Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses

Abstract

Short-term synaptic plasticity changes the reliability of transmission during repetitive activation and allows different neuronal ensembles to encode distinct features of action potential trains. Identifying the mechanisms and the locus of expression of such plasticity is essential for understanding neuronal information processing. To determine the quantal parameters and the locus of alterations during short-term plasticity of cortical glutamatergic synapses, EPSCs were evoked in hippocampal oriens-alveus interneurons by CA1 pyramidal cells. The robust short-term facilitation of this connection allowed us to examine the transmission under functionally relevant but widely different release probability (P r ) conditions. Paired whole-cell recordings permitted the functional and post hoc morphological characterization of the synapses. To determine the quantal size (q), the P r , and the number of functional release sites (N F ), two independent quantal analysis methods were used. Light and electron microscopy were performed to identify the number of synaptic junctions (N EM ) between the recorded cells. The mean number of functional release sites (N F(f) ϭ 2.9 Ϯ 0.4; n ϭ 8) as inferred from a simple binomial model with no quantal variance agreed well with the mean of N EM (2.8 Ϯ 0.8; n ϭ 6), but N F(f) never matched N EM when they were compared in individual pairs; however, including quantal variance in the model improved the functional prediction of the structural data. Furthermore, an increased P r (4.8 Ϯ 0.8-fold) fully accounted for the marked short-term facilitation of EPSCs (5.0 Ϯ 0.7-fold), and q was independent of P r . Our results are consistent with the "one-release site, one-vesicle" hypothesis.

Multivesicular Release at Schaffer Collateral–CA1 Hippocampal Synapses

“…This result implied that release was limited to a single vesicle per synapse. Studies examining transmission at other central synapses have bolstered support for UVR (Redman and Walmsley, 1983;Gulyás et al, 1993;Lawrence et al, 2003;Silver et al, 2003;Murphy et al, 2004;Biró et al, 2005). Given that numerous vesicles are ultrastructurally docked at many presynaptic active zones and constitute a readily releasable pool of functional vesicles (Lenzi et al, 1999;Schikorski and Stevens, 2001;XuFriedman et al, 2001), a mechanism must exist to prevent multiple fusion events at synapses limited to UVR.…”

“…At many central synapses, however, release caused by a single presynaptic action potential is limited to one vesicle [univesicular release (UVR)] (Gulyás et al, 1993;Lawrence et al, 2003;Silver et al, 2003;Murphy et al, 2004;Biró et al, 2005;Sargent et al, 2005). Thus far, unifying or predictive characteristics of these synapses have not emerged.…”

Distinctive Quantal Properties of Neurotransmission at Excitatory and Inhibitory Autapses Revealed Using Variance–Mean Analysis

“…Most quantal analysis has focused on the properties of the much more numerous excitatory synapses (Bekkers and Stevens, 1995;Biró et al, 2005;Tyler et al, 2006) (cf. Baldelli et al, 2007, but there is evidence that the release properties of inhibitory synapses are different (Terada et al, 1999;Moulder et al, 2007;Sakaba, 2008).…”

“…A second characteristic of the V-M approach is that, to date, it has been applied largely to excitatory, glutamate-releasing synapses (e.g., Biró et al, 2005;Sargent et al, 2005;Tyler et al, 2006) (cf. Biró et al, 2006).…”

Agykérgi szinapszisok összehasonlító vizsgálata és a szinapszisszám változása posztpartum depresszióban

“…A munkánk azon eredménye, miszerint egy patkány piramissejt aktív zónájához átlagosan egy dokkolt vezikula tartozik, összhangban van a rágcsálókon végzett korábbi eredményekkel (Gulyás et al, 1993;Silver, 2003;Biró et al, 2005), valamint azzal a hipotézissel, miszerint egy aktív zónából egyszerre csak egy vezikula szabadulhat fel (Korn et al, 1982). Ezzel szemben az emberi agykérgi méréseinkből származó adatok szerint ezekre a szinapszisokra multivezikuláris neurotranszmitter felszabadulás jellemző (Rudolph et al, 2015).…”