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Different GABAergic interneuron types have specific roles in hippocampal function, and anatomical as well as physiological features vary greatly between interneuron classes. Long-term plasticity of interneurons has mostly been studied in unidentified GABAergic cells and is known to be very heterogeneous. Here we tested whether cell type-specific plasticity properties in distinct GABAergic interneuron types might underlie this heterogeneity. We show that long-term potentiation (LTP) and depression (LTD), two common forms of synaptic plasticity, are expressed in a highly cell type-specific manner at glutamatergic synapses onto hippocampal GABAergic neurons. Both LTP and LTD are generated in interneurons expressing parvalbumin (PV+), whereas interneurons with similar axon distributions but expressing cannabinoid receptor-1 show no lasting plasticity in response to the same protocol. In addition, LTP or LTD occurs in PV+ interneurons with different efferent target domains. Perisomatic-targeting PV+ basket and axo-axonic interneurons express LTP, whereas glutamatergic synapses onto PV+ bistratified cells display LTD. Both LTP and LTD are pathway specific, independent of NMDA receptors, and occur at synapses with calcium-permeable (CP) AMPA receptors. Plasticity in interneurons with CP-AMPA receptors strongly modulates disynaptic GABAergic transmission onto CA1 pyramidal cells. We propose that long-term plasticity adjusts the synaptic strength between pyramidal cells and interneurons in a cell type-specific manner and, in the defined CA1 interneurons, shifts the spatial pattern of inhibitory weight from pyramidal cell dendrites to the perisomatic region.

Original publication

DOI

10.1523/JNEUROSCI.3481-09.2010

Type

Journal article

Journal

J Neurosci

Publication Date

27/01/2010

Volume

30

Pages

1337 - 1347

Keywords

Animals, Calcium Signaling, Cell Polarity, Cell Shape, Dendrites, Glutamic Acid, Hippocampus, Immunohistochemistry, Interneurons, Long-Term Potentiation, Long-Term Synaptic Depression, Male, Neural Inhibition, Neuronal Plasticity, Organ Culture Techniques, Parvalbumins, Patch-Clamp Techniques, Presynaptic Terminals, Rats, Rats, Sprague-Dawley, Receptor, Cannabinoid, CB1, Receptors, AMPA, Synapses, Synaptic Transmission, gamma-Aminobutyric Acid