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 Path integration in place cells of developing rats

2018 ◽  
Vol 115 (7) ◽  
pp. E1637-E1646 ◽  
Author(s):  
Tale L. Bjerknes ◽  
Nenitha C. Dagslott ◽  
Edvard I. Moser ◽  
May-Britt Moser
Keyword(s):  
Path Integration ◽  
Grid Cell ◽  
Cell System ◽  
Place Cells ◽  
Postnatal Life ◽  
Motion Information ◽  
Grid Cells ◽  
Adult Rats ◽  
Self Motion ◽  
Made In

Place cells in the hippocampus and grid cells in the medial entorhinal cortex rely on self-motion information and path integration for spatially confined firing. Place cells can be observed in young rats as soon as they leave their nest at around 2.5 wk of postnatal life. In contrast, the regularly spaced firing of grid cells develops only after weaning, during the fourth week. In the present study, we sought to determine whether place cells are able to integrate self-motion information before maturation of the grid-cell system. Place cells were recorded on a 200-cm linear track while preweaning, postweaning, and adult rats ran on successive trials from a start wall to a box at the end of a linear track. The position of the start wall was altered in the middle of the trial sequence. When recordings were made in complete darkness, place cells maintained fields at a fixed distance from the start wall regardless of the age of the animal. When lights were on, place fields were determined primarily by external landmarks, except at the very beginning of the track. This shift was observed in both young and adult animals. The results suggest that preweaning rats are able to calculate distances based on information from self-motion before the grid-cell system has matured to its full extent.

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 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 Experience-dependent trends in CA1 theta and slow gamma rhythms in freely behaving mice

2018 ◽  
Vol 119 (2) ◽  
pp. 476-489 ◽  
Author(s):  
Brian J. Gereke ◽  
Alexandra J. Mably ◽  
Laura Lee Colgin
Keyword(s):  
Spatial Information ◽  
Hippocampal Formation ◽  
Cell Activity ◽  
Place Cell ◽  
Place Cells ◽  
Running Speed ◽  
Circular Track ◽  
Gamma Rhythms ◽  
Over Time ◽  
First Session

CA1 place cells become more anticipatory with experience, an effect thought to be caused by NMDA receptor-dependent plasticity in the CA3–CA1 network. Theta (~5–12 Hz), slow gamma (~25–50 Hz), and fast gamma (~50–100 Hz) rhythms are thought to route spatial information in the hippocampal formation and to coordinate place cell ensembles. Yet, it is unknown whether these rhythms exhibit experience-dependent changes concurrent with those observed in place cells. Slow gamma rhythms are thought to indicate inputs from CA3 to CA1, and such inputs are thought to be strengthened with experience. Thus, we hypothesized that slow gamma rhythms would become more evident with experience. We tested this hypothesis using mice freely traversing a familiar circular track for three 10-min sessions per day. We found that slow gamma amplitude was reduced in the early minutes of the first session of each day, even though both theta and fast gamma amplitudes were elevated during this same period. However, in the first minutes of the second and third sessions of each day, all three rhythms were elevated. Interestingly, theta was elevated to a greater degree in the first minutes of the first session than in the first minutes of later sessions. Additionally, all three rhythms were strongly influenced by running speed in dynamic ways, with the influence of running speed on theta and slow gamma changing over time within and across sessions. These results raise the possibility that experience-dependent changes in hippocampal rhythms relate to changes in place cell activity that emerge with experience. NEW & NOTEWORTHY We show that CA1 theta, slow gamma, and fast gamma rhythms exhibit characteristic changes over time within sessions in familiar environments. These effects in familiar environments evolve across repeated sessions.

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 Modeling place cells and grid cells in multi-compartment environments: hippocampal-entorhinal loop as a multisensory integration circuit

2019 ◽  
Author(s):  
Tianyi Li ◽  
Angelo Arleo ◽  
Denis Sheynikhovich
Keyword(s):  
Experimental Studies ◽  
Place Cells ◽  
Grid Cells ◽  
Visual Cue ◽  
Conflicting Evidence ◽  
Hexagonal Grids ◽  
Continuous Interaction ◽  
Self Motion ◽  
High Degree ◽  
Key Parameter

AbstractHippocampal place cells and entorhinal grid cells are thought to form a representation of space by integrating internal and external sensory cues. Experimental studies show that different subsets of place cells are controlled by vision, self-motion or a combination of both. Moreover, recent studies in environments with a high degree of visual aliasing suggest that a continuous interaction between place cells and grid cells can result in a deformation of hexagonal grids or in a progressive loss of visual cue control. The computational nature of such a bidirectional interaction remains unclear. In this work we present a neural network model of a dynamic loop between place cells and grid cells. The model is tested in two recent experimental paradigms involving double-room environments that provide conflicting evidence about visual cue control over self-motion-based spatial codes. Analysis of the model behavior in the two experiments suggests that the strength of hippocampal-entorhinal dynamical loop is the key parameter governing differential cue control in multi-compartment environments. Construction of spatial representations in visually identical environments requires weak visual cue control, while synaptic plasticity is regulated by the mismatch between visual- and self-motion representations. More gener-ally our results suggest a functional segregation between plastic and dynamic processes in hippocampal processing.

scholarly journals Emergent Elasticity in the Neural Code for Space

2018 ◽  
Author(s):  
Samuel Ocko ◽  
Kiah Hardcastle ◽  
Lisa Giocomob ◽  
Surya Ganguli
Keyword(s):  
Neural Circuit ◽  
Topological Defects ◽  
Grid Cell ◽  
Grid Cells ◽  
Motion Cues ◽  
Hebbian Plasticity ◽  
Attractor Model ◽  
Cell Firing ◽  
Path Dependent ◽  
Self Motion

Upon encountering a novel environment, an animal must construct a consistent environmental map, as well as an internal estimate of its position within that map, by combining information from two distinct sources: self-motion cues and sensory landmark cues. How do known aspects of neural circuit dynamics and synaptic plasticity conspire to accomplish this feat? Here we show analytically how a neural attractor model that combines path integration of self-motion cues with Hebbian plasticity in synaptic weights from landmark cells can self-organize a consistent map of space as the animal explores an environment. Intriguingly, the emergence of this map can be understood as an elastic relaxation process between landmark cells mediated by the attractor network. Moreover, our model makes several experimentally testable predictions, including: (1) systematic path-dependent shifts in the firing field of grid cells towards the most recently encountered landmark, even in a fully learned environment, (2) systematic deformations in the firing fields of grid cells in irregular environments, akin to elastic deformations of solids forced into irregular containers, and (3) the creation of topological defects in grid cell firing patterns through specific environmental manipulations. Taken together, our results conceptually link known aspects of neurons and synapses to an emergent solution of a fundamental computational problem in navigation, while providing a unified account of disparate experimental observations.

scholarly journals Emergent elasticity in the neural code for space

2018 ◽  
Vol 115 (50) ◽  
pp. E11798-E11806 ◽  
Author(s):  
Samuel A. Ocko ◽  
Kiah Hardcastle ◽  
Lisa M. Giocomo ◽  
Surya Ganguli
Keyword(s):  
Neural Circuit ◽  
Topological Defects ◽  
Grid Cell ◽  
Grid Cells ◽  
Motion Cues ◽  
Hebbian Plasticity ◽  
Attractor Model ◽  
Cell Firing ◽  
Path Dependent ◽  
Self Motion

Upon encountering a novel environment, an animal must construct a consistent environmental map, as well as an internal estimate of its position within that map, by combining information from two distinct sources: self-motion cues and sensory landmark cues. How do known aspects of neural circuit dynamics and synaptic plasticity conspire to accomplish this feat? Here we show analytically how a neural attractor model that combines path integration of self-motion cues with Hebbian plasticity in synaptic weights from landmark cells can self-organize a consistent map of space as the animal explores an environment. Intriguingly, the emergence of this map can be understood as an elastic relaxation process between landmark cells mediated by the attractor network. Moreover, our model makes several experimentally testable predictions, including (i) systematic path-dependent shifts in the firing fields of grid cells toward the most recently encountered landmark, even in a fully learned environment; (ii) systematic deformations in the firing fields of grid cells in irregular environments, akin to elastic deformations of solids forced into irregular containers; and (iii) the creation of topological defects in grid cell firing patterns through specific environmental manipulations. Taken together, our results conceptually link known aspects of neurons and synapses to an emergent solution of a fundamental computational problem in navigation, while providing a unified account of disparate experimental observations.

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