Neuron
Volume 109, Issue 6, 17 March 2021, Pages 1029-1039.e8
Journal home page for Neuron

Article
Frequency of theta rhythm is controlled by acceleration, but not speed, in running rats

https://doi.org/10.1016/j.neuron.2021.01.017Get rights and content
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Highlights

  • Entorhinal-hippocampal theta frequency is not modulated by speed

  • Theta frequency is linearly related to positive, but not negative, acceleration

  • Rhythmic spiking modulation by acceleration is expressed across functional cell types

  • Slow decay of theta frequency after acceleration creates spurious speed correlation

Summary

The theta rhythm organizes neural activity across hippocampus and entorhinal cortex. A role for theta oscillations in spatial navigation is supported by half a century of research reporting that theta frequency encodes running speed linearly so that displacement can be estimated through theta frequency integration. We show that this relationship is an artifact caused by the fact that the speed of freely moving animals could not be systematically disentangled from acceleration. Using an experimental procedure that clamps running speed at pre-set values, we find that the theta frequency of local field potentials and spike activity is linearly related to positive acceleration, but not negative acceleration or speed. The modulation by positive-only acceleration makes rhythmic activity at theta frequency unfit as a code to compute displacement or any other kinematic variable. Temporally precise variations in theta frequency may instead serve as a mechanism for speeding up entorhinal-hippocampal computations during accelerated movement.

Keywords

speed
acceleration
theta rhythm
entorhinal cortex
hippocampus
space
grid cells
head direction cells
border cells
speed cells

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Present address: Douglas Mental Health University Institute, McGill University, Montreal, QC H4H 1R3, Canada

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