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

• Published in: Neuron (Cambridge, Mass.) Mass.), 2021-03, Vol.109 (6), p.1029-1039.e8
• Main Authors: Kropff, Emilio, Carmichael, James E., Moser, Edvard I., Moser, May-Britt
• Format: Article
• Language: English
• Subjects: Acceleration; Animals; border cells; Cortex (entorhinal); entorhinal cortex; Entorhinal Cortex - physiology; Firing pattern; Fourier transforms; grid cells; Grid Cells - physiology; head direction cells; Hippocampus; Hippocampus - physiology; Male; Navigation behavior; Rats; Rats, Long-Evans; Running; Running - physiology; space; Spatial Navigation - physiology; speed; speed cells; theta rhythm; Theta Rhythm - physiology; Theta rhythms
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2021.01.017

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. •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 Kropff et al. find that the frequency of the theta rhythm, one of the most prominent oscillations in the mammalian brain, does not vary with running speed as previously thought. Instead, it responds with high temporal precision to positive (but not negative) acceleration.