Distinct Transmitter Release Properties Determine Differences in Short-Term Plasticity at Functional and Silent Synapses

Abstract

Recent evidence suggests that functional and silent synapses are not only postsynaptically different but also presynaptically distinct. The presynaptic differences may be of functional importance in memory formation because a proposed mechanism for long-term potentiation is the conversion of silent synapses into functional ones. However, there is little direct experimentally evidence of these differences. We have investigated the transmitter release properties of functional and silent Schaffer collateral synapses and show that on the average functional synapses displayed a lower percentage of failures and higher excitatory postsynaptic current (EPSC) amplitudes than silent synapses at +60 mV. Moreover, functional but not silent synapses show paired-pulse facilitation (PPF) at +60 mV and thus presynaptic short-term plasticity will be distinct in the two types of synapse. We examined whether intraterminal endoplasmic reticulum Ca2+ stores influenced the release properties of these synapses. Ryanodine (100 μM) and thapsigargin (1 μM) increased the percentage of failures and decreased both the EPSC amplitude and PPF in functional synapses. Caffeine (10 mM) had the opposite effects. In contrast, silent synapses were insensitive to both ryanodine and caffeine. Hence we have identified differences in the release properties of functional and silent synapses, suggesting that synaptic terminals of functional synapses express regulatory molecular mechanisms that are absent in silent synapses.

Cholinergic-Mediated IP3-Receptor Activation Induces Long-Lasting Synaptic Enhancement in CA1 Pyramidal Neurons

“…5A), consistent with the lack of a presynaptic contribution. However, during the initial presynaptic inhibition, there was a transient increase in the PPR (data not shown) reflecting the decrease in the release probability as a result of the activation of presynaptic mAChRs (Fernandez de Sevilla et al, 2002;Cabezas and Buno, 2006).…”

Silent Synapses in Developing Rat Nucleus Tractus Solitarii Have AMPA Receptors

“…This protocol has been used previously to estimate the fraction of pure NMDAR synapses (Isaac et al, 1997;Hohnke et al, 2000;Bottjer, 2005;Cabezas and Buno, 2006). At P0, minimal stimulations evoked a mixture of successes and failures in NTS neurons ( Fig.…”

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

“…This protocol elicits all-or-none single-fiber EPSC responses (sfEPSC) [32]. Figure 5 shows sfEPSC that were recorded in DMX and dm-cNTS neurons.…”

“…Rather, such short-term plasticity plays an essential role in determining the cut-off frequency of a synapse, thus limiting the content of information flow at a specific pathway [32,30,42-45]. The most important consequences of the higher PPR of type I DMX neurons are that these neurons are capable of being activated by repeated high-frequency afferent inputs up to a few tens of Hz in a manner that contrasts with that of the dm-cNTS and type II DMX neurons that filter out high-frequency components and can be sufficiently excited only by low (~0.1 Hz) frequency inputs.…”

“…This value represents the reduction in the EPSC amplitude after the 5th stimulus when stimulated at 20 Hz compared to stimulation at 0.1 Hz. In order to record postsynaptic responses evoked by an action potential generated in a single fiber located precisely at the place of stimulation, we performed "minimal" bipolar stimulation [32]. The stimulation pipettes were fabricated from theta capillaries (WPI) with similar pulling procedures to those used to fabricate patch electrodes (tip diameter, ~1-2 μm), which were filled with ACSF and placed on the TS (see e.g., Figure 5).…”