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Neuron. 2017 Mar 8;93(5):1213-1226.e5. doi: 10.1016/j.neuron.2017.02.017.

Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling.

Author information

1
MTA-SZTE "Momentum" Oscillatory Neuronal Networks Research Group, Department of Physiology, University of Szeged, Szeged 6720, Hungary; New York University Neuroscience Institute, New York University, New York, NY 10016, USA.
2
MTA-SZTE "Momentum" Oscillatory Neuronal Networks Research Group, Department of Physiology, University of Szeged, Szeged 6720, Hungary.
3
Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, FL 32610, USA; Department of Biomedical Engineering, University of Florida, Gainesville, FL 32611, USA.
4
MTA-SZTE "Momentum" Oscillatory Neuronal Networks Research Group, Department of Physiology, University of Szeged, Szeged 6720, Hungary; New York University Neuroscience Institute, New York University, New York, NY 10016, USA. Electronic address: drberenyi@gmail.com.
5
New York University Neuroscience Institute, New York University, New York, NY 10016, USA; Center for Neural Science, New York University, New York, NY 10016, USA. Electronic address: gyorgy.buzsaki@nyumc.org.

Abstract

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:

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

PMID:
28279355
PMCID:
PMC5373668
DOI:
10.1016/j.neuron.2017.02.017
[Indexed for MEDLINE]
Free PMC Article

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