Theta (6–12 Hz) field potentials and the synchronization (coherence) of these potentials present neural network indices of hippocampal physiology. Theta signals within the hippocampal formation may reflect alterations in sensorimotor integration, the flow of sensory input, and/or distinct cognitive operations. While the power and coherence of theta signals vary across lamina within the septal hippocampus, limited information is available about variation in these indices across the septotemporal (long) or areal axis. The present study examined the relationship of locomotor speed to theta indices at CA1 and dentate gyrus (DG) sites across the septotemporal axis as well as in the entorhinal cortex. Our findings demonstrate the dominant relationship of speed to theta indices at septal sites. This relationship diminished systematically with distance from the septal pole of the hippocampus at both CA1 and DG sites. While theta power at entorhinal sites varied in relation to speed, there were no differences across the areal axis of the entorhinal cortex. Locomotor speed was also related to changes in theta coherence along the septotemporal axis as well as between the hippocampus and entorhinal cortex. In addition to the speed-related variation, we observed a decrease in theta power at more temporal hippocampal sites over repeated behavioral testing within a single day that was not observed at septal sites. The results outline a dynamic and distributed pattern of network activity across the septotemporal axis of the hippocampus in relation to locomotor speed and recent past experience.

Hippocampal theta (6-10 Hz) and gamma (25-50 Hz and 65-100 Hz) local field potentials reflect the dynamic synchronization of inputs impinging upon hippocampal neurons. Novel experience is known to engage hippocampal physiology and promote successful encoding. Does novelty synchronize or desynchronize theta and/or gamma frequency inputs across the septotemporal (long) axis of the hippocampus? The present study tested the hypothesis that a novel spatial environment would alter theta power and coherence across the long axis. We compared theta and gamma local field potential signals at individual (power) and millimeter distant electrode pairs (coherence) within the dentate gyrus (DG) and CA1 region while rats navigated a runway 1) in a familiar environment, 2) with a modified path in the same environment and 3) in a novel space. Locomotion in novel space was related to increases in theta and gamma power at most CA1 and DG sites. The increase in theta and gamma power was concurrent with an increase in theta and gamma coherence across the long axis of CA1; however, there was a significant decrease in theta coherence across the long axis of the DG. These findings illustrate significant shifts in the synchrony of entorhinal, CA3 and/or neuromodulatory afferents conveying novel spatial information to the dendritic fields of CA1 and DG targets across the long axis of the hippocampus. This shift suggests that the entire theta/gamma-related input to the CA1 network, and likely output, receives and conveys a more coherent message in response to novel sensory experience. Such may contribute to the successful encoding of novel sensory experience.

Memories of events that occur often are sensitive to interference from memories of similar events. Proactive interference plays an important and often unexamined role in memory testing for spatially and temporally unique events (“episodes”). Ketamine (NMDA receptor antagonist) treatment in humans and other mammals induces a constellation of cognitive deficits, including impairments in working and episodic memory. We examined the effects of the ketamine (2.5–100 mg/kg) on the acquisition, retrieval, and retention of memory in a delayed-match-to-place radial water maze task that can be used to assess proactive interference. Ketamine (2.5–25 mg/kg, i.p.) given 20 min before the sample trial, impaired encoding. The first errors made during the test trial were predominantly to arms located spatially adjacent to the goal arm, suggesting an established albeit weakened representation. Ketamine (25–100 mg/kg) given immediately after the sample trial had no effect on retention. Ketamine given before the test trial impaired retrieval. First errors under the influence of ketamine were predominantly to the goal location of the previous session. Thus, ketamine treatment promoted proactive interference. These memory deficits were not state dependent, because ketamine treatment at both encoding and retrieval only increased the number of errors during the test session. These data demonstrate the competing influence of distinct memory representations during the performance of a memory task in the rat. Furthermore, they demonstrate the subtle disruptive effects of the NMDA antagonist ketamine on both encoding and retrieval. Specifically, ketamine treatment disrupted retrieval by promoting proactive interference from previous episodic representations.

Theta (6–12 Hz) rhythmicity in the local field potential (LFP) reflects a clocking mechanism that brings physically isolated neurons together in time, allowing for the integration and segregation of distributed cell assemblies. Variation in the theta signal has been linked to locomotor speed, sensorimotor integration as well as cognitive processing. Previously, we have characterized the relationship between locomotor speed and theta power and how that relationship varies across the septotemporal (long) axis of the hippocampus (HPC). The current study investigated the relationship between whole body acceleration, deceleration and theta indices at CA1 and dentate gyrus (DG) sites along the septotemporal axis of the HPC in rats. Results indicate that whole body acceleration and deceleration predicts a significant amount of variability in the theta signal beyond variation in locomotor speed. Furthermore, deceleration was more predictive of variation in theta amplitude as compared to acceleration as rats traversed a linear track. Such findings highlight key variables that systematically predict the variability in the theta signal across the long axis of the HPC. A better understanding of the relative contribution of these quantifiable variables and their variation as a function of experience and environmental conditions should facilitate our understanding of the relationship between theta and sensorimotor/cognitive functions.

Hippocampal theta has been related to locomotor speed, attention, anxiety, sensorimotor integration and memory among other emergent phenomena. One difficulty in understanding the function of theta is that the hippocampus (HPC) modulates voluntary behavior at the same time that it processes sensory input. Both functions are correlated with characteristic changes in theta indices. The current review highlights a series of studies examining theta local field potential (LFP) signals across the septotemporal or longitudinal axis of the HPC. While the theta signal is coherent throughout the entirety of the HPC, the amplitude, but not the frequency, of theta varies significantly across its three-dimensional expanse. We suggest that the theta signal offers a rich vein of information about how distributed neuronal ensembles support emergent function. Further, we speculate that emergent function across the long axis varies with respect to spatiotemporal scale. Thus, septal hippocampus processes details of the proximal spatiotemporal environment while more temporal aspects process larger spaces and wider time-scales. The degree to which emergent functions are supported by the synchronization of theta across the septotemporal axis is an open question. Our working model is that theta synchrony serves to bind ensembles representing varying resolutions of spatiotemporal information at interdependent septotemporal areas of the HPC. Such synchrony and cooperative interactions along the septotemporal axis likely support memory formation and subsequent consolidation and retrieval.