Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

Abstract

Pyramidal cells in piriform cortex receive excitatory inputs from two different sources that are segregated onto adjacent segments of their apical dendrites. The present studies show that excitatory postsynaptic potentials (EPSPs) evoked by primary olfactory tract afferents that terminate on distal apical segments display paired shock facilitation whereas ESPSs evoked by intrinsic association fibers that terminate on proximal apical segments do not. An ultrastructural comparison of the presynaptic elements of these two fiber systems has revealed that the facilitating olfactory tract afferent synapses have a much lower packing density of synaptic vesicles than do the nonfacilitating association fiber synapses. Further, a search of the literature has revealed that where both morphological and physiological data are available for the same synapses, this same correlation appears to apply. We propose a hypothesis to account for this correlation based on synaptic vesicles to buffer internal calcium and the biochemical characteristics of preterminal calcium-dependent mechanisms affecting the number of vesicles available for release.At many synapses, the second of an identical pair of appropriately timed presynaptic activations evokes a larger excitatory postsynaptic potential (EPSP) than the first (1-4). This synaptic property, termed paired shock facilitation, has been demonstrated in numerous peripheral and central nervous system synapses. However, there are also synapses that do not facilitate. The factors underlying this difference in the physiological characteristics of different synapses are as yet unknown, but presumably a fundamental mechanism regulating neurotransmitter release is involved. We report here the existence of a system that appears to be well suited for study of the mechanism of paired shock facilitation. Using in vitro brain slices of olfactory (piriform) cortex, we have found that the apical dendrites of single pyramidal cells are contacted by facilitating and nonfacilitating synapses with each type spatially segregated from the other and arising from different fiber systems. Specifically, EPSPs evoked by primary olfactory tract afferents that terminate on distal apical dendritic segments display paired shock facilitation, whereas EPSPs evoked by intrinsic association fibers that terminate on proximal apical segments do not (see Fig. 1). Previous ultrastructural studies comparing the presynaptic elements of these two fiber systems showed that the facilitating olfactory tract afferent synapses have a much lower packing density of synaptic vesicles than do the nonfacilitating association fiber synapses. Further, a search of the literature has revealed that where both morphological and physiological data are available, this same correlation appears to apply for other excitatory synapses. We therefore propose a hypothesis that may account for this correlation based on the ability of synaptic vesicles to buffer internal calcium and therefore affect the ability of subsequent vesicles to be mobi...

Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses

“…Murthy et al (1997) find that the lower release probability boutons exhibited the largest amount of paired pulse facilitation. This observation is in agreement with the finding of Bower and Haberly (1986) that a class of smaller boutons have greater facilitation. Although the relationship between the number of docked vesicles and release probability remains to be established at individual synapses, the data in Figure 6 indicate that the hypothesis is a tenable one.…”

Age-Dependent and Selective Impairment of Long-Term Potentiation in the Anterior Piriform Cortex of Mice Lacking the Fragile X Mental Retardation Protein

“…A second difference between piriform ASSN synapses and hippocampal CA1 synapses is their paired-pulse characteristics. CA1 synapses exhibit facilitation (Creager et al, 1980), whereas piriform ASSN synapses exhibit depression (Bower and Haberly, 1986). The mechanism responsible and significance of these differences are not clear.…”

“…One stimulation electrode (S1) was positioned rostral to the recording electrode and activated the ASSN fibers orthodromically; the other (S2) was placed caudal to the recording electrode and activated a separate population of ASSN synapses via antidromic activation of caudally directed fibers and orthodromic activation of feedback fibers. Laminar profiles and paired-pulse stimulation were used to distinguish between ASSN and LOT synapses as described previously (Bower and Haberly, 1986;Jung et al, 1990a,b) and to optimally position electrodes in each slice tested. All slices from each animal were tested before experiments, and one or two slices exhibiting the largest ASSN field potentials were selected for study.…”

Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex

“…Previous work using both extracellular (Haberly, 1973) and intracellular recordings (Bower and Haberly, 1986;Hasselmo and Bower, 1990) has shown paired-pulse facilitation of EPSPs after stimulation of LOT, but not layer Ib, inputs to layer II neurons. This agrees with our findings for SP cells, but not for SL cells (Fig.…”