Ripples Make Waves: Binding Structured Activity and Plasticity in Hippocampal Networks

Abstract

Establishing novel episodic memories and stable spatial representations depends on an exquisitely choreographed, multistage process involving the online encoding and offline consolidation of sensory information, a process that is largely dependent on the hippocampus. Each step is influenced by distinct neural network states that influence the pattern of activation across cellular assemblies. In recent years, the occurrence of hippocampal sharp wave ripple (SWR) oscillations has emerged as a potentially vital network phenomenon mediating the steps between encoding and consolidation, both at a cellular and network level by promoting the rapid replay and reactivation of recent activity patterns. Such events facilitate memory formation by optimising the conditions for synaptic plasticity to occur between contingent neural elements. In this paper, we explore the ways in which SWRs and other network events can bridge the gap between spatiomnemonic processing at cellular/synaptic and network levels in the hippocampus.

Rapid, parallel path planning by propagating wavefronts of spiking neural activity

“…These results point to the awake-state SWRs as a possible biological candidate process for parallel mental exploration as required in our model. Moreover, it has been suggested that the SWRs provide optimal conditions for the activation of synaptic plasticity processes, such as STDP (Sadowski et al, 2011)—which, again, is consistent with our assumption that a propagating wave of neural activity should be able to modify connectivity within the network in order to create structured SVFs.…”

Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation

“…Out of the two phenomena, reactivation appears less constrained to specific behavioural paradigms (for example, hippocampal place cell activation while traversing a maze), and more importantly, occurs at a time (just following a new experience) when it could play a pivotal role in consolidation. However, while behavioural state-dependent hippocampal oscillations (such as sharp wave ripples; SPWRs) may support sequential replay, the mechanisms mediating reactivation are still completely unknown17. Critically, it is still unclear whether hippocampal oscillations, replay, or reactivation are required for memory consolidation following novel learning.…”

Synaptic plasticity at the interface of health and disease: New insights on the role of endoplasmic reticulum intracellular calcium stores

“…During the development of the central nervous system for example the interplay of specific molecular gradients, diverse adhesion molecules and activity-dependent synaptic changes allows for the establishment of precise structural and functional connectivity between cells (Tongiorgi, 2008;Budnik and Salinas, 2011;Kerschensteiner, 2013). Similarly, during learning, long-term changes of specific synaptic inputs in distributed networks lead to persistent changes in the behavioral patterns, actions and choices, which are often interpreted as the retention of information, i.e., memory formation (Behrens et al, 2005;Sadowski et al, 2011;Buzsaki and Moser, 2013;Carasatorre and Ramirez-Amaya, 2013;Headley and Pare, 2013). Furthermore, the ability of synapses to adjust their capacity to express synaptic plasticity (Abraham and Bear, 1996;Hulme et al, 2013) or their actual strength in a compensatory/homeostatic manner (Turrigiano, 2012;Vitureira et al, 2012;Davis, 2013) has been recognized to play an important role in stabilizing neuronal networks (c.f., Marder and Goaillard, 2006).…”