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.
Metrics
-
- 11,960
- views
-
- 438
- downloads
-
- 15
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Excitatory and inhibitory synapse reorganization immediately after critical sensory experience in a vocal learner
eLife 7:e37571.
https://doi.org/10.7554/eLife.37571
Further reading
-
- Neuroscience
By influencing calcium homeostasis, local protein synthesis and the endoplasmic reticulum, a small protein called Rab10 emerges as a crucial cytoplasmic regulator of neuropeptide secretion.
-
- Neuroscience
The infralimbic cortex (IL) is essential for flexible behavioral responses to threatening environmental events. Reactive behaviors such as freezing or flight are adaptive in some contexts, but in others a strategic avoidance behavior may be more advantageous. IL has been implicated in avoidance, but the contribution of distinct IL neural subtypes with differing molecular identities and wiring patterns is poorly understood. Here, we study IL parvalbumin (PV) interneurons in mice as they engage in active avoidance behavior, a behavior in which mice must suppress freezing in order to move to safety. We find that activity in inhibitory PV neurons increases during movement to avoid the shock in this behavioral paradigm, and that PV activity during movement emerges after mice have experienced a single shock, prior to learning avoidance. PV neural activity does not change during movement toward cued rewards or during general locomotion in the open field, behavioral paradigms where freezing does not need to be suppressed to enable movement. Optogenetic suppression of PV neurons increases the duration of freezing and delays the onset of avoidance behavior, but does not affect movement toward rewards or general locomotion. These data provide evidence that IL PV neurons support strategic avoidance behavior by suppressing freezing.
