scholarly journals Neuronal sequences during theta rely on behavior-dependent spatial maps

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Eloy Parra-Barrero ◽  
Kamran Diba ◽  
Sen Cheng
Keyword(s):  
Running Speed ◽  
True Location ◽  
Phase Code ◽  
Phase Precession ◽  
Relevant Variables ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
Exact Relationship ◽  
Spatial Maps ◽  
Speed Characteristic

Navigation 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 provided by neuronal sequences start behind the animal's true location and then sweep forward. However, the exact relationship between theta phase, represented position and true location remains unclear and even paradoxical. Here, we formalize previous notions of 'spatial' or 'temporal' theta sweeps that have appeared in the literature. We analyze single-cell and population variables in unit recordings from rat CA1 place cells and compare them to model simulations based on each of these schemes. We show that neither spatial nor temporal sweeps quantitatively accounts for how all relevant variables change with running speed. To reconcile these schemes with our observations, we introduce 'behavior-dependent' sweeps, in which theta sweep length and place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. These behavior-dependent spatial maps provide a structured heterogeneity that is essential for understanding the hippocampal code.

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 Spatial cell firing during virtual navigation of open arenas by head-restrained mice

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Guifen Chen ◽  
John Andrew King ◽  
Yi Lu ◽  
Francesca Cacucci ◽  
Neil Burgess
Keyword(s):  
Place Cell ◽  
Head Movements ◽  
Running Speed ◽  
Firing Patterns ◽  
Firing Rates ◽  
Theta Frequency ◽  
Phase Precession ◽  
Cell Firing ◽  
Theta Phase ◽  
Theta Phase Precession

We present a mouse virtual reality (VR) system which restrains head-movements to horizontal rotations, compatible with multi-photon imaging. This system allows expression of the spatial navigation and neuronal firing patterns characteristic of real open arenas (R). Comparing VR to R: place and grid, but not head-direction, cell firing had broader spatial tuning; place, but not grid, cell firing was more directional; theta frequency increased less with running speed, whereas increases in firing rates with running speed and place and grid cells' theta phase precession were similar. These results suggest that the omni-directional place cell firing in R may require local-cues unavailable in VR, and that the scale of grid and place cell firing patterns, and theta frequency, reflect translational motion inferred from both virtual (visual and proprioceptive) and real (vestibular translation and extra-maze) cues. By contrast, firing rates and theta phase precession appear to reflect visual and proprioceptive cues alone.

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 Alternating sequences of future and past behavior encoded within hippocampal theta oscillations

Science ◽  
2020 ◽  
Vol 370 (6513) ◽  
pp. 247-250 ◽  
Author(s):  
Mengni Wang ◽  
David J. Foster ◽  
Brad E. Pfeiffer
Keyword(s):  
Activity Patterns ◽  
Place Cells ◽  
Theta Oscillations ◽  
Retrospective Evaluation ◽  
Past Behavior ◽  
Hippocampal Ca1 ◽  
Ongoing Behavior ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
And Storage

Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.

scholarly journals Hippocampal theta phase–contingent memory retrieval in delay and trace eyeblink conditioning

2018 ◽  
Vol 337 ◽  
pp. 264-270 ◽  
Author(s):  
Tomi Waselius ◽  
Eveliina Pöllänen ◽  
Jan Wikgren ◽  
Markku Penttonen ◽  
Miriam S. Nokia
Keyword(s):  
Memory Retrieval ◽  
Eyeblink Conditioning ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
Trace Eyeblink Conditioning
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