Theta and gamma hippocampal–neocortical oscillations during the episodic-like memory test: impairment in epileptogenic rats

Abstract

Cortical oscillations in different frequency bands have been shown to be intimately involved in exploration of environment and cognition. Here, the local field potentials in the hippocampus, the medial prefrontal cortex (mPFC), and the medial entorhinal cortex (mEC) were recorded simultaneously in rats during the execution of the episodic-like memory task. The power of hippocampal theta (~4-10 Hz), slow gamma (~25-50 Hz), and fast gamma oscillations (~55-100 Hz) was analyzed in all structures examined. Particular attention was paid to the theta coherence between three mentioned structures. The modulation of the power of gamma rhythms by the phase of theta cycle during the execution of the episodic-like memory test by rats was also closely studied. Healthy rats and rats one month after kainate-induced status epilepticus (SE) were examined. Paroxysmal activity in the hippocampus (high amplitude interictal spikes), excessive excitability of animals, and the death of hippocampal and dentate granular cells in rats with kainate-evoked SE were observed, which indicated the development of seizure focus in the hippocampus (epileptogenesis). One month after SE, the rats exhibited a specific impairment of episodic memory for the what-where-when triad: unlike healthy rats, epileptogenic SE animals did not identify the objects during the test. This impairment was associated with the changes in the characteristics of theta and gamma rhythms and specific violation of theta coherence and theta/gamma coupling in these structures in comparison with the healthy animals. We believe that these disturbances in the cortical areas play a role in episodic memory dysfunction in kainate-treated animals. These findings can shed light on the mechanisms of cognitive deficit during epileptogenesis.

A dynamical computational model of theta generation in hippocampal circuits to study theta-gamma oscillations during neurostimulation

“…These conflicting results may originate from differences in experimental protocols and from a poor understanding of their biophysical underpinnings. Among such mechanisms, the involvement of hippocampal theta oscillations (4)(5)(6)(7)(8)(9)(10)(11)(12) and their interactions with higher-frequency gamma oscillations (30-120 Hz) in memory-related processes has been reported in multiple studies (Lisman et al, 2005;de Almeida et al, 2007;Lega et al, 2012;Lin et al, 2017;Malkov et al, 2021;Abbaspoor et al, 2022). Moreover, the modulation of gamma oscillations by the phase of theta oscillations in hippocampal circuits, a phenomenon termed theta-gamma phase-amplitude coupling (PAC), correlates with the efficacy of memory encoding and retrieval (Jensen and Colgin, 2007;Tort et al, 2009;Canolty and Knight, 2010;Axmacher et al, 2010;Fell and Axmacher, 2011;Lisman and Jensen, 2013;Lega et al, 2016).…”