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.
Highlights
The hippocampal formation flexibly combines computations subserving spatial navigation, driven by external environmental cue stimuli (McNaughton et al, 1983; O’Keefe and Nadel, 1978), and memory processing, dependent on internally generated firing sequences (Pastalkova et al, 2008; Wang et al, 2015)
Using optogenetic tools targeted to CA3 parvalbumin interneurons, we show the specific modulation of the CA3-associated vs. the EC-associated theta generators, demonstrating independent theta oscillations in the hippocampus
Using spatial discrimination techniques to separate LFP sources contributed by different synaptic pathways, based on independent component analysis (ICA, Figure 1—figure supplement 1; Benito et al, 2014; Fernandez-Ruiz and Herreras, 2013; Herreras, 2016; Herreras et al, 2015; Leski et al, 2010; Makarov et al, 2010; Makarova et al, 2011; Ortuno et al, 2019; Schomburg et al, 2014), we dissected three robust components in all subjects (Figure 1; Materials and methods)
Summary
The hippocampal formation flexibly combines computations subserving spatial navigation, driven by external environmental cue stimuli (McNaughton et al, 1983; O’Keefe and Nadel, 1978), and memory processing, dependent on internally generated firing sequences (Pastalkova et al, 2008; Wang et al, 2015). Theoretical and experimental work in the hippocampus have associated the processing of environmental cues and the encoding of memories with the input from the entorhinal cortex (EC) arriving at CA1 at a particular phase of the theta cycle, and the retrieval of memories with the CA3 output to CA1 in a different phase of the cycle
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