Hippocampal delta oscillations entrain neuronal activity, modulate gamma amplitude and convey information about running speed on a treadmill

Abstract

Locomotion has long been associated with rhythmic oscillations in the rat hippocampus. Running speed and acceleration affect the spectral density at the theta (6-10 Hz) and gamma (30-150 Hz) bands and the rhythmic entrainment of neuronal activity. However, less is known about other oscillatory rhythms. Recent studies have shown that oscillatory activity in the delta (1-4 Hz) band also relates to locomotion in stationary conditions, such as running on a treadmill or in a running wheel. To further investigate the effects of stationary running on hippocampal oscillations, we recorded CA1 local field potentials and neuronal activity while rats ran at different speed protocols on a treadmill. We found a remarkable oscillatory activity at 2 Hz that was strongly modulated by running speed. Delta power and peak frequency were highest at the fastest running speed, both in constant and progressively increasing speed protocols. Delta and theta oscillations co-occurred and showed independent relationships in their instantaneous power and frequency. Moreover, the delta phase modulated the amplitude of low-gamma (20-50 Hz) oscillations and the spiking activity of putative pyramidal neurons in a speed-dependent manner. Finally, spectral components in the delta frequency range, but not theta, predicted running speed using a naive Bayes classifier. In summary, our study shows that locomotion-related delta oscillations convey information about stationary running speed and coordinate hippocampal rhythmic activity in a speed-dependent manner. Statement of significanceTheta and gamma oscillations are hallmarks of rhythmic activity in the rat hippocampus during locomotion and exploratory behaviors, but less is known about other oscillatory rhythms. This study shows the emergence of delta ([~]2 Hz) oscillations in the dorsal CA1 of rats running on a treadmill. Locomotion-related delta oscillations are independent of the concomitant theta activity and convey information about running speed. Delta waves modulate low-gamma oscillations and the spiking activity of pyramidal neurons in a speed-dependent way. These results suggest that oscillatory activity in the delta band aids rhythmic coordination during stationary locomotor behaviors.