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Published in: European Radiology 5/2015

01-05-2015 | Pediatric

Structural connectivity analysis reveals abnormal brain connections in agenesis of the corpus callosum in children

Authors: Avner Meoded, Rohan Katipally, Thangamadhan Bosemani, Thierry A. G. M. Huisman, Andrea Poretti

Published in: European Radiology | Issue 5/2015

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Abstract

Objectives

Structural connectivity analysis is an ideal tool to study connections in brain malformations. We aimed to characterize the topological network measures and study sub-networks in children with agenesis of the corpus callosum (AgCC). We hypothesized a more segregated structural network in children with AgCC.

Methods

Structural connectivity analysis including topology analysis and network-based-statistics was applied in children with AgCC and age-matched controls. Probabilistic-tractography and brain segmentation into 108 regions were performed. For controls, structural connectivity has been analyzed after excluding the callosal connections (‘virtual callosotomy’).

Results

Ten patients (six males, mean age 6.5 years, SD 4.5 years) and ten controls (mean age 5.9 years, SD 4.7 years) were included. In patients, topology analysis revealed higher clustering coefficient and transitivity and lower small world index and assortativity compared to controls. The bilateral insula were identified as hubs in patients, whereas the cerebellum was detected as a hub only in controls. Three sub-networks of increased connectivity were identified in patients.

Conclusions

We found reduced global and increased local connectivity in children with AgCC compared to controls. Neural plasticity in AgCC may attempt to increase the interhemispheric connectivity through alternative decussating pathways other than the corpus callosum.

Key Points

The structural connectivity analysis quantifies white-matter networks within the brain
In callosal agenesis there is reduced global and increased local connectivity
In callosal agenesis, alternative decussating pathways are used for interhemispheric connectivity
Appendix
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Literature
1.
go back to reference Wahl M, Strominger Z, Jeremy RJ et al (2009) Variability of homotopic and heterotopic callosal connectivity in partial agenesis of the corpus callosum: a 3T diffusion tensor imaging and Q-ball tractography study. AJNR Am J Neuroradiol 30:282–289CrossRefPubMed Wahl M, Strominger Z, Jeremy RJ et al (2009) Variability of homotopic and heterotopic callosal connectivity in partial agenesis of the corpus callosum: a 3T diffusion tensor imaging and Q-ball tractography study. AJNR Am J Neuroradiol 30:282–289CrossRefPubMed
2.
go back to reference Raybaud C (2010) The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation. Neuroradiology 52:447–477CrossRefPubMed Raybaud C (2010) The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation. Neuroradiology 52:447–477CrossRefPubMed
3.
go back to reference Brown WS, Jeeves MA, Dietrich R, Burnison DS (1999) Bilateral field advantage and evoked potential interhemispheric transmission in commissurotomy and callosal agenesis. Neuropsychologia 37:1165–1180CrossRefPubMed Brown WS, Jeeves MA, Dietrich R, Burnison DS (1999) Bilateral field advantage and evoked potential interhemispheric transmission in commissurotomy and callosal agenesis. Neuropsychologia 37:1165–1180CrossRefPubMed
4.
go back to reference Paul LK, Van Lancker-Sidtis D, Schieffer B, Dietrich R, Brown WS (2003) Communicative deficits in agenesis of the corpus callosum: nonliteral language and affective prosody. Brain Lang 85:313–324CrossRefPubMed Paul LK, Van Lancker-Sidtis D, Schieffer B, Dietrich R, Brown WS (2003) Communicative deficits in agenesis of the corpus callosum: nonliteral language and affective prosody. Brain Lang 85:313–324CrossRefPubMed
5.
go back to reference Edwards TJ, Sherr EH, Barkovich AJ, Richards LJ (2014) Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes. Brain Edwards TJ, Sherr EH, Barkovich AJ, Richards LJ (2014) Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes. Brain
6.
go back to reference Paul LK, Brown WS, Adolphs R et al (2007) Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8:287–299CrossRefPubMed Paul LK, Brown WS, Adolphs R et al (2007) Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8:287–299CrossRefPubMed
7.
go back to reference Sotiriadis A, Makrydimas G (2012) Neurodevelopment after prenatal diagnosis of isolated agenesis of the corpus callosum: an integrative review. Am J Obstet Gynecol 206:e331–335CrossRef Sotiriadis A, Makrydimas G (2012) Neurodevelopment after prenatal diagnosis of isolated agenesis of the corpus callosum: an integrative review. Am J Obstet Gynecol 206:e331–335CrossRef
8.
go back to reference Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219CrossRefPubMed Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219CrossRefPubMed
9.
go back to reference Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269CrossRefPubMed Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269CrossRefPubMed
10.
go back to reference Lee SK, Mori S, Kim DJ, Kim SY, Kim DI (2004) Diffusion tensor MR imaging visualizes the altered hemispheric fiber connection in callosal dysgenesis. AJNR Am J Neuroradiol 25:25–28PubMed Lee SK, Mori S, Kim DJ, Kim SY, Kim DI (2004) Diffusion tensor MR imaging visualizes the altered hemispheric fiber connection in callosal dysgenesis. AJNR Am J Neuroradiol 25:25–28PubMed
11.
go back to reference Meoded A, Poretti A, Tekes A, Flammang A, Pryde S, Huisman TA (2011) Prenatal MR diffusion tractography in a fetus with complete corpus callosum agenesis. Neuropediatrics 42:122–123CrossRefPubMed Meoded A, Poretti A, Tekes A, Flammang A, Pryde S, Huisman TA (2011) Prenatal MR diffusion tractography in a fetus with complete corpus callosum agenesis. Neuropediatrics 42:122–123CrossRefPubMed
12.
go back to reference Kasprian G, Brugger PC, Schopf V et al (2013) Assessing prenatal white matter connectivity in commissural agenesis. Brain 136:168–179CrossRefPubMed Kasprian G, Brugger PC, Schopf V et al (2013) Assessing prenatal white matter connectivity in commissural agenesis. Brain 136:168–179CrossRefPubMed
14.
go back to reference Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198CrossRefPubMed Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198CrossRefPubMed
15.
go back to reference Bullmore ET, Bassett DS (2011) Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 7:113–140CrossRefPubMed Bullmore ET, Bassett DS (2011) Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 7:113–140CrossRefPubMed
16.
go back to reference Zalesky A, Fornito A, Harding IH et al (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970–983CrossRefPubMed Zalesky A, Fornito A, Harding IH et al (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970–983CrossRefPubMed
17.
go back to reference Tovar-Moll F, Moll J, de Oliveira-Souza R, Bramati I, Andreiuolo PA, Lent R (2007) Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. Cereb Cortex 17:531–541CrossRefPubMed Tovar-Moll F, Moll J, de Oliveira-Souza R, Bramati I, Andreiuolo PA, Lent R (2007) Neuroplasticity in human callosal dysgenesis: a diffusion tensor imaging study. Cereb Cortex 17:531–541CrossRefPubMed
18.
19.
go back to reference Pierpaoli C, Walker L, Irfanoglu MO et al (2010) TORTOISE: an integrated software package for processing of diffusion MRI data 18th Annual Meeting of the International Society of Magnetic Resonance in Medicine Stockholm, pp 1597 Pierpaoli C, Walker L, Irfanoglu MO et al (2010) TORTOISE: an integrated software package for processing of diffusion MRI data 18th Annual Meeting of the International Society of Magnetic Resonance in Medicine Stockholm, pp 1597
20.
21.
go back to reference Filippi M, van den Heuvel MP, Fornito A et al (2013) Assessment of system dysfunction in the brain through MRI-based connectomics. Lancet Neurol 12:1189–1199CrossRefPubMed Filippi M, van den Heuvel MP, Fornito A et al (2013) Assessment of system dysfunction in the brain through MRI-based connectomics. Lancet Neurol 12:1189–1199CrossRefPubMed
22.
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289CrossRefPubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289CrossRefPubMed
23.
go back to reference Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239CrossRefPubMed Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239CrossRefPubMed
24.
go back to reference Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155CrossRefPubMed Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155CrossRefPubMed
25.
go back to reference Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMed Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMed
26.
go back to reference Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910–913CrossRefPubMed Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910–913CrossRefPubMed
27.
go back to reference Hosseini SM, Hoeft F, Kesler SR (2012) GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS One 7:e40709CrossRefPubMedCentralPubMed Hosseini SM, Hoeft F, Kesler SR (2012) GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS One 7:e40709CrossRefPubMedCentralPubMed
29.
go back to reference Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197–1207CrossRefPubMed Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197–1207CrossRefPubMed
30.
go back to reference Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045CrossRefPubMedCentralPubMed Smith SM, Fox PT, Miller KL et al (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045CrossRefPubMedCentralPubMed
31.
go back to reference Owen JP, Li YO, Yang FG et al (2013) Resting-state networks and the functional connectome of the human brain in agenesis of the corpus callosum. Brain Connect 3:547–562CrossRefPubMedCentralPubMed Owen JP, Li YO, Yang FG et al (2013) Resting-state networks and the functional connectome of the human brain in agenesis of the corpus callosum. Brain Connect 3:547–562CrossRefPubMedCentralPubMed
33.
go back to reference Sporns O (2006) Small-world connectivity, motif composition, ad complexity of fractal neuronal connections. Biosystems 85:55–64CrossRefPubMed Sporns O (2006) Small-world connectivity, motif composition, ad complexity of fractal neuronal connections. Biosystems 85:55–64CrossRefPubMed
36.
go back to reference van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775–15786CrossRefPubMed van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775–15786CrossRefPubMed
37.
go back to reference Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349PubMed Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349PubMed
38.
go back to reference Hetts SW, Sherr EH, Chao S, Gobuty S, Barkovich AJ (2006) Anomalies of the corpus callosum: an MR analysis of the phenotypic spectrum of associated malformations. AJR Am J Roentgenol 187:1343–1348CrossRefPubMed Hetts SW, Sherr EH, Chao S, Gobuty S, Barkovich AJ (2006) Anomalies of the corpus callosum: an MR analysis of the phenotypic spectrum of associated malformations. AJR Am J Roentgenol 187:1343–1348CrossRefPubMed
39.
go back to reference Vulliemoz S, Raineteau O, Jabaudon D (2005) Reaching beyond the midline: why are human brains cross wired? Lancet Neurol 4:87–99CrossRefPubMed Vulliemoz S, Raineteau O, Jabaudon D (2005) Reaching beyond the midline: why are human brains cross wired? Lancet Neurol 4:87–99CrossRefPubMed
40.
go back to reference Shinbrot T, Young W (2008) Why decussate? Topological constraints on 3D wiring. Anat Rec (Hoboken) 291:1278–1292CrossRef Shinbrot T, Young W (2008) Why decussate? Topological constraints on 3D wiring. Anat Rec (Hoboken) 291:1278–1292CrossRef
41.
go back to reference Seymour SE, Reuter-Lorenz PA, Gazzaniga MS (1994) The disconnection syndrome. Basic findings reaffirmed. Brain 117:105–115CrossRefPubMed Seymour SE, Reuter-Lorenz PA, Gazzaniga MS (1994) The disconnection syndrome. Basic findings reaffirmed. Brain 117:105–115CrossRefPubMed
42.
go back to reference Choudhri AF, Whitehead MT, McGregor AL, Einhaus SL, Boop FA, Wheless JW (2013) Diffusion tensor imaging to evaluate commissural disconnection after corpus callosotomy. Neuroradiology 55:1397–1403CrossRefPubMed Choudhri AF, Whitehead MT, McGregor AL, Einhaus SL, Boop FA, Wheless JW (2013) Diffusion tensor imaging to evaluate commissural disconnection after corpus callosotomy. Neuroradiology 55:1397–1403CrossRefPubMed
43.
go back to reference Crossley NA, Mechelli A, Scott J et al (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137:2382–2395CrossRefPubMedCentralPubMed Crossley NA, Mechelli A, Scott J et al (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137:2382–2395CrossRefPubMedCentralPubMed
Metadata
Title
Structural connectivity analysis reveals abnormal brain connections in agenesis of the corpus callosum in children
Authors
Avner Meoded
Rohan Katipally
Thangamadhan Bosemani
Thierry A. G. M. Huisman
Andrea Poretti
Publication date
01-05-2015
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 5/2015
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-014-3541-y

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