Research Article: Asynchronous ripple oscillations between left and right hippocampi during slow-wave sleep

Date Published: February 3, 2017

Publisher: Public Library of Science

Author(s): Claudio Villalobos, Pedro E. Maldonado, José L. Valdés, Stephen D Ginsberg.

http://doi.org/10.1371/journal.pone.0171304

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.

Partial Text

The hippocampus has been widely associated with learning and memory, playing a significant role in navigation in both humans and rodents [1,2]. Anatomically, 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 brain functions in humans [3–5]. Furthermore, the hippocampus seems to show significant levels of compartmentalization of functions, with several studies having identified the left hippocampus to be involved in language processing and sequential organization of choices whereas the right hippocampus predominantly involved in spatial navigation in humans [6–12]. In addition, recent investigations in rodents have revealed unexpected asymmetries between left and right hippocampi at cellular and molecular level [13–16]. All this evidence have contributed to the categorization of spatial memory as a lateralized process within the hippocampus, yet the physiological mechanisms underlying this specialization remain to be elucidated. The stabilization of recently acquired memory traces, a process known as memory consolidation, has been strongly associated with sharp-wave ripple (SWR) complexes and reactivation in the hippocampus [17–20]. The precise mechanism linking memory consolidation and ripple events, high-frequency oscillatory patterns usually present during immobility and slow wave sleep is still unclear however, some studies have suggested that these oscillations could exert their influence through spike-timed dependent plasticity [21–23], thus initiating plastic changes in structures downstream of the hippocampus. This evidence highlights the importance of ripples’ temporal occurrence within the hippocampus in the development of the memory consolidation process.

In this study, 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. These findings suggest that the origin of the majority of ripple events within the hippocampus may be restricted within each hemisphere. Furthermore, the lack of synchronization of these events also suggests the existence of multiple rather than a common driver coordinating the appearance of individual ripple events, with anatomically separated inputs driving these oscillations. If ripple events were trigger by a common driver in both hemispheres, we would have expected a larger number of synchronized events recorded from contra-lateral tetrodes. Our results indicate that this is not the case, even when a wider time window (100ms) was used to analyze event synchrony in order to account for traveling ripples as well as for the temporal differences of local events due to the delays in the cell assemblies recruited for ripple initiation. The identity of the structures/sources triggering ripple events is currently unknown, and further research is needed in order to determine its functionality and location. It is noteworthy to indicate that for this study we detected and analyzed only the fast oscillatory patterns of the LFP (100 – 250Hz) within the SWR complex commonly found in the hippocampus CA1 region. A recent report [31,20] showed that CA1 ripples originated from CA2 region can be found separated from their sharp-wave component, therefore, the conclusions extracted from this study cannot be extrapolated to the sharp-wave component of the SWR complex. Further analysis and experiments should be carried out in order to establish a sharp-wave/ripple synchrony between hemispheres.

 

Source:

http://doi.org/10.1371/journal.pone.0171304

 

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