Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP
Article first published online: 25 JAN 2010
Copyright © 2009 Wiley-Liss, Inc.
Volume 21, Issue 4, pages 354–373, April 2011
How to Cite
Bourne, J. N. and Harris, K. M. (2011), Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus, 21: 354–373. doi: 10.1002/hipo.20768
- Issue published online: 25 JAN 2010
- Article first published online: 25 JAN 2010
- Manuscript Accepted: 30 NOV 2009
- NIH. Grant Numbers: NS21184, NS33574, EB002170.
Vol. 23, Issue 10, 969–970, Article first published online: 11 JUN 2013
- serial section transmission electron microscopy;
- 3D reconstruction;
- dendritic spine;
- hippocampal slice;
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.