Abstract

Neuronal oscillations in the rat hippocampus relate to both memory and locomotion, raising the question of how these cognitive and behavioral correlates interact to determine the oscillatory network state of this region. Here, rats freely locomoted while performing an object-location task designed to test hippocampus-dependent spatial associative memory. Rhythmic activity in theta, beta, slow gamma, and fast gamma frequency ranges were observed in both action potentials and local field potentials (LFPs) across four main hippocampal subregions. Several patterns of LFP oscillations corresponded to overt behavior (e.g., increased dentate gyrus-CA3 beta coherence during stationary moments and CA1-subiculum theta coherence during locomotion). In comparison, slow gamma (∼40Hz) oscillations throughout the hippocampus related most specifically to object-location associative memory encoding rather than overt behavior. The results help to untangle how hippocampal oscillations relate to both memory and motion and single out slow gamma oscillations as a distinguishing correlate of spatial associative memory.

Highlights

  • Neuronal oscillations reflect rhythmic fluctuations of transmembrane ion currents summed across neurons (Buzsaki et al, 2012)

  • The results reveal that slow gamma oscillations across the major hippocampal subregions mark an oscillatory network state of effective associative memory encoding

  • To ask how hippocampal network activity related to both memory and overt behavior, action potentials and local field potentials (LFPs) were recorded simultaneously from dentate gyrus (DG), CA3, CA1, and subiculum in six rats as the animals performed a novel object recognition memory task that probed the rats’ memory for objects and objects’ locations

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Summary

Introduction

Neuronal oscillations reflect rhythmic fluctuations of transmembrane ion currents summed across neurons (Buzsaki et al, 2012) This rhythmicity modulates the timing—and the efficacy—of synaptic transmission and synaptic plasticity (Huerta and Lisman, 1995; Hyman et al, 2003; Orr et al, 2001; Zarnadze et al, 2016), shaping interactions between populations of neurons within and across brain regions (Engel et al, 2001; Fries, 2015; Singer, 1999; Varela et al, 2001). An important question is how the patterns of oscillations in the hippocampus distinguish object exploration from other behaviors during spatial navigation and whether these oscillatory patterns relate to encoding object-location associative memories or more narrowly reflect the act of exploration

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