Journal Article

Differential role of pre- and postsynaptic neurons in the activity-dependent control of synaptic strengths across dendrites

Thoumine, Olivier, Levet, Florian, Letellier, Mathieu, Goda, Yukiko

2019

Overview

Neurons receive a large number of active synaptic inputs from their many presynaptic partners across their dendritic tree. However, little is known about how the strengths of individual synapses are controlled in balance with other synapses to effectively encode information while maintaining network homeostasis. This is in part due to the difficulty in assessing the activity of individual synapses with identified afferent and efferent connections for a synapse population in the brain. Here, to gain insights into the basic cellular rules that drive the activity-dependent spatial distribution of pre- and postsynaptic strengths across incoming axons and dendrites, we combine patch-clamp recordings with live-cell imaging of hippocampal pyramidal neurons in dissociated cultures and organotypic slices. Under basal conditions, both pre- and postsynaptic strengths cluster on single dendritic branches according to the identity of the presynaptic neurons, thus highlighting the ability of single dendritic branches to exhibit input specificity. Stimulating a single presynaptic neuron induces input-specific and dendritic branchwise spatial clustering of presynaptic strengths, which accompanies a widespread multiplicative scaling of postsynaptic strengths in dissociated cultures and heterosynaptic plasticity at distant synapses in organotypic slices. Our study provides evidence for a potential homeostatic mechanism by which the rapid changes in global or distant postsynaptic strengths compensate for input-specific presynaptic plasticity.

• Publisher: Public Library of Science,Public Library of Science (PLoS)
• Subject: Animals / Axons / Biology and Life Sciences / Brain / Brain slice preparation / CA3 Region, Hippocampal - physiology / Clustering / Connectivity / Dendrites / Dendrites - metabolism / Dendrites - physiology / Dendritic cells / Dendritic structure / Excitatory Postsynaptic Potentials / Funding / Hippocampus / Hippocampus - physiology / Homeostasis / Information processing / Information storage / Interdisciplinary aspects / Life Sciences / Medicine and Health Sciences / Mice / Mice, Inbred C57BL / Models, Neurological / Neuroimaging / Neurons / Neurons - physiology / Neurons and Cognition / Neurosciences / Patch-Clamp Techniques / Physiological aspects / Plastic properties / Plasticity / Presynaptic plasticity / Presynaptic Terminals - physiology / Pyramidal cells / Pyramidal Cells - physiology / Research and Analysis Methods / Scaling / Sensory neurons / Sleep / Social Sciences / Spatial distribution / Synapses / Synapses - physiology / Synaptic Potentials - physiology / Wavelet transforms