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Cereb Cortex. 2016 May;26(5):2105-2114. doi: 10.1093/cercor/bhv033. Epub 2015 Mar 10.

Frequency-Dependent Gating of Hippocampal-Neocortical Interactions.

Author information

1
Centre for Cognitive and Neural Systems, Edinburgh Neuroscience, University of Edinburgh, Edinburgh EH8 9JZ, UK.
2
Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas, Universidad Miguel Hernández, Sant Joan d'Alacant 03550, Spain.

Abstract

How and where hippocampal-neocortical interactions required for memory formation take place is a major issue of current research. Using a combined in vivo functional magnetic resonance imaging/electrophysiology approach, we have investigated whether specific frequencies of CA3 neuronal activation, inducing different forms of short-term plasticity at CA1 synapses, contribute to differential activity propagation in brain-wide networks connected to the hippocampus. We report that localized activation of CA3 neurons in dorsal hippocampus produced activity propagation within the hippocampal formation, including the subiculum and entorhinal cortex, which increased monotonically with frequency to a maximum at 20-40 Hz. However, robust extrahippocampal propagation was seen specifically at theta-beta frequencies (10-20 Hz), reaching a network of midline neocortical and mesolimbic structures. Activation in those regions correlated with a frequency-dependent facilitation of spiking activity recorded in CA1. These results provide a mechanistic link between the dynamic properties of short-term plasticity in the efferent synapses of CA3 neurons in CA1 and activity propagation in brain-wide networks, and identify polysynaptic information channels segregated in the frequency domain.

KEYWORDS:

activity propagation; beta oscillations; electrophysiology; fMRI; gating; hippocampus; memory; neocortex; rat; short-term plasticity; theta oscillations

PMID:
25761637
DOI:
10.1093/cercor/bhv033
[Indexed for MEDLINE]

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