Computer assisted detection of axonal bouton structural plasticity in in vivo time-lapse images
- Northeastern University, United States
- University of Geneva, Switzerland
- École Polytechnique Fédérale de Lausanne, Switzerland
Abstract
The ability to measure minute structural changes in neural circuits is essential for long-term in vivo imaging studies. Here, we propose a methodology for detection and measurement of structural changes in axonal boutons imaged with time-lapse two-photon laser scanning microscopy (2PLSM). Correlative 2PLSM and 3D electron microscopy (EM) analysis, performed in mouse barrel cortex, showed that the proposed method has low fractions of false positive/negative bouton detections (2/0 out of 18), and that 2PLSM-based bouton weights are correlated with their volumes measured in EM (r=0.93). Next, the method was applied to a set of axons imaged in quick succession to characterize measurement uncertainty. The results were used to construct a statistical model in which bouton addition, elimination, and size changes are described probabilistically, rather than being treated as deterministic events. Finally, we demonstrate that the model can be used to quantify significant structural changes in boutons in long-term imaging experiments.
Data availability
-
Data from: Computer assisted detection of axonal bouton structural plasticity in in vivo time-lapse imagesAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
National Institutes of Health (R01 NS091421)
- Armen Stepanyants
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (331003A_153448)
- Anthony Holtmaat
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII3-154453)
- Graham Knott
- Anthony Holtmaat
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (51NF40_158776)
- Anthony Holtmaat
International Foundation for Research in Paraplegia (Chair Alain Rossier)
- Anthony Holtmaat
Air Force Office of Scientific Research (FA9550-15-1-0398)
- Armen Stepanyants
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Eve Marder, Brandeis University, United States
Ethics
Animal experimentation: All experiments were performed according to the guidelines of the Swiss Federal Act on Animal Protection and Swiss Animal Protection Ordinance. The ethics committee of the University of Geneva and the Cantonal Veterinary Office of Geneva, Switzerland (approval code GE/61/17) approved all experiments.
Version history
- Received: June 6, 2017
- Accepted: October 22, 2017
- Accepted Manuscript published: October 23, 2017 (version 1)
- Version of Record published: November 7, 2017 (version 2)
Copyright
© 2017, Gala 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
-
- 2,428
- Page views
-
- 350
- Downloads
-
- 12
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
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)
Computer assisted detection of axonal bouton structural plasticity in in vivo time-lapse images
eLife 6:e29315.
https://doi.org/10.7554/eLife.29315
Further reading
-
- Neuroscience
Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.
-
- Neuroscience
Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.
