scholarly journals Hippocampal spike-time correlations and place-field overlaps during open field foraging

2019 ◽  
Author(s):  
Mauro M. Monsalve-Mercado ◽  
Yasser Roudi
Keyword(s):  
Open Field ◽  
Spatial Information ◽  
Time Lag ◽  
Place Cells ◽  
Spike Time ◽  
Place Field ◽  
Phase Code ◽  
Place Fields ◽  
Cross Correlations ◽  
The Relationship

AbstractPhase precessing place cells encode spatial information on fine timescales via the timing of their spikes. This phase code has been extensively studied on linear tracks and for short runs in the open field. However, less is known about the phase code on unconstrained trajectories lasting tens of minutes, typical of open field foraging. In previous work (Monsalve-Mercado and Leibold, 2017), an analytic expression was derived for the spike-time cross-correlation between phase precessing place cells during natural foraging in the open field. This expression makes two predictions on how this phase code differs from the linear track case: cross-correlations are symmetric with respect to time, and they represent the distance between pairs of place fields in that the theta-filtered cross-correlations around zero time-lag are positive for cells with nearby fields while they are negative for those with fields further apart. Here we analyze several available open field recordings and show that these predictions hold for pairs of CA1 place cells. We also show that the relationship remains during remapping in CA1, and it is also present in place cells in area CA3. For CA1 place cells of Fmr1-null mice, which exhibit normal place fields but somewhat weaker temporal coordination with respect to theta compared to wild type, the cross-correlations still remain symmetric but the relationship to place field overlap is largely lost. The relationship discussed here describes how spatial information is communicated by place cells to downstream areas in a finer theta-timescale, relevant for learning and memory formation in behavioural tasks lasting tens of minutes in the open field.

scholarly journals Differences in reward biased spatial representations in the lateral septum and hippocampus

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Hannah S Wirtshafter ◽  
Matthew A Wilson
Keyword(s):  
Spatial Information ◽  
Place Cells ◽  
Lateral Septum ◽  
Field Size ◽  
Spatial Representations ◽  
Navigation Task ◽  
Place Fields ◽  
Cross Correlations

The lateral septum (LS), which is innervated by the hippocampus, is known to represent spatial information. However, the details of place representation in the LS, and whether this place information is combined with reward signaling, remains unknown. We simultaneously recorded from rat CA1 and caudodorsal lateral septum in rat during a rewarded navigation task and compared spatial firing in the two areas. While LS place cells are less numerous than in hippocampus, they are similar to the hippocampus in field size and number of fields per cell, but with field shape and center distributions that are more skewed toward reward. Spike cross-correlations between the hippocampus and LS are greatest for cells that have reward-proximate place fields, suggesting a role for the LS in relaying task-relevant hippocampal spatial information to downstream areas, such as the VTA.

scholarly journals Spatial information transfer in hippocampal place cells depends on trial-to-trial variability, symmetry of place-field firing and biophysical heterogeneities

2020 ◽  
Author(s):  
Ankit Roy ◽  
Rishikesh Narayanan
Keyword(s):  
Information Transfer ◽  
Spatial Information ◽  
Tuning Curve ◽  
Place Cells ◽  
Place Field ◽  
Tuning Curves ◽  
Spatial Tuning ◽  
Model Tuning ◽  
The Impact ◽  
The Relationship

ABSTRACTThe relationship between the feature-tuning curve and information transfer profile of individual neurons provides vital insights about neural encoding. However, the relationship between the spatial tuning curve and spatial information transfer of hippocampal place cells remains unexplored. Here, employing a stochastic search procedure spanning thousands of models, we arrived at 127 conductance-based place-cell models that exhibited signature electrophysiological characteristics and sharp spatial tuning, with parametric values that exhibited neither clustering nor strong pairwise correlations. We introduced trial-to-trial variability in responses and computed model tuning curves and information transfer profiles, using stimulus-specific (SSI) and mutual (MI) information metrics, across locations within the place field. We found spatial information transfer to be heterogeneous across models, but to reduce consistently with increasing degrees of variability. Importantly, whereas reliable low-variability responses implied that maximal information transfer occurred at high-slope regions of the tuning curve, increase in variability resulted in maximal transfer occurring at the peak-firing location in a subset of models. Moreover, experience-dependent asymmetry in place-field firing introduced asymmetries in the information transfer computed through MI, but not SSI, and the impact of activity-dependent variability on information transfer was minimal compared to activity-independent variability. Biophysically, we unveiled a many-to-one relationship between different ion channels and information transfer, and demonstrated critical roles for N-methyl-D-aspartate receptors, transient potassium and dendritic sodium channels in regulating information transfer. Our results emphasize the need to account for trial-to-trial variability, tuning-curve shape and biological heterogeneities while assessing information transfer, and demonstrate ion-channel degeneracy in the regulation of spatial information transfer.

Task-Dependent Representations in Rat Hippocampal Place Neurons

1997 ◽  
Vol 78 (2) ◽  
pp. 597-613 ◽  
Author(s):  
Tsuneyuki Kobayashi ◽  
Hisao Nishijo ◽  
Masaji Fukuda ◽  
Jan Bures ◽  
Taketoshi Ono
Keyword(s):  
Open Field ◽  
Hippocampal Neurons ◽  
Hippocampal Formation ◽  
Movement Speed ◽  
Neuron Activity ◽  
Place Field ◽  
Complex Spike ◽  
Place Fields ◽  
Sequential Trials ◽  
Self Stimulation

Kobayashi, Tsuneyuki, Hisao Nishijo, Masaji Fukuda, Jan Bures, and Taketoshi Ono. Task-dependent representations in rat hippocampal place neurons. J. Neurophysiol. 78: 597–613, 1997. It is suggested that the hippocampal formation is essential to spatial representations by flexible encoding of diverse information during navigation, which includes not only externally generated sensory information such as visual and auditory sensation but also ideothetic information concerning locomotion (i.e., internally generated information such as proprioceptive and vestibular sensation) as well as information concerning reward. In the present study, we investigated how various types of information are represented in the hippocampal formation, by recording hippocampal complex-spike cells from rats that performed three types of place learning tasks in a circular open field with the use of intracranial self-stimulation as reward. The intracranial self-stimulation reward was delivered in the following three contexts: if the rat 1) entered an experimenter-determined reward place within the open field, and this place was randomly varied in sequential trials; 2) entered two specific places, one within and one outside the place field (an area identified by change in activity of a place neuron); or 3) entered an experimenter-specified place outside the place field. Because the behavioral trails during navigation were more constant in the second task than in the first task, ideothetic information concerning locomotion was more relevant to acquiring reward in the second task than in the first task. Of 43 complex-spike cells recorded, 37 displayed place fields under the first task. Of these 37 place neurons, 34 also had significant reward correlates only inside the place field. Although reward and place correlates of the place neuron activity did not change between the first and second tasks, neuronal correlates to behavioral variables for locomotion such as movement speed, direction, and turning angle significantly increased in the second task. Furthermore, 6 of 31 place neurons tested with the third task, in which the reward place was located outside the original place field, shifted place fields. The results indicated that neuronal correlates of most place neurons flexibly increased their sensitivity to relevant information in a given context and environment, and some place neurons changed the place field per se with place reward association. These results suggest two strategies for how hippocampal neurons incorporate an incredible variety of perceptions into a unified representation of the environment: through flexible use of information and the creation of new representations.

scholarly journals Place cells in head-fixed mice navigating a floating real-world environment

2020 ◽  
Author(s):  
Mary Ann Go ◽  
Jake Rogers ◽  
Giuseppe P. Gava ◽  
Catherine Davey ◽  
Seigfred Prado ◽  
...  
Keyword(s):  
Virtual Reality ◽  
Real World ◽  
Spatial Information ◽  
Memory Function ◽  
Place Cells ◽  
Neural Population ◽  
Spatial Coding ◽  
Place Fields ◽  
Freely Moving ◽  
World Environment

ABSTRACTThe hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of a track floating on air, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells with place fields remapping when animals entered a different environment. When animals re-entered the same environment, place fields typically remapped over a time period of multiple days, faster than in freely moving preparations, but comparable with virtual reality. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.

scholarly journals Behavior-dependent spatial maps enable efficient theta phase coding

2021 ◽  
Author(s):  
Eloy Parra-Barrero ◽  
Kamran Diba ◽  
Sen Cheng
Keyword(s):  
Place Cells ◽  
Spatial Representations ◽  
Place Field ◽  
Phase Code ◽  
Phase Precession ◽  
Relevant Variables ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
Exact Relationship ◽  
Speed Characteristic

AbstractNavigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations start behind the animal’s location and then sweep forward. However, the exact relationship between phase and represented and true positions remains unclear and even paradoxical. Here, we formalize previous notions as ‘spatial’ or ‘temporal’ sweeps, analyze single-cell and population variables in recordings from rat CA1 place cells, and compare them to model simulations. We show that neither sweep type quantitatively accounts for all relevant variables. Thus we introduce ‘behavior-dependent’ sweeps, which fit our key observation that sweep length, and hence place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. This structured heterogeneity is essential for understanding the hippocampal code.

scholarly journals Place Cells in Head-Fixed Mice Navigating a Floating Real-World Environment

2021 ◽  
Vol 15 ◽  
Author(s):  
Mary Ann Go ◽  
Jake Rogers ◽  
Giuseppe P. Gava ◽  
Catherine E. Davey ◽  
Seigfred Prado ◽  
...  
Keyword(s):  
Virtual Reality ◽  
Real World ◽  
Spatial Information ◽  
Memory Function ◽  
Place Cells ◽  
Neural Population ◽  
Spatial Coding ◽  
Place Fields ◽  
Freely Moving ◽  
World Environment

The hippocampal place cell system in rodents has provided a major paradigm for the scientific investigation of memory function and dysfunction. Place cells have been observed in area CA1 of the hippocampus of both freely moving animals, and of head-fixed animals navigating in virtual reality environments. However, spatial coding in virtual reality preparations has been observed to be impaired. Here we show that the use of a real-world environment system for head-fixed mice, consisting of an air-floating track with proximal cues, provides some advantages over virtual reality systems for the study of spatial memory. We imaged the hippocampus of head-fixed mice injected with the genetically encoded calcium indicator GCaMP6s while they navigated circularly constrained or open environments on the floating platform. We observed consistent place tuning in a substantial fraction of cells despite the absence of distal visual cues. Place fields remapped when animals entered a different environment. When animals re-entered the same environment, place fields typically remapped over a time period of multiple days, faster than in freely moving preparations, but comparable with virtual reality. Spatial information rates were within the range observed in freely moving mice. Manifold analysis indicated that spatial information could be extracted from a low-dimensional subspace of the neural population dynamics. This is the first demonstration of place cells in head-fixed mice navigating on an air-lifted real-world platform, validating its use for the study of brain circuits involved in memory and affected by neurodegenerative disorders.

scholarly journals Asymmetry of the temporal code for space by hippocampal place cells

2016 ◽  
Author(s):  
Bryan C. Souza ◽  
Adriano B. L. Tort
Keyword(s):  
Firing Rate ◽  
Spatial Information ◽  
Place Cells ◽  
Spike Timing ◽  
Temporal Coding ◽  
Place Field ◽  
Phase Precession ◽  
Wide Debate ◽  
Rate Coding ◽  
Theta Phase

Hippocampal place cells convey spatial information through spike frequency (“rate coding”) and spike timing relative to the theta phase (“temporal coding”). Whether rate and temporal coding are due to independent or related mechanisms has been the subject of wide debate. Here we show that the spike timing of place cells couples to theta phase before major increases in firing rate, anticipating the animal’s entrance into the classical, rate-based place field. In contrast, spikes rapidly decouple from theta as the animal leaves the place field and firing rate decreases. Therefore, temporal coding has strong asymmetry around the place field center. We further show that the dynamics of temporal coding along space evolves in three stages: phase coupling, phase precession and phase decoupling. These results suggest that place cells represent more future than past locations through their spike timing and that independent mechanisms govern rate and temporal coding.

scholarly journals Intuitive planning: global navigation through cognitive maps based on grid-like codes

2018 ◽  
Author(s):  
Alon B. Baram ◽  
Timothy H. Muller ◽  
James C.R. Whittington ◽  
Timothy E.J. Behrens
Keyword(s):  
Spatial Information ◽  
Distance Measure ◽  
Grid Cell ◽  
Simple Algorithm ◽  
Place Cells ◽  
Grid Cells ◽  
Global Knowledge ◽  
The World ◽  
One Step ◽  
The Relationship

AbstractIt is proposed that a cognitive map encoding the relationships between objects supports the ability to flexibly navigate the world. Place cells and grid cells provide evidence for such a map in a spatial context. Emerging evidence suggests analogous cells code for non-spatial information. Further, it has been shown that grid cells resemble the eigenvectors of the relationship between place cells and can be learnt from local inputs. Here we show that these locally-learnt eigenvectors contain not only local information but also global knowledge that can provide both distributions over future states as well as a global distance measure encoding approximate distances between every object in the world. By simply changing the weights in the grid cell population, it is possible to switch between computing these different measures. We demonstrate a simple algorithm can use these measures to globally navigate arbitrary topologies without searching more than one step ahead. We refer to this as intuitive planning.

scholarly journals Choice of method of place cell classification determines the population of cells identified

2021 ◽  
Vol 17 (7) ◽  
pp. e1008835
Author(s):  
Dori M. Grijseels ◽  
Kira Shaw ◽  
Caswell Barry ◽  
Catherine N. Hall
Keyword(s):  
Spatial Information ◽  
Real Data ◽  
Place Cell ◽  
Place Cells ◽  
Optical Methods ◽  
Combination Method ◽  
Cell Detection ◽  
Imaging Data ◽  
Place Field ◽  
Implanted Electrodes

Place cells, spatially responsive hippocampal cells, provide the neural substrate supporting navigation and spatial memory. Historically most studies of these neurons have used electrophysiological recordings from implanted electrodes but optical methods, measuring intracellular calcium, are becoming increasingly common. Several methods have been proposed as a means to identify place cells based on their calcium activity but there is no common standard and it is unclear how reliable different approaches are. Here we tested four methods that have previously been applied to two-photon hippocampal imaging or electrophysiological data, using both model datasets and real imaging data. These methods use different parameters to identify place cells, including the peak activity in the place field, compared to other locations (the Peak method); the stability of cells’ activity over repeated traversals of an environment (Stability method); a combination of these parameters with the size of the place field (Combination method); and the spatial information held by the cells (Information method). The methods performed differently from each other on both model and real data. In real datasets, vastly different numbers of place cells were identified using the four methods, with little overlap between the populations identified as place cells. Therefore, choice of place cell detection method dramatically affects the number and properties of identified cells. Ultimately, we recommend the Peak method be used in future studies to identify place cell populations, as this method is robust to moderate variations in place field within a session, and makes no inherent assumptions about the spatial information in place fields, unless there is an explicit theoretical reason for detecting cells with more narrowly defined properties.

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