Sharp wave/ripple network oscillations and learning-associated hippocampal maps

Jozsef Csicsvari David Dupret Articles on similar topics can be found in the following collections Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service rstb.royalsocietypublishing.org Review One contribution of 24 to a Theo Murphy Meeting Issue Space in the brain: cells, circuits, codes and cognition. Subject Areas: neuroscience Author for correspondence: Jozsef Csicsvari e-mail: Sharp wave/ripple network oscillations and learning-associated hippocampal maps Jozsef Csicsvari1 and David Dupret2 1IST Austria, Am Campus 1, 3400 Klosterneuburg, Austria 2MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK Sharp wave/ripple (SWR, 150 250 Hz) hippocampal events have long been postulated to be involved in memory consolidation. However, more recent work has investigated SWRs that occur during active waking behaviour: findings that suggest that SWRs may also play a role in cell assembly strengthening or spatial working memory. Do such theories of SWR function apply to animal learning? This review discusses how general theories linking SWRs to memory-related function may explain circuit mechanisms related to rodent spatial learning and to the associated stabilization of new cognitive maps. 1. Introduction There is increasing evidence suggesting that network oscillatory patterns play major roles in the memory-related function of the hippocampus. Among these, the so-called sharp wave/ripple (SWR) patterns have drawn special attention because these are linked to memory consolidation. These SWR events are best marked by the transiently occurring 150 250 Hz ripple oscillations near the CA1 pyramidal cell layer [1 3]. They are usually present in inactive behavioural periods such as waking immobility and slow-wave sleep but they also occur during consummatory behaviour, grooming and brief interruptions in locomotion [4,5]. The possible role of SWRs originated from theories suggesting a specific role of the hippocampus in memory consolidation during sleep [6]. According to this theory, the hippocampus transiently stores recently learned memory traces, which are spontaneously reactivated during sleep. This process could enable the transfer of memory traces to extra-hippocampal locations, where they are ultimately stored. Because large number of neurons synchronously fire action potentials together during SWRs, it has been suggested that this network state is optimal for the transfer of these memory traces to extra-hippocampal locations [7,8]. Therefore, it has been suggested that during SWRs, previous waking neuronal activity is reactivated, which represent memory traces that might undergo a process of consolidation. Indeed, a large number of studies have confirmed the reactivation of waking neuronal activity patterns during sleep, particularly during SWRs [5,9 12]. It was also shown that the disruption of sleep SWRs through electrical stimulation leads to mild spatial memory impairments [13,14], although it is unclear whether SWR-coupled electrical stimulation caused plastic changes of synaptic weights in these experiments. More recent work focused on the role of SWRs that occur during active waking periods, suggesting additional roles for SWRs beyond memory consolidation. It was proposed that the overlay of sensory-driven activity with the underlying network burst during these SWRs enables plastic processes to strengthen cell assemblies [5]. However, because the blockade of waking SWRs impairs spatial working memory [15], they are suggested to represent recall of memory traces that could be used for working memory. This review discusses work suggesting roles for SWRs in learning and associated mnemonic functions from rodent experiments. It argues that the & 2013 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. stabilization of cognitive maps in the hippocampus and beyond may be an underlying process through which spatial memories might be stabilized and examines the possibility that SWRs might facilitate such map stabilization. 2. Contribution of sharp wave/ripples in spatial learning and map stabilization The simplest form of spatial learning is related to the ability of the animal to recognize the degree of familiarity of an environment, which is closely related to the recall of stable hippocampal place maps. This ability to detect place-associated novelty has been suggested to involve the hippocampus [16,17]. Moreover, the ability of animals to recognize changes of spatial configuration, for example the misplacement of local object cues, requires the hippocampus [18]. Place cells reorganize rapidly when the animal is placed into a new environment: typically new place fields appear, existing place fields disappear or move to different locations (for review: [19]). This remapping of place fields leads to the formation of an entirely new representation of that environment. Importantly, this map is reinstated later, when the animal is placed back into the same environment. The successful reinstatement of new hippocampal maps requires their stabilization, a process which is N-methyl-D-aspartate (NMDA) receptor-dependent and requires protein synthesis [20,21], and long-term potentiation induction triggers the remapping of hippocampal place fields [22]. Hence, the stabilization of newly formed maps in a novel environment is closely related to the ability of the animal to recognize this environment and this process requires circuit reorganization involving NMDA-dependent synaptic plasticity. In order to examine whether SWRs play a role in the spatial recognition of entire environments, one needs to explore whether SWRs occurring during sleep or waking periods promote the stabilization of new place maps. Since, many studies have clearly indicated that sleep promotes memory consolidation [23,24], sleep SWRs are likely candidates for place map stabilization. Although a direct link has not been established between SWR-related reactivation and map stabilization, the reactivation of neuronal patterns representing novel environments supports such a role. In comparing the reactivation of familiar and novel environments, it was revealed that reactivation of newly formed maps is stronger. Moreover, the time period necessary for the animal to spend at a given location so that this location is reliably reactivated is similar to that needed for the stabilization of place fields [25,26]. How might reactivation during SWRs contribute to the stabilization of maps? SWR events have been shown to enable synaptic potentiation in vivo between those cells that are active within the same SWRs [27]. (...truncated)