scholarly journals Place cells on a maze encode routes rather than destinations

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Roddy M Grieves ◽  
Emma R Wood ◽  
Paul A Dudchenko

Hippocampal place cells fire at different rates when a rodent runs through a given location on its way to different destinations. However, it is unclear whether such firing represents the animal’s intended destination or the execution of a specific trajectory. To distinguish between these possibilities, Lister Hooded rats (n = 8) were trained to navigate from a start box to three goal locations via four partially overlapping routes. Two of these led to the same goal location. Of the cells that fired on these two routes, 95.8% showed route-dependent firing (firing on only one route), whereas only two cells (4.2%) showed goal-dependent firing (firing similarly on both routes). In addition, route-dependent place cells over-represented the less discriminable routes, and place cells in general over-represented the start location. These results indicate that place cell firing on overlapping routes reflects the animal’s route, not its goals, and that this firing may aid spatial discrimination.

2021 ◽  
Author(s):  
Jake Ormond ◽  
John O'Keefe

One function of the Hippocampal Cognitive Map is to provide information about salient locations in familiar environments such as those containing reward or danger, and to support navigation towards or away from those locations. Although much is known about how the hippocampus encodes location in world-centred coordinates, how it supports flexible navigation is less well understood. We recorded from CA1 place cells while rats navigated to a goal or freely foraged on the honeycomb maze. The maze tests the animal's ability to navigate using indirect as well as direct paths to the goal and allows the directionality of place cells to be assessed at each choice point during traversal to the goal. Place fields showed strong directional polarization in the navigation task, and to a lesser extent during random foraging. This polarization was characterized by vector fields which converged to sinks distributed throughout the environment. The distribution of these convergence sinks was centred near the goal location, and the population vector field converged on the goal, providing a strong navigational signal. Changing the goal location led to the movement of ConSinks and vector fields towards the new goal and within-days, the ConSink distance to the goal decreased with continued training. The honeycomb maze allows the independent assessment of spatial representation and spatial action in place cell activity and shows how the latter depends on the former. The results suggest a vector-based model of how the hippocampus supports flexible navigation, allowing animals to select optimal paths to destinations from any location in the environment.


2021 ◽  
Author(s):  
Daniel Bush ◽  
Freyja Olafsdottir ◽  
Caswell Barry ◽  
Neil Burgess

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.


2020 ◽  
Author(s):  
Ryan E. Harvey ◽  
Laura E. Berkowitz ◽  
Daniel D. Savage ◽  
Derek A. Hamilton ◽  
Benjamin J. Clark

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.


1997 ◽  
Vol 352 (1360) ◽  
pp. 1535-1543 ◽  
Author(s):  
Neil Burgess ◽  
James G. Donnett ◽  
Kathryn J. Jeffery ◽  
John O–keefe

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.


2019 ◽  
Author(s):  
Dmitri Laptev ◽  
Neil Burgess

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.


1997 ◽  
Vol 352 (1360) ◽  
pp. 1505-1513 ◽  
Author(s):  
Alexander Rotenberg ◽  
Robert U. Muller

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.


2021 ◽  
Author(s):  
Eliott R J Levy ◽  
Eun Hye Park ◽  
William T Redman ◽  
André A Fenton

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.


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.


2018 ◽  
Author(s):  
Laurenz Muessig ◽  
Michal Lasek ◽  
Isabella Varsavsky ◽  
Francesca Cacucci ◽  
Thomas J Wills

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.


2018 ◽  
Author(s):  
Victor Pedrosa ◽  
Claudia Clopath

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.


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