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 Position–theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate

2019 ◽  
Vol 116 (52) ◽  
pp. 27035-27042 ◽  
Author(s):  
Kathryn McClain ◽  
David Tingley ◽  
David J. 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

Spiking 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 conditions; 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.

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 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 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 Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

2019 ◽  
Author(s):  
Mark C. Zielinski ◽  
Justin D. Shin ◽  
Shantanu P. Jadhav
Keyword(s):  
Prefrontal Cortex ◽  
Spatial Memory ◽  
Spatial Information ◽  
Cell Activity ◽  
Memory Task ◽  
Physiological Mechanism ◽  
Spatial Position ◽  
Theta Oscillations ◽  
Male Rats ◽  
Theta Phase

ABSTRACTInteractions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (~8 Hz) underlie a key physiological mechanism for mediating these coordinated interactions, and theta oscillatory coherence and phase-locked spiking in the two regions have been shown to be important for spatial memory. Hippocampal place cell activity associated with theta oscillations encodes spatial position during behavior, and theta-phase associated spiking is known to further mediate a temporal code for space within CA1 place fields. Although prefrontal neurons are prominently phase-locked to hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations mediate processing of spatial information across these networks remains unclear. Here, we addressed these questions using simultaneous recordings of dorsal CA1 – PFC ensembles and population decoding analyses in male rats performing a continuous spatial working memory task known to require hippocampal-prefrontal interactions. We found that in addition to CA1, population activity in PFC can also encode the animal’s current spatial position on a theta-cycle timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, incorporating theta-phase information during decoding to account for theta-phase associated spiking resulted in a significant improvement in the accuracy of prefrontal spatial representations, similar to concurrent CA1 representations. These findings indicate a theta-oscillation mediated mechanism of temporal coordination for shared processing and communication of spatial information across the two networks during spatial memory-guided behavior.

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 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.

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