A large fraction of neocortical myelin ensheathes axons of local inhibitory neurons

Abstract
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Abstract

Myelin is best known for its role in increasing the conduction velocity and metabolic efficiency of long-range excitatory axons. Accordingly, the myelin observed in neocortical gray matter is thought to mostly ensheath excitatory axons connecting to subcortical regions and distant cortical areas. Using independent analyses of light and electron microscopy data from mouse neocortex, we show that a surprisingly large fraction of cortical myelin (half the myelin in layer 2/3 and a quarter in layer 4) ensheathes axons of inhibitory neurons, specifically of parvalbumin-positive basket cells. This myelin differs significantly from that of excitatory axons in distribution and protein composition. Myelin on inhibitory axons is unlikely to meaningfully hasten the arrival of spikes at their pre-synaptic terminals, due to the patchy distribution and short path-lengths observed. Our results thus highlight the need for exploring alternative roles for myelin in neocortical circuits.

Data availability

The following previously published data sets were used

1. Bock DD
2. Lee WC
3. Kerlin AM
4. Andermann ML
5. Hood G
6. Wetzel AW
7. Yurgenson S
8. Soucy ER
9. Kim HS
10. Reid RC
(2011) Network anatomy and in vivo physiology of visual cortical neurons.
Publicly available at the Open Connectome Project (Mouse V1; http://openconnecto.me/bock11/).

http://openconnecto.me/catmaid/?pid=4&zp=0&yp=59903&xp=67711&tool=navigator&sid0=4&s0=10

Article and author information

Author details

Kristina D Micheva

Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States

For correspondence
kmicheva@stanford.edu

Competing interests
Kristina D Micheva, Have founder's equity interests in Aratome, LLC (Menlo Park, CA), an enterprise that produces array tomography materials and services. Also listed as inventors on two US patents regarding array tomography methods that have been issued to Stanford University (US patents 7,767,414 and 9,008,378).
Dylan Wolman

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-5012-1690
Brett D Mensh

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
No competing interests declared.
Elizabeth Pax

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

Competing interests
No competing interests declared.
JoAnn Buchanan

Allen Institute for Brain Science, Seattle, United States

Competing interests
No competing interests declared.
Stephen J Smith

Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States

Competing interests
Stephen J Smith, Have founder's equity interests in Aratome, LLC (Menlo Park, CA), an enterprise that produces array tomography materials and services. Also listed as inventors on two US patents regarding array tomography methods that have been issued to Stanford University (US patents 7,767,414 and 9,008,378).
Davi D Bock

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

For correspondence
bockd@janelia.hhmi.org

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-8218-7926

Ethics

Animal experimentation: The tissue for the array tomography experiments was provided by Dr. Richard Weinberg, University of North Carolina (UNC). All animal procedures were performed according to NIH and UNC guidelines with a protocol (#13-258.0) approved by the UNC Institutional Animal Care and Use Committee. Mice were housed in an approved UNC animal care facility on a 12-hour light/dark cycle with ad libitum food and water access. Immediately before the terminal surgery, mice were transported to the research laboratory, where they were deeply anesthetized with sodium pentobarbital (80 mg/kg ip). JRC Immunohistochemistry: Mice were housed on a 12-hour light/dark cycle with ad libitum food and water access. Experimental procedures were conducted according to the National Institute of Health guidelines for animal research and approved by the Institutional Animal Care and Use Committee at Janelia Farm Research Campus. Approved animal protocol is IACUC 11-71.

Copyright

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.