Neuron
Volume 79, Issue 6, 18 September 2013, Pages 1208-1221
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Article
A Cortico-Hippocampal Learning Rule Shapes Inhibitory Microcircuit Activity to Enhance Hippocampal Information Flow

https://doi.org/10.1016/j.neuron.2013.07.001Get rights and content
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Highlights

  • CCK interneurons mediate strong feedforward inhibition of CA1 pyramidal neurons

  • Corticohippocampal activity suppresses perisomatic inhibition from CCK interneurons

  • The reduced inhibition boosts intrahippocampal excitation of CA1 pyramidal neurons

  • Cortical inputs thus act as a long-term gate of hippocampal information flow

Summary

How does coordinated activity between distinct brain regions implement a set of learning rules to sculpt information processing in a given neural circuit? Using interneuron cell-type-specific optical activation and pharmacogenetic silencing in vitro, we show that temporally precise pairing of direct entorhinal perforant path (PP) and hippocampal Schaffer collateral (SC) inputs to CA1 pyramidal cells selectively suppresses SC-associated perisomatic inhibition from cholecystokinin (CCK)-expressing interneurons. The CCK interneurons provide a surprisingly strong feedforward inhibitory drive to effectively control the coincident excitation of CA1 pyramidal neurons by convergent inputs. Thus, in-phase cortico-hippocampal activity provides a powerful heterosynaptic learning rule for long-term gating of information flow through the hippocampal excitatory macrocircuit by the silencing of the CCK inhibitory microcircuit.

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Present Address: Max Planck Florida Institute for Neuroscience, Jupiter, FL 33458, USA