The relevance of heterotopic callosal fibers to interhemispheric connectivity of the mammalian brain.
axonal tracing
corpus callosum
diffusion-weighted imaging
structural brain connectivity
tractography
Journal
Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718
Informations de publication
Date de publication:
04 04 2023
04 04 2023
Historique:
received:
04
07
2022
revised:
29
08
2022
accepted:
30
08
2022
medline:
19
4
2023
pubmed:
1
10
2022
entrez:
30
9
2022
Statut:
ppublish
Résumé
The corpus callosum (CC) is the largest white matter structure and the primary pathway for interhemispheric brain communication. Investigating callosal connectivity is crucial to unraveling the brain's anatomical and functional organization in health and disease. Classical anatomical studies have characterized the bulk of callosal axonal fibers as connecting primarily homotopic cortical areas. Whenever detected, heterotopic callosal fibers were ascribed to altered sprouting and pruning mechanisms in neurodevelopmental diseases such as CC dysgenesis (CCD). We hypothesized that these heterotopic connections had been grossly underestimated due to their complex nature and methodological limitations. We used the Allen Mouse Brain Connectivity Atlas and high-resolution diffusion-weighted imaging to identify and quantify homotopic and heterotopic callosal connections in mice, marmosets, and humans. In all 3 species, we show that ~75% of interhemispheric callosal connections are heterotopic and comprise the central core of the CC, whereas the homotopic fibers lay along its periphery. We also demonstrate that heterotopic connections have an essential role in determining the global properties of brain networks. These findings reshape our view of the corpus callosum's role as the primary hub for interhemispheric brain communication, directly impacting multiple neuroscience fields investigating cortical connectivity, neurodevelopment, and neurodevelopmental disorders.
Identifiants
pubmed: 36178137
pii: 6731723
doi: 10.1093/cercor/bhac377
pmc: PMC10110439
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4752-4760Subventions
Organisme : NIA NIH HHS
ID : R24 AG073190
Pays : United States
Organisme : NIA NIH HHS
ID : U19 AG074866
Pays : United States
Informations de copyright
© The Author(s) 2022. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Références
Front Hum Neurosci. 2014 Jul 14;8:497
pubmed: 25071525
Proc Natl Acad Sci U S A. 2015 May 19;112(20):6473-8
pubmed: 25941372
Neuroimage Clin. 2020;28:102425
pubmed: 32979843
Neuroimage Clin. 2016 Jun 07;12:23-33
pubmed: 27358766
Neuroimage. 2015 May 1;111:277-88
pubmed: 25725467
Front Cell Neurosci. 2017 Feb 21;11:36
pubmed: 28270750
Brain Commun. 2021 May 14;3(2):fcab057
pubmed: 34704021
Braz J Med Biol Res. 2002 Dec;35(12):1441-53
pubmed: 12436187
Proc Natl Acad Sci U S A. 2017 Nov 7;114(45):E9692-E9701
pubmed: 29078382
Psychiatry Res Neuroimaging. 2021 Jul 30;313:111301
pubmed: 34022542
Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):E2714-23
pubmed: 23812756
Trends Neurosci. 2015 May;38(5):264-72
pubmed: 25841797
Brain. 2014 Jun;137(Pt 6):1813-29
pubmed: 24771497
Prog Neurobiol. 2022 Jan;208:102186
pubmed: 34780864
Neurosurg Clin N Am. 2010 Jul;21(3):399-426
pubmed: 20561492
Neuroimage. 2002 Jan;15(1):273-89
pubmed: 11771995
Neuroimage. 2016 Oct 1;139:259-270
pubmed: 27338515
Eur J Neurosci. 2003 Aug;18(4):775-88
pubmed: 12925004
Eur Radiol. 2016 Aug;26(8):2587-96
pubmed: 26560723
Sci Rep. 2019 Mar 4;9(1):3346
pubmed: 30833662
J Comp Neurol. 1988 Apr 22;270(4):575-90
pubmed: 3372749
Cereb Cortex. 2007 Mar;17(3):531-41
pubmed: 16627861
Semin Pediatr Neurol. 2009 Sep;16(3):127-42
pubmed: 19778710
Cortex. 2019 Dec;121:454-467
pubmed: 31731212
Neuroimage. 2013 Oct 15;80:62-79
pubmed: 23684880
J Comp Neurol. 2001 May 28;434(2):147-57
pubmed: 11331522
Front Hum Neurosci. 2015 Jun 30;9:386
pubmed: 26175682
Nat Neurosci. 2016 Apr;19(4):533-41
pubmed: 27021938
PLoS Comput Biol. 2005 Sep;1(4):e42
pubmed: 16201007
Biol Psychiatry. 2015 Jul 15;78(2):126-34
pubmed: 25850620
Neuroimage. 2013 Apr 15;70:340-55
pubmed: 23268782
Eur J Neurosci. 2007 Mar;25(5):1384-94
pubmed: 17425565
J Neurosci. 2011 Nov 2;31(44):15775-86
pubmed: 22049421
Hum Brain Mapp. 2016 Dec;37(12):4718-4735
pubmed: 27500966
Neuroimage. 2020 Aug 15;217:116875
pubmed: 32335262
J Comp Neurol. 1965 Jun;124(3):353-65
pubmed: 5861718
Proc Natl Acad Sci U S A. 2017 Dec 12;114(50):13278-13283
pubmed: 29183973
Neuroimage. 2018 Apr 1;169:106-116
pubmed: 29208569
Mol Cell Neurosci. 2019 Oct;100:103397
pubmed: 31454665
Psychiatry Res Neuroimaging. 2016 Oct 30;256:8-14
pubmed: 27619071
Development. 2003 Oct;130(20):4999-5008
pubmed: 12952902
J Comp Neurol. 1994 Feb 15;340(3):328-36
pubmed: 8188854
Proc Natl Acad Sci U S A. 2014 May 27;111(21):7843-8
pubmed: 24821757
Neuroimage. 2020 Aug 15;217:116868
pubmed: 32360691
Nat Rev Neurosci. 2007 Apr;8(4):287-99
pubmed: 17375041
Proc Natl Acad Sci U S A. 2018 Sep 18;115(38):9622-9627
pubmed: 30181276
Nature. 2014 Apr 10;508(7495):207-14
pubmed: 24695228
Trends Neurosci. 2011 Jan;34(1):41-50
pubmed: 21129791
Brain. 2015 Jul;138(Pt 7):2046-58
pubmed: 25937563
Neuroscience. 2017 Mar 6;344:56-66
pubmed: 28042027
Exp Brain Res. 1999 Jan;124(1):1-7
pubmed: 9928783
Brain Res. 1974 Mar 15;68(1):1-18
pubmed: 4470444
Neuroimage. 2013 Sep;78:196-203
pubmed: 23587687