Accelerated redevelopment of vocal skills is preceded by lasting reorganization of the song motor circuitry
- Max Planck Institute for Ornithology, Germany
- Institut Hospital del Mar d'Investigacions Mèdiques (IMIM), Spain
- Eötvös Loránd University, Hungary
- University of Southern Denmark, Denmark
- University of Antwerp, Belgium
Abstract
Complex motor skills take considerable time and practice to learn. Without continued practice the level of skill performance quickly degrades, posing a problem for the timely utilization of skilled motor behaviors. Here we quantified the recurring development of vocal motor skills and the accompanying changes in synaptic connectivity in the brain of a songbird, while manipulating skill performance by consecutively administrating and withdrawing testosterone. We demonstrate that a songbird with prior singing experience can significantly accelerate the re-acquisition of vocal performance. We further demonstrate that an increase in vocal performance is accompanied by a pronounced synaptic pruning in the forebrain vocal motor area HVC, a reduction that is not reversed when birds stop singing. These results provide evidence that lasting synaptic changes in the motor circuitry are associated with the savings of motor skills, enabling a rapid recovery of motor performance under environmental time constraints.
Data availability
SQL data of extracted song features for each individual have been deposited in Dryad.Further source data files have been provided for Figure 2, Figure 2 -figure supplement 1, Figure 3, Figure 3 -figure supplement 1, Figure 4, Figure 4 -figure supplement 1, Figure 4 -figure supplement 2, Figure 5.
-
Data from: Vocal motor experiences consolidate the vocal motor circuitry and accelerate future vocal skill developmentDryad Digital Repository, doi:10.5061/dryad.kb814nh.
Article and author information
Author details
Funding
Horizon 2020 Framework Programme (701660)
- Michiel Vellema
National Research, Development and Innovation Office Hungary (K-115970)
- Sándor Zsebők
Interuniversity Attraction Poles (IUAP-NIMI-P6/38)
- Annemie Van der Linden
Max-Planck-Gesellschaft
- Manfred Gahr
National Research, Development and Innovation Office Hungary (K-129215)
- Sándor Zsebők
National Research, Development and Innovation Office Hungary (PD-115730)
- Sándor Zsebők
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Experimental procedures were conducted according to the guidelines of the Federation of European Animal Science Associations (FELASA) and approved by the Ethical Committee on animal experiments of the University of Antwerp (protocol number: 2007-14) .
Copyright
© 2019, Vellema 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
-
- 1,158
- views
-
- 181
- 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)
Accelerated redevelopment of vocal skills is preceded by lasting reorganization of the song motor circuitry
eLife 8:e43194.
https://doi.org/10.7554/eLife.43194
Further reading
-
- Neuroscience
Biological memory networks are thought to store information by experience-dependent changes in the synaptic connectivity between assemblies of neurons. Recent models suggest that these assemblies contain both excitatory and inhibitory neurons (E/I assemblies), resulting in co-tuning and precise balance of excitation and inhibition. To understand computational consequences of E/I assemblies under biologically realistic constraints we built a spiking network model based on experimental data from telencephalic area Dp of adult zebrafish, a precisely balanced recurrent network homologous to piriform cortex. We found that E/I assemblies stabilized firing rate distributions compared to networks with excitatory assemblies and global inhibition. Unlike classical memory models, networks with E/I assemblies did not show discrete attractor dynamics. Rather, responses to learned inputs were locally constrained onto manifolds that ‘focused’ activity into neuronal subspaces. The covariance structure of these manifolds supported pattern classification when information was retrieved from selected neuronal subsets. Networks with E/I assemblies therefore transformed the geometry of neuronal coding space, resulting in continuous representations that reflected both relatedness of inputs and an individual’s experience. Such continuous representations enable fast pattern classification, can support continual learning, and may provide a basis for higher-order learning and cognitive computations.
-
- Neuroscience
The central amygdala (CeA) has emerged as an important brain region for regulating both negative (fear and anxiety) and positive (reward) affective behaviors. The CeA has been proposed to encode affective information in the form of valence (whether the stimulus is good or bad) or salience (how significant is the stimulus), but the extent to which these two types of stimulus representation occur in the CeA is not known. Here, we used single cell calcium imaging in mice during appetitive and aversive conditioning and found that majority of CeA neurons (~65%) encode the valence of the unconditioned stimulus (US) with a smaller subset of cells (~15%) encoding the salience of the US. Valence and salience encoding of the conditioned stimulus (CS) was also observed, albeit to a lesser extent. These findings show that the CeA is a site of convergence for encoding oppositely valenced US information.
