Mathieu Letellier et al in Plos Biology
Differential role of pre and postsynaptic neurons in the activity-dependent control of synaptic strengths across dendrites
Letellier M, Levet F, Thoumine O, Goda Y (2019) Differential role of pre- and postsynaptic neurons in the activity-dependent control of synaptic strengths across dendrites. PLoS Biol 17(6): e2006223. https://doi.org/10.1371/journal.pbio.2006223
Mathieu Letellier1,2,3,#, Florian Levet2-6, Olivier Thoumine2,3 and Yukiko Goda1,7,#
1 RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, JAPAN
2 Interdisciplinary Institute for Neuroscience, University of Bordeaux, Bordeaux, France.
3 InterdisciplinaryInstitute for Neuroscience, Centre National de la Recherche Scientifique (CNRS) UMR 5297, Bordeaux, France.
4 Bordeaux Imaging Center, University of Bordeaux, Bordeaux, France.
5 Bordeaux Imaging Center, CNRS UMS 3420, Bordeaux, France.
6 Bordeaux Imaging Center, INSERM US04, Bordeaux, France.
7 Present affiliation: RIKEN Center for Brain Science, 2-1 Hirosawa, Wako, Saitama 351-0198, JAPAN
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.