Sharp-Wave Ripples Orchestrate the Induction of Synaptic Plasticity during Reactivation of Place Cell Firing Patterns in the Hippocampus

• Published in: Cell reports (Cambridge) Vol. 14; no. 8; pp. 1916 - 1929
• Main Authors: Sadowski, Josef H.L.P., Jones, Matthew W., Mellor, Jack R.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.03.2016; Cell Press; Elsevier
• Subjects: Action Potentials - physiology; Animals; CA1 Region, Hippocampal - cytology; CA1 Region, Hippocampal - physiology; CA3 Region, Hippocampal - cytology; CA3 Region, Hippocampal - physiology; Dendrites - physiology; Dendrites - ultrastructure; Electrodes, Implanted; Long-Term Potentiation - physiology; Male; Memory, Long-Term - physiology; Nerve Net - physiology; Nerve Net - ultrastructure; Patch-Clamp Techniques; Pyramidal Cells - cytology; Pyramidal Cells - physiology; Rats; Rats, Wistar; Rest - physiology; Sleep - physiology; Stereotaxic Techniques; Synapses - physiology; Synapses - ultrastructure
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2016.01.061

Place cell firing patterns reactivated during hippocampal sharp-wave ripples (SWRs) in rest or sleep are thought to induce synaptic plasticity and thereby promote the consolidation of recently encoded information. However, the capacity of reactivated spike trains to induce plasticity has not been directly tested. Here, we show that reactivated place cell firing patterns simultaneously recorded from CA3 and CA1 of rat dorsal hippocampus are able to induce long-term potentiation (LTP) at synapses between CA3 and CA1 cells but only if accompanied by SWR-associated synaptic activity and resulting dendritic depolarization. In addition, we show that the precise timing of coincident CA3 and CA1 place cell spikes in relation to SWR onset is critical for the induction of LTP and predictive of plasticity generated by reactivation. Our findings confirm an important role for SWRs in triggering and tuning plasticity processes that underlie memory consolidation in the hippocampus during rest or sleep. [Display omitted] •Reactivated place cell firing patterns can induce LTP in the hippocampus•Sharp-wave ripples are required for the induction of LTP•Dendritic depolarization during sharp-wave ripples is required for LTP•The timing of place cell firing within sharp-wave ripples controls LTP induction Sadowski et al. show that reactivation of neuronal firing patterns during sleep induces synaptic plasticity, providing a mechanism for the observation that memories are consolidated during sleep.