Skip to main content

Umbrella menu

  • SfN.org
  • eNeuro
  • The Journal of Neuroscience
  • Neuronline
  • BrainFacts.org

Main menu

  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Latest Articles
    • Issue Archive
    • Editorials
    • Research Highlights
  • TOPICS
    • Cognition and Behavior
    • Development
    • Disorders of the Nervous System
    • History, Teaching and Public Awareness
    • Integrative Systems
    • Neuronal Excitability
    • Novel Tools and Methods
    • Sensory and Motor Systems
  • ALERTS
  • FOR AUTHORS
  • EDITORIAL BOARD
  • BLOG
  • ABOUT
    • Overview
    • For the Media
    • Privacy Policy
    • Contact Us
    • Feedback
  • SfN.org
  • eNeuro
  • The Journal of Neuroscience
  • Neuronline
  • BrainFacts.org

User menu

  • My alerts

Search

  • Advanced search
eNeuro
  • My alerts

eNeuro

Advanced Search

Submit a Manuscript
  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Latest Articles
    • Issue Archive
    • Editorials
    • Research Highlights
  • TOPICS
    • Cognition and Behavior
    • Development
    • Disorders of the Nervous System
    • History, Teaching and Public Awareness
    • Integrative Systems
    • Neuronal Excitability
    • Novel Tools and Methods
    • Sensory and Motor Systems
  • ALERTS
  • FOR AUTHORS
  • EDITORIAL BOARD
  • BLOG
  • ABOUT
    • Overview
    • For the Media
    • Privacy Policy
    • Contact Us
    • Feedback
PreviousNext
Research ArticleResearch Article: New Research, Disorders of the Nervous System

Variable Interhemispheric Asymmetry in Layer V of the Supplementary Motor Area following Cervical Hemisection in Adult Macaque Monkeys

A. Contestabile, R. Colangiulo, M. Lucchini, E.M. Rouiller and E. Schmidlin
eNeuro 11 September 2020, 7 (5) ENEURO.0280-20.2020; DOI: https://doi.org/10.1523/ENEURO.0280-20.2020
A. Contestabile
1Department of Basic Neuroscience, University of Geneva, Genève CH-1205, Switzerland
2Department of Neurosciences and Movement Sciences, Section of Medicine, Faculty of Sciences and Medicine, Fribourg Center of Cognition, University of Fribourg, Fribourg CH-1700, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for A. Contestabile
R. Colangiulo
2Department of Neurosciences and Movement Sciences, Section of Medicine, Faculty of Sciences and Medicine, Fribourg Center of Cognition, University of Fribourg, Fribourg CH-1700, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
M. Lucchini
1Department of Basic Neuroscience, University of Geneva, Genève CH-1205, Switzerland
2Department of Neurosciences and Movement Sciences, Section of Medicine, Faculty of Sciences and Medicine, Fribourg Center of Cognition, University of Fribourg, Fribourg CH-1700, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
E.M. Rouiller
2Department of Neurosciences and Movement Sciences, Section of Medicine, Faculty of Sciences and Medicine, Fribourg Center of Cognition, University of Fribourg, Fribourg CH-1700, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
E. Schmidlin
2Department of Neurosciences and Movement Sciences, Section of Medicine, Faculty of Sciences and Medicine, Fribourg Center of Cognition, University of Fribourg, Fribourg CH-1700, Switzerland
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for E. Schmidlin
  • Article
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF
Loading

Article Figures & Data

Figures

  • Tables
  • Figure1
    • Download figure
    • Open in new tab
    • Download powerpoint
  • Figure 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 1.

    CS projection of SMA. A, upper panel, Schematic representation of a macaque brain showing the location of pre-SMA (area F6), SMA-proper (area F3), and M1. Lower panel, Schematic representation of the CS projections of F6 (bilateral). B, lower panel, Upper cervical spinal cord section showing the localization of CS axons labeled by a unilateral BDA injection in the SMA. Upper panel, Pie chart reporting the percentage of BDA-positive CS axons present in the ipsilateral ventromedial, ipsilateral dorsolateral, and contralateral dorsomedial part of the spinal cord. The majority of BDA positive CS axons are located in the contralateral dorsolateral part of the spinal cord. C, Photomicrographs of sagittal histologic sections of the spinal cord of a lesioned animal (Mk-CS) showing the induced permanent lesion at the C7/C8 level. The histologic sections derived from two different series processed to visualize SMI-32 staining (left) or Nissl staining (right). Scale bar: 500 μm. D, Graphical representation of behavioral performance in the modified Brinkman board task of the macaque monkeys included in this study (SCI in green and SCI + anti-Nogo-A treatment in dark gray). The manual performance of the ipsilesional hand is given by the score (number of pellets retrieved in the first 30 s of the task from the randomly distributed wells) as a function of time (days) before and after a SCI. Day 0 corresponds to the day of the lesion (vertical red line). Prelesional and postlesional average of the scores are indicated with horizontal gray lines. The total duration of functional recovery of manual dexterity after lesion is given by the time interval between the lesion (red vertical line) and the onset of the postlesion plateau (brown area). Figure Contributions: E. M. Rouiller and E. Schmidlin performed and supervised the experiments on the monkeys and analyzed the data.

  • Figure 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 2.

    Neuronal density in the Layer V of SMA in intact and SCI monkeys. A, Photomicrograph of coronal brain histologic section of an intact macaque monkey (Mk-IR) stained with SMI-32 and magnified in F3 (scale bar: 40 μm). Layers III and V are visible and SMI-32-positive pyramidal neurons are indicated with arrows. B–D, Localization of SMI-32-positive Layer V neurons in bilateral F3 and F6 areas of three representative macaque monkeys (intact: Mk-IR, SCI: Mk-CG and SCI + anti-Nogo-A treatment: Mk-AM). Four sections per macaque monkeys are shown and the relative rostro-caudal position of the sections from the F3-F6 border is reported in millimeters. Negative distance values belong to F6 and positive distance values belong to F3. E, Graphs representing the rostro-caudal gradient (from F6 to F3) of SMI-32-positive cell density in Layer V of all monkeys (intact: Mk-IC, Mk-IE, Mk-IR, and Mk-IZ; SCI: Mk-CG, Mk-CGa, Mk-CH, Mk-CP, and Mk-CS; SCI + anti-Nogo-A treatment: Mk-AG, Mk-AM, and Mk-AP). The cell density for each hemisphere is plotted as a function of the distance from the F3-F6 border, which has been set to 3 mm rostrally to the genu of the arcuate sulcus. Negative distance values belong to F6 and positive distance values belong to F3. The symbol # was used to indicate that the analyzed cortex region was not complete (sections lacking for the analysis). Figure Contributions: E. M. Rouiller and E. Schmidlin performed the experiments on the monkeys and generated the histologic sections. A. Contestabile and R. Colangiulo performed the microscopic analysis of the histologic sections. A. Contestabile analyzed the data.

  • Figure 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 3.

    IDCD after SCI in F3 and F6. A, Histograms reporting the cell density of Layer V SMI-32-positive neurons in F3 for intact (white background), SCI (light gray background), and SCI-treated monkeys (dark gray background). For each couple of histograms are reported the side (L = left and R = right) and the location in function of the SCI (Ipsi = ipsilesional and Contra = contralesional). As statistical test, a paired t test or Wilcoxon test was performed (p values are reported) comparing the cell density in the two hemispheres in each consecutive histologic section. B, Histograms showing the IDCD of Layer V SMI-32-positive neurons of F3 for intact (white background), SCI (light gray background), and SCI-treated monkeys (dark gray background). A positive IDCD corresponds to an ipsilesional bias in pyramidal cell density, while a negative IDCD corresponds to a contralesional bias in pyramidal cell density. B’, upper left inset, Comparison of calculated IDCD in F3 between groups. No statistical difference is observed (unpaired t test: t(10) = 0.8276, p = 0.4272). C, Histograms reporting the cell density of Layer V SMI-32-positive neurons in F6 for intact (white background), SCI (light gray background), and SCI-treated monkeys (dark gray background). For each couple of histograms, are reported the side (L = left and R = right) and the location in function of the SCI (Ipsi = ipsilesional and Contra = contralesional). As statistical test, a paired t test or Wilcoxon test was performed (p values are reported) comparing the cell density in the two hemispheres in each consecutive histologic section. D, Histograms showing the IDCD of Layer V SMI-32-positive neurons of F6 for intact (white background), SCI (light gray background), and SCI-treated monkeys (dark gray background). D’, upper left inset, Comparison of calculated IDCD in F6 between groups. No statistical difference is observed (unpaired t test: t(7) = 1.084, p = 0.3142). For A, C, the median and the interquartile range are indicated. For B, D, the mean ± SD are reported. L = left hemisphere, R = right hemisphere, *p ≤ 0.05, **p ≤ 0.01). Figure Contributions: E. M. Rouiller and E. Schmidlin performed the experiments on the monkeys and generated the histologic sections. A. Contestabile and R. Colangiulo performed the microscopic analysis of the histologic sections. A. Contestabile analyzed the data.

  • Figure 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 4.

    Arborization of Layer V SMI-32-positive neurons in F3 after a SCI. A, Neuronal reconstruction example of basal dendrites of a Layer V SMI-32-positive neuron. B–F, Sholl profiles of basal dendrites of Layer V SMI-32-positive neurons in each hemisphere in two intact monkeys (A, B) and in three SCI monkeys (D–F). For each monkey, the IDCD are reported in the upper right angle. G, Neuronal reconstruction example of apical dendrite of a Layer V SMI-32-positive neuron. H–L, Sholl profiles of apical dendrites of Layer V SMI-32-positive neurons in each hemisphere in two intact monkeys (H, I) and in three SCI monkeys (J–L). The curves represent the mean intersection values ± SD. As statistical test, a two-way ANOVA wit Bonferroni’s multiple comparison post hoc test was performed (*p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001). The p values for the distance to soma main effect (up) and hemisphere main effect (right) are report for each monkey. # in the upper right angle means a significative p value for the interaction between the distance to soma and the hemisphere main effect. Figure Contributions: A. Contestabile and M. Lucchini performed the microscopic analysis of the histologic sections. A. Contestabile analyzed the data.

  • Figure 5.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 5.

    Relationship of IDCD, proportion of hemisection extent, duration of recovery and percentage of functional recovery. A, The IDCD in F3 was plotted in function of the proportion of hemisection extent. The gray line represents the hypothesized interhemispheric cell density asymmetry (see Introduction). B, The IDCD in F3 was plotted in function of the duration of functional recovery. C, The duration of functional recovery was plotted in function of the proportion of hemisection extent. D, The IDCD in F3 was plotted in function of the functional recovery. E, The functional recovery of the animals was plotted in function of the duration of functional recovery. Intact (in white), SCI (light gray), and SCI-treated (dark gray) animals are divided by color code. In each graph, the R and the p value of the linear regression are reported. Figure Contributions: A. Contestabile, R. Colangiulo, E. M. Rouiller, and E. Schmidlin performed the experiments and collected the data. A. Contestabile analyzed the data.

Tables

  • Figures
    • View popup
    Table 1

    Summary of the individual properties of each monkey

    IntactUntreatedTreated with anti-Nogo-A antibody
    Mk-ICMk-IEMk-IRMk-IZMk-CGMK-CGa3Mk-CHMk-CPMk-CSMk-AG3Mk-AMMk-AP
    General informationBirthday17.07.9915.06.9602.02.0412.05.9620.02.0121.05.0320.02.0122.12.9730.04.9728.03.0220.02.0109.03.98
    SexMMFMMMMFMMMF
    SpeciesFascmulFascFascfascfascfascfascmulfascfascfasc
    Date of killing17.08.0915.02.0222.12.0909.02.0413.01.0519.01.0707.02.0509.11.0421.09.0103.08.0514.02.0516.11.04
    LesionDate of lesion----25.08.0416.08.0629.09.0404.05.0407.03.0113.04.0529.09.0402.06.04
    SCI side----leftrightrightleftleftleftrightleft
    Weight at time of lesion (kg)----5.1-4.13.84.03.74.54.2
    Age at the time of the lesion (d)----12821183131723251407111213172277
    Hemisection extent (%)----5173904563788058
    Degree of functional recovery from SCI, total score (%)1 ----901005383221009699
    Duration of functional recovery (d)2 ----494341494772736
    Treatmenttype of antibody----ctrlctrlctrlctrlctrlATIATI11c7
    Cocentration (mg/ml)----9793.73.73.693.7
    Volume (ml)----42444244
    Days of antibody injection----3029282932282815
    • M = male; F = female; fasc = M. fascicularis; mul = M. mulatta; rhe = Rhesus.

    • ↵1 Expressed in percentages of postlesion total score at plateau divided by prelesion total score in the modified Brinkman board task: all slots.

    • ↵2 Time interval from the day of lesion to the beginning of postlesion plateau, as defined by Kaeser et al. (2011).

    • ↵3 Mk-CGa and Mk-AG suffered from a more caudal lesion than C7/C8. These monkeys were taken into account in this study but with some reserves.

Back to top

In this issue

eneuro: 7 (5)
eNeuro
Vol. 7, Issue 5
September/October 2020
  • Table of Contents
  • Index by author
Email

Thank you for sharing this eNeuro article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Variable Interhemispheric Asymmetry in Layer V of the Supplementary Motor Area following Cervical Hemisection in Adult Macaque Monkeys
(Your Name) has forwarded a page to you from eNeuro
(Your Name) thought you would be interested in this article in eNeuro.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Print
View Full Page PDF
Citation Tools
Variable Interhemispheric Asymmetry in Layer V of the Supplementary Motor Area following Cervical Hemisection in Adult Macaque Monkeys
A. Contestabile, R. Colangiulo, M. Lucchini, E.M. Rouiller, E. Schmidlin
eNeuro 11 September 2020, 7 (5) ENEURO.0280-20.2020; DOI: 10.1523/ENEURO.0280-20.2020

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Respond to this article
Share
Variable Interhemispheric Asymmetry in Layer V of the Supplementary Motor Area following Cervical Hemisection in Adult Macaque Monkeys
A. Contestabile, R. Colangiulo, M. Lucchini, E.M. Rouiller, E. Schmidlin
eNeuro 11 September 2020, 7 (5) ENEURO.0280-20.2020; DOI: 10.1523/ENEURO.0280-20.2020
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Visual Abstract
    • Abstract
    • Significance Statement
    • Introduction
    • Materials and Methods
    • Results
    • Discussion
    • Conclusion
    • Acknowledgments
    • Footnotes
    • References
    • Synthesis
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF

Keywords

  • corticospinal projections
  • interhemispheric asymmetry
  • non-human primate
  • pyramidal neurons
  • spinal cord injury
  • supplementary motor area

Responses to this article

Respond to this article

Jump to comment:

No eLetters have been published for this article.

Related Articles

Cited By...

More in this TOC Section

Research Article: New Research

  • Dauer Formation in C. elegans Is Modulated through AWC and ASI-Dependent Chemosensation
  • Activation of Transient Receptor Potential Vanilloid 1 Channels in the Nucleus of the Solitary Tract and Activation of Dynorphin Input to the Median Preoptic Nucleus Contribute to Impaired BAT Thermogenesis in Diet-Induced Obesity
  • The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
Show more Research Article: New Research

Disorders of the Nervous System

  • Phenotypic differences between the Alzheimer’s disease-related hAPP-J20 model and heterozygous Zbtb20 knockout mice
  • Distinct basal metabolism in three mouse models of neurodevelopmental disorders
  • HIV-1 Tat and morphine differentially disrupt pyramidal cell structure and function and spatial learning in hippocampal area CA1: Continuous versus interrupted morphine exposure
Show more Disorders of the Nervous System

Subjects

  • Disorders of the Nervous System
  • Home
  • Alerts
  • Visit Society for Neuroscience on Facebook
  • Follow Society for Neuroscience on Twitter
  • Follow Society for Neuroscience on LinkedIn
  • Visit Society for Neuroscience on Youtube
  • Follow our RSS feeds

Content

  • Early Release
  • Current Issue
  • Latest Articles
  • Issue Archive
  • Blog
  • Browse by Topic

Information

  • For Authors
  • For the Media

About

  • About the Journal
  • Editorial Board
  • Privacy Policy
  • Contact
  • Feedback
(eNeuro logo)
(SfN logo)

Copyright © 2021 by the Society for Neuroscience.
eNeuro eISSN: 2373-2822

The ideas and opinions expressed in eNeuro do not necessarily reflect those of SfN or the eNeuro Editorial Board. Publication of an advertisement or other product mention in eNeuro should not be construed as an endorsement of the manufacturer’s claims. SfN does not assume any responsibility for any injury and/or damage to persons or property arising from or related to any use of any material contained in eNeuro.