Neuron
Volume 93, Issue 5, 8 March 2017, Pages 1213-1226.e5
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Article
Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling

https://doi.org/10.1016/j.neuron.2017.02.017Get rights and content
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Highlights

  • Cooperation of entorhinal and CA3 inputs controls spike timing of hippocampal neurons

  • Phase precession is under dual entorhinal and CA3 control

  • Spike timing in REM and learning depends on the strengths of upstream gamma inputs

  • Feedback inhibition is layer specific and varies within place fields

Summary

Theta-gamma phase coupling and spike timing within theta oscillations are prominent features of the hippocampus and are often related to navigation and memory. However, the mechanisms that give rise to these relationships are not well understood. Using high spatial resolution electrophysiology, we investigated the influence of CA3 and entorhinal inputs on the timing of CA1 neurons. The theta-phase preference and excitatory strength of the afferent CA3 and entorhinal inputs effectively timed the principal neuron activity, as well as regulated distinct CA1 interneuron populations in multiple tasks and behavioral states. Feedback potentiation of distal dendritic inhibition by CA1 place cells attenuated the excitatory entorhinal input at place field entry, coupled with feedback depression of proximal dendritic and perisomatic inhibition, allowing the CA3 input to gain control toward the exit. Thus, upstream inputs interact with local mechanisms to determine theta-phase timing of hippocampal neurons to support memory and spatial navigation.

Keywords

oscillations
phase precession
memory recall
memory encoding
place coding
temporal coding
cross-frequency coupling
phase coupling
inhibition
high-density recordings

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