occur in conjunction with changes in neural activity somewhere in the nervous system. The experiments described in this paper suggest that hippocampal place cells are part of a perceptual system. Variations were made of a ‘cue–card rotation’ experiment on rats in which the angular position of a prominent visual stimulus on the wall of cylinder is changed in the rat's presence. The three main results are as follows. (i) Place–cell firing fields remain stationary if the cue is rotated by 180° so that the relation between the cue and the field is altered. (ii) Firing fields rotate by 45° when the cue is rotated by 45°and the relation between the field and the card is maintained. (iii) If the cue is first rotated by 180°and then rotated in a series of 45° steps, the field finishes at a different angular position relative to the card when the card is back in its original position. Thus, place cells can fire in two different ways in reponse to a continuously viewed stimulus. It is concluded that place cells reveal that the hippocampal mapping system also has properties expected of a perceptual system.

scholarly journals On the Organization of Grid and Place Cells: Neural Denoising via Subspace Learning

2019 ◽  
Vol 31 (8) ◽  
pp. 1519-1550
Author(s):  
David M. Schwartz ◽  
O. Ozan Koyluoglu
Keyword(s):  
Hebbian Learning ◽  
Grid Cell ◽  
Subspace Learning ◽  
Place Cell ◽  
Place Cells ◽  
Neural Code ◽  
Neural Representation ◽  
Cell Populations ◽  
Medial Entorhinal Cortex ◽  
Cell Networks

Place cells in the hippocampus (HC) are active when an animal visits a certain location (referred to as a place field) within an environment. Grid cells in the medial entorhinal cortex (MEC) respond at multiple locations, with firing fields that form a periodic and hexagonal tiling of the environment. The joint activity of grid and place cell populations, as a function of location, forms a neural code for space. In this article, we develop an understanding of the relationships between coding theoretically relevant properties of the combined activity of these populations and how these properties limit the robustness of this representation to noise-induced interference. These relationships are revisited by measuring the performances of biologically realizable algorithms implemented by networks of place and grid cell populations, as well as constraint neurons, which perform denoising operations. Contributions of this work include the investigation of coding theoretic limitations of the mammalian neural code for location and how communication between grid and place cell networks may improve the accuracy of each population's representation. Simulations demonstrate that denoising mechanisms analyzed here can significantly improve the fidelity of this neural representation of space. Furthermore, patterns observed in connectivity of each population of simulated cells predict that anti-Hebbian learning drives decreases in inter-HC-MEC connectivity along the dorsoventral axis.

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