Running speed affects theta (6-10 Hz) oscillations, the most prominent rhythm in the rat hippocampus. Many reports have found a strong positive correlation between locomotion speed and the amplitude and frequency of theta oscillations. However, less is known about how other rhythms such as delta (0.5-4 Hz) and gamma (25-100 Hz) are affected, and how consecutive runs impact oscillatory activity in hippocampal networks. Here, we investigated whether the successive execution of short-term runs modulates local field potentials (LFPs) in the rat hippocampus. To do this, we trained Long-Evans rats to perform voluntary 15-s runs at 30 cm/s on a treadmill placed on the central stem of an eight-shape maze, in which they subsequently performed a spatial alternation task. We bilaterally recorded CA1 LFPs while rats executed at least 35 runs on the treadmillmaze apparatus. Within running periods, we observed progressive increases in delta band power along with decreases in the power of the theta and gamma bands across runs. Concurrently, the inter-hemispheric phase coherence in the delta band significantly increased, while in the theta and gamma bands exhibited no changes. Delta power and inter-hemispheric coherence correlated better with the trial number than with the actual running speed. We observed no significant differences in running speed, head direction, nor in spatial occupancy across runs. Our results thus show that consecutive treadmill runs at the same speed positively modulates the power and coherence of delta oscillations in the rat hippocampus.

Episodic memory depends on the recollection of spatial and temporal aspects of past experiences in which the hippocampus plays a critical role. Studies on hippocampal lesions in rodents have shown that dentate gyrus (DG) and CA3 are necessary to detect object displacement in memory tasks. However, the understanding of real-time oscillatory activity underlying memory discrimination of subtle and pronounced displacements remains elusive. Here, we chronically implanted microelectrode arrays in adult male Wistar rats to record network oscillations from DG, CA3, and CA1 of the dorsal hippocampus while animals executed an object recognition task of high and low spatial displacement tests (HD: 108 cm, and LD: 54 cm, respectively). Behavioral analysis showed that the animals discriminate between stationary and displaced objects in the HD but not LD conditions. To investigate the hypothesis that theta and gamma oscillations in different areas of the hippocampus support discrimination processes in a recognition memory task, we compared epochs of object exploration between HD and LD conditions as well as displaced and stationary objects. We observed that object exploration epochs were accompanied by strong rhythmic activity in the theta frequency (6–12 Hz) band in the three hippocampal areas. Comparison between test conditions revealed higher theta band power and higher theta-gamma phase-amplitude coupling in the DG during HD than LD conditions. Similarly, direct comparison between displaced and stationary objects within the HD test showed higher theta band power in CA3 during exploration of displaced objects. Moreover, the discrimination index between displaced and stationary objects directly correlated with CA1 gamma band power in epochs of object exploration. We thus conclude that theta and gamma oscillations in the dorsal hippocampus support the successful discrimination of object displacement in a recognition memory task.

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.