Within-session dynamics of theta–gamma coupling and high-frequency oscillations during spatial alternation in rat hippocampal area CA1

Abstract

Theta-gamma coupling in the hippocampus is thought to be involved in cognitive processes. A large body of research establishes that the hippocampus plays a crucial role in the organization and maintenance of episodic memory, and that sharp-wave ripples (SWR) contribute to memory consolidation processes. Here, we investigated how the local field potentials in the hippocampal CA1 area adapted along with rats' behavioral changes within a session during a spatial alternation task that included a 1-s fixation and a 1.5-s delay. We observed that, as the session progressed, the duration from fixation onset to nose-poking in the choice hole reduced as well as the number of premature responses during the delay. Parallel with the behavioral transitions, the power of high gamma during the delay period increased whereas that of low gamma decreased later in the session. Furthermore, the strength of theta-gamma modulation later in the session showed significant increase as compared to earlier in the session. Examining SWR during the reward period, we found that the number of SWR events decreased as well as the power in a wide frequency range during SWR events. In addition, the correlation between SWR and gamma oscillations just before SWR events was higher in the earlier trials than in the later trials. Our findings support the notion that the inputs from CA3 and entorhinal cortex play a critical role in memory consolidation as well as in cognitive processes. We suggest that SWR and the inputs from the two areas serve to stabilize the task behavior and neural activities.

Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task

“…There is a growing literature connecting theta–gamma coupling with successful behavioral performance, both in model organisms and in humans. Much of the animal literature is focused on theta–gamma coupling within the hippocampus, which increases during acquisition of item-context associations 19 and correlates with performance in spatial memory 18 and spatial alternation tasks 35 . In human subjects, intra-hippocampal theta–gamma coupling strength correlates with performance on a visual recognition working memory task 17 .…”

Gamma Oscillations Facilitate Effective Learning in Excitatory-Inhibitory Balanced Neural Circuits

“…In the moderate synchronous state, we observed the switching dynamics between asynchronous spiking and synchronous spiking. If the switching frequency is in theta band, it is highly similar to the spindle [ 6 , 53 , 54 ] observed in the hippocampus during sleeping, which has been assumed to relate to memory consolidation. It is also found in an experimental study that U1 snRNA overexpression mice, having weaker gamma oscillation than normal mice due to reduction in inhibition-related proteins, have deficit in learning [ 55 ].…”

Paired Burst Stimulation Causes GABAA Receptor-Dependent Spike Firing Facilitation in CA1 of Rat Hippocampal Slices

“…In various brain regions, HFO is often observed together with low-frequency oscillations, such as theta oscillations (Buzsáki and da Silva, 2012 ). In the hippocampus, gamma-theta interactions are thought to be a crucial computational mechanism for processing neural information (Lisman and Jensen, 2013 ; Nishida et al, 2014 ). Theta oscillations have long been known to play an important role in encoding information in neural circuits (Buzsáki, 2005 ) and in memory consolidation during sleep (Mehta et al, 2002 ).…”