Abstract

Spatial memory, among many other brain processes, shows hemispheric lateralization. Most of the published evidence suggests that the right hippocampus plays a leading role in the manipulation of spatial information. Concurrently in the hippocampus, memory consolidation during sleep periods is one of the key steps in the formation of newly acquired spatial memory traces. One of the most characteristic oscillatory patterns in the hippocampus are sharp-wave ripple (SWR) complexes. Within this complex, fast-field oscillations or ripples have been demonstrated to be instrumental in the memory consolidation process. Since these ripples are relevant for the consolidation of memory traces associated with spatial navigation, and this process appears to be lateralized, we hypothesize that ripple events between both hippocampi would exhibit different temporal dynamics. We tested this idea by using a modified "split-hyperdrive" that allows us to record simultaneous LFPs from both right and left hippocampi of Sprague-Dawley rats during sleep. We detected individual events and found that during sleep periods these ripples exhibited a different occurrence patterns between hemispheres. Most ripple events were synchronous between intra- rather than inter-hemispherical recordings, suggesting that ripples in the hippocampus are independently generated and locally propagated within a specific hemisphere. In this study, we propose the ripples’ lack of synchrony between left and right hippocampi as the putative physiological mechanism underlying lateralization of spatial memory.

Highlights

  • The hippocampus has been widely associated with learning and memory, playing a significant role in navigation in both humans and rodents [1,2]

  • We found for the first time that contrary to the common assumption of brain oscillations being completely synchronous between hemispheres, there are temporal differences in specific high-frequency oscillatory patterns between the left and right hippocampi

  • Our results show that a much greater number of ripple events recorded from the dorsal CA1 region during sleep were synchronized only between ipsi-lateral as compared to contra-lateral recordings

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Summary

Introduction

The hippocampus has been widely associated with learning and memory, playing a significant role in navigation in both humans and rodents [1,2]. The hippocampus is comprised of two indistinguishable parts, located in the medial temporal lobe of each hemisphere. Left and right hippocampi are commonly considered to be functional equivalents and often synchronized. In spite of this vision, there is abundant evidence suggesting the lateralization of PLOS ONE | DOI:10.1371/journal.pone.0171304. Interhippocampal ripple synchrony funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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