COORDINATION OF SIZE AND NUMBER OF EXCITATORY AND INHIBITORY SYNAPSES RESULTS IN A BALANCED STRUCTURAL PLASTICITY ALONG MATURE HIPPOCAMPAL CA1 DENDRITES DURING LTP

By Jennifer N. Bourne, Kristen M. Harris. 2011

325 citations recorded by the source corpus.

Enlargement of dendritic spines and synapses correlates with enhanced synaptic strength during long‐term potentiation (LTP), especially in immature hippocampal neurons. Less clear is the nature of this structural synaptic plasticity on mature hippocampal neurons, and nothing is known about the structural plasticity of inhibitory synapses during LTP. Here the timing and extent of structural synaptic plasticity and changes in local protein synthesis evidenced by polyribosomes were systematically evaluated at both excitatory and inhibitory synapses on CA1 dendrites from mature rats following induction of LTP with theta‐burst stimulation (TBS). Recent work suggests dendritic segments can act as functional units of plasticity. To test whether structural synaptic plasticity is similarly coordinated, we reconstructed from serial section transmission electron microscopy all of the spines and synapses along representative dendritic segments receiving control stimulation or TBS‐LTP. At 5 min after TBS, polyribosomes were elevated in large spines suggesting an initial burst of local protein synthesis, and by 2 h only those spines with further enlarged synapses contained polyribosomes. Rapid induction of synaptogenesis was evidenced by an elevation in asymmetric shaft synapses and stubby spines at 5 min and more nonsynaptic filopodia at 30 min. By 2 h, the smallest synaptic spines were markedly reduced in number. This synapse loss was perfectly counterbalanced by enlargement of the remaining excitatory synapses such that the summed synaptic surface area per length of dendritic segment was constant across time and conditions. Remarkably, the inhibitory synapses showed a parallel synaptic plasticity, also demonstrating a decrease in number perfectly counterbalanced by an increase in synaptic surface area. Thus, TBS‐LTP triggered spinogenesis followed by loss of small excitatory and inhibitory synapses and a subsequent enlargement of the remaining synapses by 2 h. These data suggest that dendritic segments coordinate structural plasticity across multiple synapses and maintain a homeostatic balance of excitatory and inhibitory inputs through local protein‐synthesis and selective capture or redistribution of dendritic resources. ©2010 Wiley‐Liss, Inc.

Subfields: Cellular and Molecular Neuroscience, Electrical and Electronic Engineering

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Citations in the corpus

The temporal paradox of Hebbian learning and homeostatic plasticity (2017, background): “dritic locality is consistent with work on local or branch specific conservation of total synaptic conductance [106, 111].”
Inhibitory synaptic plasticity: spike timing-dependence and putative network function (2013, background): “In this light, a dendritic, local regulation of excitatory and inhibitory synapses should exist and be actively maintained during synaptic plasticity (Liu, 2004; Liu et al., 2007; Bourne and Harris, 2011).”
Heterosynaptic structural plasticity on local dendritic segments of hippocampal CA1 neurons (2014, background): “…studies have shown that LTP-inducing theta-burst stimuli lead to increased spine sizes and decreased spine densities in the hippocampus (Bourne and Harris, 2011) and motor skill training leads to increased numbers of multiple-synapse boutons and decreased size of neighboring spines in…”
Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation (2013, background): “In a healthy brain, the balance between excitatory and inhibitory synapses is dynamically regulated and changes in excitatory and inhibitory synapses often occur in a coordinated fashion (Liu, 2004; Bourne and Harris, 2011; Chen et al., 2012).”
Nanoconnectomic upper bound on the variability of synaptic plasticity (2015, background): “…the skewed shape of the frequency histograms, and the number of synapses per unit of volume (Figures 1–3), are consistent with previous observations (Harris and Stevens, 1989; Schikorski and Stevens, 1997; Sorra et al., 2006; Bourne and Harris, 2011; Bourne et al., 2013; Bell et al., 2014).”