LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite

Abstract

Structural remodelling of synapses and formation of new synaptic contacts has been postulated as a possible mechanism underlying the late phase of long-term potentiation (LTP), a form of plasticity which is involved in learning and memory. Here we use electron microscopy to analyse the morphology of synapses activated by high-frequency stimulation and identified by accumulated calcium in dendritic spines. LTP induction resulted in a sequence of morphological changes consisting of a transient remodelling of the postsynaptic membrane followed by a marked increase in the proportion of axon terminals contacting two or more dendritic spines. Three-dimensional reconstruction revealed that these spines arose from the same dendrite. As pharmacological blockade of LTP prevented these morphological changes, we conclude that LTP is associated with the formation of new, mature and probably functional synapses contacting the same presynaptic terminal and thereby duplicating activated synapses.

Neuronal and morphological bases of cognitive decline in aged rhesus monkeys

“…The frequencies of single-synapse boutons, multiplesynapse boutons (MSBs), and boutons with no apparent synaptic contacts (nonsynaptic boutons, NSBs) in the OML were determined using serial section electron microscopy. MSBs are presynaptic boutons synaptically connected to more than one dendritic spine and potentially act as a morphological substrate to increase coupling between presynaptic and postsynaptic neurons (Harris 1995;Toni et al 1999;Geinisman et al 2001;Yankova et al 2001). MSBs are implicated in structural plasticity and hippocampus-dependent associative learning Toni et al 1999;Geinisman et al 2001).…”

“…MSBs are presynaptic boutons synaptically connected to more than one dendritic spine and potentially act as a morphological substrate to increase coupling between presynaptic and postsynaptic neurons (Harris 1995;Toni et al 1999;Geinisman et al 2001;Yankova et al 2001). MSBs are implicated in structural plasticity and hippocampus-dependent associative learning Toni et al 1999;Geinisman et al 2001). While there are no age effects on bouton density or average size in the DG OML, the proportion of NSBs is doubled in aged compared to young monkeys (Hara et al 2011), suggesting that aging results in a lower turnover or higher retraction of spines, leading to a greater proportion of boutons that fail to make or maintain a synaptic contact.…”

Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells

“…These time points were chosen based on our previous observations indicating a marked remodeling of excitatory CA1 synapses and the formation of new spines during the first hour following theta-burst stimulation (Toni et al, 1999(Toni et al, , 2001 or brief OGD episode (Jourdain et al, 2002). We took special care to correctly identify pyramidal cells in the CA1 region of organotypic hippocampal slice cultures.…”

Homers regulate drug-induced neuroplasticity: Implications for addiction

“…Experience-dependent changes in spine shape, size and number contribute to alterations in synaptic strength, in part by regulating connective opportunities [192][193][194] and neuronal morphology, as well as the ability to induce morphological changes within dendritic spines depends upon an intact cytoskeleton [197]. Increases in spine size, emergence of new spines and the perforation of the PSD are all thought to reflect spine head splitting and synapse duplication, contributing to a long-lasting enhancement of synaptic efficacy [e.g., [192][193][194][195][196][197].…”