Non-Hebbian long-term potentiation of inhibitory synapses in the thalamus

Andrea Rahel Sieber, Rogier Min, Thomas Nevian

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31 Citations (Scopus)

Abstract

The thalamus integrates and transmits sensory information to the neocortex. The activity of thalamocortical relay (TC) cells is modulated by specific inhibitory circuits. Although this inhibition plays a crucial role in regulating thalamic activity, little is known about long-term changes in synaptic strength at these inhibitory synapses. Therefore, we studied long-term plasticity of inhibitory inputs to TC cells in the posterior medial nucleus of the thalamus by combining patch-clamp recordings with two-photon fluorescence microscopy in rat brain slices. We found that specific activity patterns in the postsynaptic TC cell induced inhibitory long-term potentiation (iLTP). This iLTP was non-Hebbian because it did not depend on the timing between presynaptic and postsynaptic activity, but it could be induced by postsynaptic burst activity alone. iLTP required postsynaptic dendritic Ca(2+) influx evoked by low-threshold Ca(2+) spikes. In contrast, tonic postsynaptic spiking from a depolarized membrane potential (-50 mV), which suppressed these low-threshold Ca(2+) spikes, induced no plasticity. The postsynaptic dendritic Ca(2+) increase triggered the synthesis of nitric oxide that retrogradely activated presynaptic guanylyl cyclase, resulting in the presynaptic expression of iLTP. The dependence of iLTP on the membrane potential and therefore on the postsynaptic discharge mode suggests that this form of iLTP might occur during sleep, when TC cells discharge in bursts. Therefore, iLTP might be involved in sleep state-dependent modulation of thalamic information processing and thalamic oscillations.

Original languageEnglish
Pages (from-to)15675-85
Number of pages11
JournalJournal of neuroscience
Volume33
Issue number40
DOIs
Publication statusPublished - 2 Oct 2013

Keywords

  • Action Potentials/physiology
  • Animals
  • Calcium/metabolism
  • Excitatory Postsynaptic Potentials/physiology
  • Long-Term Potentiation/physiology
  • Neocortex/physiology
  • Neural Inhibition/physiology
  • Neurons/physiology
  • Patch-Clamp Techniques
  • Rats
  • Rats, Wistar
  • Synapses/physiology
  • Synaptic Transmission/physiology
  • Thalamus/physiology

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