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Brain Struct Funct. 2017 Nov;222(8):3677-3690. doi: 10.1007/s00429-017-1427-x. Epub 2017 May 2.

Differential surface density and modulatory effects of presynaptic GABAB receptors in hippocampal cholecystokinin and parvalbumin basket cells.

Author information

1
Institute for Integrative Neuroanatomy, Neurocure Cluster of Excellence, Charité-Universitätmedizin Berlin, 10115, Berlin, Germany. sbooker@exseed.ed.ac.uk.
2
Centre for Integrative Physiology, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh, EH8 9XE, UK. sbooker@exseed.ed.ac.uk.
3
Institute of Physiology, University of Freiburg, Freiburg, Germany.
4
Institute for Integrative Neuroanatomy, Neurocure Cluster of Excellence, Charité-Universitätmedizin Berlin, 10115, Berlin, Germany.
5
Department of Anatomy, Graduate School of Medicine, Hokkaido University, Sapporo, 0608638, Japan.
6
BIOSS Centre for Biological Signalling Studies, University of Freiburg, Freiburg, Germany.
7
Institute for Integrative Neuroanatomy, Neurocure Cluster of Excellence, Charité-Universitätmedizin Berlin, 10115, Berlin, Germany. imre.vida@charite.de.

Abstract

The perisomatic domain of cortical neurons is under the control of two major GABAergic inhibitory interneuron types: regular-spiking cholecystokinin (CCK) basket cells (BCs) and fast-spiking parvalbumin (PV) BCs. CCK and PV BCs are different not only in their intrinsic physiological, anatomical and molecular characteristics, but also in their presynaptic modulation of their synaptic output. Most GABAergic terminals are known to contain GABAB receptors (GABABR), but their role in presynaptic inhibition and surface expression have not been comparatively characterized in the two BC types. To address this, we performed whole-cell recordings from CCK and PV BCs and postsynaptic pyramidal cells (PCs), as well as freeze-fracture replica-based quantitative immunogold electron microscopy of their synapses in the rat hippocampal CA1 area. Our results demonstrate that while both CCK and PV BCs contain functional presynaptic GABABRs, their modulatory effects and relative abundance are markedly different at these two synapses: GABA release is dramatically inhibited by the agonist baclofen at CCK BC synapses, whereas a moderate reduction in inhibitory transmission is observed at PV BC synapses. Furthermore, GABABR activation has divergent effects on synaptic dynamics: paired-pulse depression (PPD) is enhanced at CCK BC synapses, but abolished at PV BC synapses. Consistent with the quantitative differences in presynaptic inhibition, virtually all CCK BC terminals were found to contain GABABRs at high densities, but only 40% of PV BC axon terminals contain GABABRs at detectable levels. These findings add to an increasing list of differences between these two interneuron types, with implications for their network functions.

KEYWORDS:

Electron microscope; GABAergic interneurons; Presynaptic inhibition; Short-term plasticity; Synaptic transmission

PMID:
28466358
PMCID:
PMC5676818
DOI:
10.1007/s00429-017-1427-x
[Indexed for MEDLINE]
Free PMC Article

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