Excitatory and inhibitory synapse reorganization immediately after critical sensory experience in a vocal learner
- University of Zurich/ETH Zurich, Switzerland
- Wellesley College, United States
Abstract
Excitatory and inhibitory synapses are the brain's most abundant synapse types. However, little is known about their formation during critical periods of motor skill learning, when sensory experience defines a motor target that animals strive to imitate. In songbirds, we find that exposure to tutor song leads to elimination of excitatory synapses in HVC (used here as a proper name), a key song generating brain area. A similar pruning is associated with song maturation, because juvenile birds have fewer excitatory synapses, the better their song imitations. In contrast, tutoring is associated with rapid insertion of inhibitory synapses, but the tutoring-induced structural imbalance between excitation and inhibition is eliminated during subsequent song maturation. Our work suggests that sensory exposure triggers the developmental onset of goal-specific motor circuits by increasing the relative strength of inhibition and it suggests a synapse-elimination model of song memorization.
Data availability
We provide all SSEM synaptic density data for Experiments I and II in the Matlab file ssSEM_exp1and2_groupSeperated.mat. We provide all FIBSEM data for Experiment I in the Matlab file FIBSEM_exp1.mat. HVC volume data for Experiment II is provided in the Matlab file HVCvolume_exp2.mat.To reproduce our linear mixed effects analyses, we provide the Matlab function getLME. For example, to reproduce the comparison between synaptic densities in LONG and LONG60 birds, one first needs to load the data: load ssSEM_exp1and2_groupSeperated, then one needs to concatenate the relevant variables: data=vertcat(data_ssSEM_exp1_LONG,data_ssSEM_exp2_TUT60), and finally, one needs to run the function: getLME(data), followed by typing 1 for running the analysis for asymmetric synapses for example. All Matlab files can be retrieved from https://www.research-collection.ethz.ch/handle/20.500.11850/285394, DOI 10.3929/ethz-b-000285394.
Article and author information
Author details
Richard HR Hahnloser
Funding
Swiss National Science Foundation (31003A_127024)
- Richard HR Hahnloser
ETH Zürich Foundation (Project 2015-48 3)
- Richard HR Hahnloser
Swiss National Science Foundation (31003A_156976)
- Richard HR Hahnloser
Swiss National Science Foundation (ZKOZ3_160663)
- Richard HR Hahnloser
European Research Council (FP7/2007-2013 / ERC Grant AdG 268911)
- Richard HR Hahnloser
Susan Todd Horton Class of 1910 Trust
- Houda G Khaled
Hubel Neuroscience Summer Research Fellowship
- Houda G Khaled
Seven College Conference Junior Year Abroad Award
- Houda G Khaled
Five Faculty Awards from Wellesley College
- Sharon MH Gobes
National Institutes of Health (R15HD085143)
- Sharon MH Gobes
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experimental procedures were in accordance with the Veterinary Office of the Canton of Zurich (207-2013).
Copyright
© 2018, Huang et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Excitatory and inhibitory synapse reorganization immediately after critical sensory experience in a vocal learner
eLife 7:e37571.
https://doi.org/10.7554/eLife.37571
