Neuron
Volume 93, Issue 2, 18 January 2017, Pages 308-314
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Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal Ripple Oscillations in Awake Mice In Vivo

https://doi.org/10.1016/j.neuron.2016.12.018Get rights and content
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Highlights

  • High-resolution synaptic current recording during sharp wave-ripples (SWRs) in vivo

  • Inhibition dominates over excitation during SWRs in the hippocampal CA1 region

  • Phasic inhibition, but not excitation, is phase-locked to individual ripple cycles

  • PV+ interneurons substantially contribute to SWR-associated inhibitory conductance

Summary

Sharp wave-ripple (SWR) oscillations play a key role in memory consolidation during non-rapid eye movement sleep, immobility, and consummatory behavior. However, whether temporally modulated synaptic excitation or inhibition underlies the ripples is controversial. To address this question, we performed simultaneous recordings of excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) and local field potentials (LFPs) in the CA1 region of awake mice in vivo. During SWRs, inhibition dominated over excitation, with a peak conductance ratio of 4.1 ± 0.5. Furthermore, the amplitude of SWR-associated IPSCs was positively correlated with SWR magnitude, whereas that of EPSCs was not. Finally, phase analysis indicated that IPSCs were phase-locked to individual ripple cycles, whereas EPSCs were uniformly distributed in phase space. Optogenetic inhibition indicated that PV+ interneurons provided a major contribution to SWR-associated IPSCs. Thus, phasic inhibition, but not excitation, shapes SWR oscillations in the hippocampal CA1 region in vivo.

Keywords

sharp wave-ripples
in vivo recording
in vivo voltage clamp
EPSCs
IPSCs
hippocampus
CA1 region
network oscillations
PV+ interneurons
GABAergic synapses

Cited by (0)

2

Present address: Department of Speech Language Pathology and Audiology, National Taipei University of Nursing and Health Science, Taipei 11219, Taiwan

3

Present address: Center for Drug Evaluation, Taipei 11557, Taiwan

4

Present address: University of Vienna, Dr. Bohr-Gasse 7, Vienna Biocenter, A-1030 Vienna, Austria

5

Lead Contact