Abstract
Parvalbumin- (PV-) containing basket cells constitute perisomatic GABAergic inhibitory interneurons innervating principal cells at perisomatic area, a strategic location that allows them to efficiently control the output and synchronize oscillatory activity at gamma frequency (30–90 Hz) oscillations. This oscillatory activity can convert into higher frequency epileptiform activity, and therefore could play an important role in the generation of seizures. However, the role of endogenous modulators of seizure activity, such as Neuropeptide Y (NPY), has not been fully explored in at PV input and output synapses. Here, using selective optogenetic activation of PV cells in the hippocampus, we show that seizures, induced by rapid kindling (RK) stimulations, enhance gamma-aminobutyric acid (GABA) release from PV cells onto dentate gyrus (DG) granule cells (GC). However, PV-GC synapses did not differ between controls and kindled animals in terms of GABA release probability, short-term plasticity and sensitivity to NPY. Kinetics of gamma-aminobutyric acid A (GABA-A) mediated currents in postsynaptic GC were also unaffected. When challenged by repetitive high-frequency optogenetic stimulations, PV synapses in kindled animals responded with enhanced GABA release onto GC. These results unveil a mechanism that might possibly contribute to the generation of abnormal synchrony and maintenance of epileptic seizures.
Highlights
Perisomatic inhibition comprises a variety of different GABAergic cell types that innervate target cells in the region that includes the cell soma, axon initial segment and proximal dendrites
We have previously shown, using the same protocol of rapid kindling (RK) stimulations, FIGURE 3 | Neuropeptide Y (NPY) reduces the frequency of spontaneous excitatory post-synaptic currents recorded from PV cells. (A) Biocytin staining showing the axonal arborization of a PV cell, localized to the granule cell layer (GCL) and hilus
The main finding of this study is that synchronous gammaaminobutyric acid (GABA) release from the ensembles of PV cell onto granule cells (GC) is not altered by NPY in the kindled hippocampus, suggesting that NPY does not directly regulate inhibitory inputs from multiple PV cells to GC in these conditions
Summary
Perisomatic inhibition comprises a variety of different GABAergic cell types that innervate target cells in the region that includes the cell soma, axon initial segment and proximal dendrites. The most abundant perisomatic inhibitory GABAergic cell types are the so-called basket cells. There are two major subpopulations of basket cells in the hippocampus, the parvalbumin (PV-) and the cholecystokinin (CCK-) containing basket cells (Somogyi and Klausberger, 2005). Their location and morphology are similar, their electrical properties and roles in the hippocampal network are remarkably different (Freund and Katona, 2007). PV-basket cells fire high-frequency non-accommodating action potentials, receive three times more local
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