Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks

Abstract

Hippocampal firing is organized in theta sequences controlled by internal memory processes and by external sensory cues, but how these computations are coordinated is not fully understood. Although theta activity is commonly studied as a unique coherent oscillation, it is the result of complex interactions between different rhythm generators. Here, by separating hippocampal theta activity in three different current generators, we found epochs with variable theta frequency and phase coupling, suggesting flexible interactions between theta generators. We found that epochs of highly synchronized theta rhythmicity preferentially occurred during behavioral tasks requiring coordination between internal memory representations and incoming sensory information. In addition, we found that gamma oscillations were associated with specific theta generators and the strength of theta-gamma coupling predicted the synchronization between theta generators. We propose a mechanism for segregating or integrating hippocampal computations based on the flexible coordination of different theta frameworks to accommodate the cognitive needs.

A model of the CA1 field rhythms

“…Subsequent experimental research using optogenetics methods showed our correctness. When the PV basket neurons were stimulated in the CA3 field, the theta rhythm power in the CA1 field decreased (López-Madrona et al, 2020). Our prediction about the role of the perforant path in theta rhythm generation, made in our previous work (Mysin et al, 2019), was also confirmed.…”

“…Our prediction about the role of the perforant path in theta rhythm generation, made in our previous work (Mysin et al, 2019), was also confirmed. The perforant path input does not play a role in theta rhythm generation, as confirmed by experiments with signal suppression from the entorhinal cortex (López-Madrona et al, 2020). Although the results (López-Madrona et al, 2020) directly contradict the results of previous studies (Middleton & McHugh, 2016).…”

The Theta Rhythm of the Hippocampus: From Neuronal and Circuit Mechanisms to Behavior

“…Note phase locking between both rhythms (θ-γ coupling) and the amplitude modulation of the intracellular γ; modified from Penttonen et al (1998). Jutras et al, 2009;López-Madrona et al, 2020). These authors suggest that successful memory performance requires coupling of γ rhythms to particular phases of the hippocampal θ (termed θ-γ coupling).…”

“…During these active states, γ oscillations are prominent and also participate in memory formation (Buzsaki and Draguhn, 2004 ). γ oscillations are prominent in the entorhinal–hippocampal network during a variety of memory tasks in different species (Montgomery and Buzsáki, 2007 ; Sederberg et al, 2007 ; Jutras et al, 2009 ; López-Madrona et al, 2020 ). These authors suggest that successful memory performance requires coupling of γ rhythms to particular phases of the hippocampal θ (termed θ–γ coupling).…”

Rapid coordination of effective learning by the human hippocampus

“…This interpretation is consonant with shifts in hippocampal states from pronounced theta oscillations during novel exploration, to theta-free epochs marked with sharp-wave ripple events (35) thought to support replay of prior experience (36). Eye-movement tracking therefore provided a marker of memory processing with the requisite temporal precision to resolve the behavioral ramifications of dynamic changes in hippocampal activity reflecting encoding versus retrieval that occur rapidly over a brief interval (34, 37), even during a single episode during which learning occurs for a novel stimulus.…”