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.

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 are affected, and how consecutive runnings impact oscillatory activity in hippocampal networks. Here, we investigated whether the successive execution of short-term runnings modulates local field potentials (LFPs) in the rat hippocampus. To do this, we trained Long-Evans rats to perform voluntary 15-s runnings 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 laps on the treadmill-maze apparatus. Within running periods, we observed progressive increases in delta band power (0.5-4 Hz) along with gradual decreases in theta band power across laps. A significant negative correlation in the power of these bands was observed along runnings. In addition, we found an increase in the interhemispheric phase coherence in the delta band, with no significant changes in the theta band. Our results thus show a differential modulation of delta and theta in CA1 LFPs while rats perform successive treadmill runnings at the same speed.

The ability to form different neural representations for similar inputs is a central process of episodic memory. Although the dorsal dentate gyrus and CA3 have been indicated as important in this phenomenon, the neuronal circuits underlying spatiotemporal memory processing with different levels of spatial similarity are still elusive. In this study, we measured the expression of the immediate early gene c‐Fos to evaluate brain areas activated when rats recalled the temporal order of object locations in a task, with either high or low levels of spatial interference. Animals showed spatiotemporal memory in both conditions once they spent more time exploring the older object locations relative to the more recent ones. We found no difference in the levels of c‐Fos expression between high and low spatial interference. However, the levels of c‐Fos expression in CA2 positively correlated with the discrimination index in the low spatial interference condition. More importantly, functional network connectivity analysis revealed a wider and more interconnected neuronal circuit in conditions of high than in low spatial interference. Our study advances the understanding of brain networks recruited in episodic memory with different degrees of spatial similarity.

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 significance: Theta 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.

Recent studies described 2–4 Hz oscillations in the hippocampus of rats performing stationary locomotion on treadmills and other apparatus. Since the 2–4 Hz rhythm shares common features with theta (5–12 Hz) oscillations—such as a positive amplitude-running speed relationship and modulation of spiking activity—many have questioned whether these rhythms are related or independently generated. Here, we analyzed local field potentials and spiking activity from the dorsal CA1 of rats executing a spatial alternation task and running for ~15 s in a wheel during the intertrial intervals both before and after muscimol injection into the medial septum. We observed remarkable 4-Hz oscillations during wheel runs, which presented amplitude positively correlated with running speed. Surprisingly, the amplitude of 4-Hz and theta oscillations were inversely related. Medial septum inactivation abolished hippocampal theta but preserved 4-Hz oscillations. It also affected the entrainment of pyramidal cells and interneurons by 4-Hz rhythmic activity. In all, these results dissociate the underlying mechanism of 4-Hz and theta oscillations in the rat hippocampus.