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

ABSTRACT: 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.

SUBMITTER: McClain K

PROVIDER: S-EPMC6936353 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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

McClain Kathryn K Tingley David D Heeger David J DJ Buzsáki György G

Proceedings of the National Academy of Sciences of the United States of America 20191216 52

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 cond ...[more]

PMID: 31843934

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Project description:The 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 levels 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. We unveiled ion-channel degeneracy in the regulation of spatial information transfer, and demonstrated critical roles for N-methyl-d-aspartate receptors, transient potassium and dendritic sodium channels in regulating information transfer. Our results demonstrate that trial-to-trial variability, tuning-curve shape and biological heterogeneities critically regulate the relationship between the spatial tuning curve and spatial information transfer in hippocampal place cells.

Project description:BackgroundRunning is a hugely popular sport. Unfortunately, running-related injury (RRI) rates are high, particularly amongst amateur and recreational runners. Finding ways to reduce RRI rates and maximise comfort and performance for runners is important. Evidence regarding whether orthotics can successfully improve these parameters is limited and contradicting. Further research is required to provide runners with clearer guidance on the usefulness of orthotics.AimTo investigate the effect of Aetrex Orthotics on comfort, speed and RRI rates during recreational running.MethodsOne hundred and six recreational runners were recruited on a voluntary basis via running clubs and social media pages and randomised into either the intervention or control group. Participants in the intervention group ran with Aetrex L700 Speed Orthotics inserted in their usual running shoes, whilst participants in the control group ran in their usual running shoes with no orthotics. The study ran for an 8-wk period. Participants provided data relating to running comfort, distance, and time during weeks 3-6. Participants provided data relating to any RRIs they sustained during all 8 wks. Running distance and time were used to calculate running speed in miles per hour (mph). For each outcome variable, 95% confidence intervals and P values were calculated to assess the statistical significance between the groups. For comfort and speed data, univariate multi-level analysis was performed, and for outcome variables with significant between group differences, multi-level multivariate analysis was performed to evaluate any confounding effects of gender and age.ResultsNinety-four participants were included in the final analysis (drop-out rate = 11%). Comfort and speed from 940 runs and 978 injury data reports were analysed. Participants who ran with orthotics reported, on average, speeds 0.30 mph faster (P = 0.20) and comfort scores 1.27 points higher (P ≤ 0.001) than participants who ran with no orthotics. They were also 2.22 times less likely to sustain an injury (P = 0.08) than participants who ran with no orthotics. However, findings were only significant for comfort and not for speed or injury rates. Age and gender were found to be significant predictors of comfort. However, the improvements in comfort reported by participants who ran with orthotics were still significant after adjusting for age and gender.ConclusionThis study found orthotics to improve comfort and speed and prevent RRIs whilst running. However, these findings were only statistically significant for comfort.

Dataset Information

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

Publications

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

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