Single bursts of individual granule cells functionally rearrange feedforward inhibition

M. Neubrandt, Viktor János Oláh, János Brunner, Endre Levente Marosi, Ivan Soltesz, J. Szabadics

Research output: Contribution to journalArticle

Abstract

The sparse single-spike activity of dentate gyrus granule cells (DG GCs) is punctuated by occasional brief bursts of 3–7 action potentials. It is well-known that such presynaptic bursts in individual mossy fibers (MFs; axons of granule cells) are often able to discharge postsynaptic CA3 pyramidal cells due to powerful short-term facilitation. However, what happens in the CA3 network after the passage of a brief MF burst, before the arrival of the next burst or solitary spike, is not understood. Because MFs innervate significantly more CA3 interneurons than pyramidal cells, we focused on unitary MF responses in identified interneurons in the seconds-long postburst period, using paired recordings in rat hippocampal slices. Single bursts as short as 5 spikes in < 30 ms in individual presynaptic MFs caused a sustained, large increase (tripling) in the amplitude of the unitary MF-EPSCs for several seconds in ivy, axo-axonic/chandelier and basket interneurons. The postburst unitary MF-EPSCs in these feedforward interneurons reached amplitudes that were even larger than the MF-EPSCs during the bursts in the same cells. In contrast, no comparable postburst enhancement of MF-EPSCs could be observed in pyramidal cells or nonfeedforward interneurons. The robust postburst increase in MF-EPSCs in feedforward interneurons was associated with significant shortening of the unitary synaptic delay and large downstream increases in disynaptic IPSCs in pyramidal cells. These results reveal a new cell type-specific plasticity that enables even solitary brief bursts in single GCs to powerfully enhance inhibition at the DG-CA3 interface in the seconds-long time-scales of interburst intervals.

Original languageEnglish
Pages (from-to)1711-1724
Number of pages14
JournalJournal of Neuroscience
Volume38
Issue number7
DOIs
Publication statusPublished - Feb 14 2018

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Interneurons
Pyramidal Cells
Dentate Gyrus
Action Potentials
Axons

Keywords

  • Burst firing
  • Feedforward inhibition
  • Hippocampus

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Single bursts of individual granule cells functionally rearrange feedforward inhibition. / Neubrandt, M.; Oláh, Viktor János; Brunner, János; Marosi, Endre Levente; Soltesz, Ivan; Szabadics, J.

In: Journal of Neuroscience, Vol. 38, No. 7, 14.02.2018, p. 1711-1724.

Research output: Contribution to journalArticle

Neubrandt, M. ; Oláh, Viktor János ; Brunner, János ; Marosi, Endre Levente ; Soltesz, Ivan ; Szabadics, J. / Single bursts of individual granule cells functionally rearrange feedforward inhibition. In: Journal of Neuroscience. 2018 ; Vol. 38, No. 7. pp. 1711-1724.
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