Differential Activity-Dependent Increase in Synaptic Inhibition and Parvalbumin Interneuron Recruitment in Dentate Granule Cells and Semilunar Granule Cells

Milad Afrasiabi, Akshay Gupta, Huaying Xu, Bogumila Swietek, Vijayalakshmi Santhakumar

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Strong inhibitory synaptic gating of dentate gyrus granule cells (GCs), attributed largely to fast-spiking parvalbumin interneurons (PV-INs), is essential to maintain sparse network activity needed for dentate dependent behaviors. However, the contribution of PV-INs to basal and input-driven sustained synaptic inhibition in GCs and semilunar granule cells (SGCs), a sparse morphologically distinct dentate projection neuron subtype, is currently unknown. In studies conducted in hippocampal slices from mice, we find that although basal IPSCs are more frequent in SGCs and optical activation of PV-INs reliably elicited IPSCs in both GCs and SGCs, optical suppression of PV-INs failed to reduce IPSC frequency in either cell type. Amplitude and kinetics of IPSCs evoked by perforant path (PP) activation were not different between GCs and SGCs. However, the robust increase in sustained polysynaptic IPSCs elicited by paired afferent stimulation was lower in SGCs than in simultaneously recorded GCs. Optical suppression of PV-IN selectively reduced sustained IPSCs in SGCs but not in GCs. These results demonstrate that PV-INs, while contributing minimally to basal synaptic inhibition in both GCs and SGCs in slices, mediate sustained feedback inhibition selectively in SGCs. The temporally selective blunting of activity-driven sustained inhibitory gating of SGCs could support their preferential and persistent recruitment during behavioral tasks.

Original languageEnglish (US)
Pages (from-to)1090-1103
Number of pages14
JournalJournal of Neuroscience
Volume42
Issue number6
DOIs
StatePublished - Feb 9 2022
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Medicine(all)

Keywords

  • GABA
  • dentate gyrus
  • feedback inhibition
  • parvalbumin
  • semilunar granule cell

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