Hippocampal non-theta state: The “Janus face” of information processing

Abstract

The vast majority of studies on hippocampal rhythms have been conducted on animals or humans in situations where their attention was focused on external stimuli or solving cognitive tasks. These studies formed the basis for the idea that rhythmical activity coordinates the work of neurons during information processing. However, at rest, when attention is not directed to external stimuli, brain rhythms do not disappear, although the parameters of oscillatory activity change. What is the functional load of rhythmical activity at rest? Hippocampal oscillatory activity during rest is called the non-theta state, as opposed to the theta state, a characteristic activity during active behavior. We dedicate our review to discussing the present state of the art in the research of the non-theta state. The key provisions of the review are as follows: (1) the non-theta state has its own characteristics of oscillatory and neuronal activity; (2) hippocampal non-theta state is possibly caused and maintained by change of rhythmicity of medial septal input under the influence of raphe nuclei; (3) there is no consensus in the literature about cognitive functions of the non-theta-non-ripple state; and (4) the antagonistic relationship between theta and delta rhythms observed in rodents is not always observed in humans. Most attention is paid to the non-theta-non-ripple state, since this aspect of hippocampal activity has not been investigated properly and discussed in reviews.

Theta oscillons in behaving rats

“…5B). As the animal moves out of the θ -state, noise amplifies by an order of magnitude and decouples from the locomotion, indicating an onset of a “non-theta” state [67], in which the amplitude of θ -oscillon drops by about 50 − 80% (Fig. 5B, see also [68]).…”

Disruption of awake sharp-wave ripples does not affect memorization of locations in repeated-acquisition spatial memory tasks

“…We believe that this might be a good candidate neural mechanism required for the short-term rehearsal. Furthermore, one can speculate that also in primates the key neural activity required for good short-term retention of new information coincides rather with the ‘theta’ than with the ‘non-theta’ brain states - generally associated with SWRs ( Mysin and Shubina, 2023 ). This hypothesis is in line with a recent report showing the importance of medial-temporal lobe theta oscillations for human short-term retention in a visual task ( Kragel et al, 2021 ).…”

“…Promoting the ‘theta’ brain state might be an interesting way to improve memory retention over a short timescale. Alternatively, more research could be done on the ‘non-theta-non-ripple state’ as this also remains an understudied domain both in rodents and primates ( Mysin and Shubina, 2023 ).…”

Modeling the contribution of theta-gamma coupling to sequential memory, imagination, and dreaming

“…Although this is a plausible hypothesis, several recent data support a different scenario, i.e., that theta oscillation in the hippocampus emerges from a complex interplay between local mechanisms and an external rhythmic drive ( Etter et al, 2023 ; Mysin and Shubina, 2023 ; Robinson et al, 2023 ). In this regard, particular emphasis has been given to a role by the medial septum (MS).…”