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Published in: Clinical Neuroradiology 3/2017

01-09-2017 | Original Article

Inter-hemispheric Claustral Connections in Human Brain: A Constrained Spherical Deconvolution-Based Study

Authors: A. Arrigo, E. Mormina, A. Calamuneri, M. Gaeta, F. Granata, S. Marino, G. P. Anastasi, D. Milardi, A. Quartarone

Published in: Clinical Neuroradiology | Issue 3/2017

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Abstract

Purpose

Complex claustral connection network was widely demonstrated both in humans and animals. Moreover, several studies have suggested that claustral connections directly involve also the contralateral hemisphere. Detection of contralateral cortico-claustral and inter-claustral connections was reported mainly in animals and only partially in humans. The main purpose of this study was to provide more robust tractography-driven support of the existence of inter-hemispheric claustral connections in humans, by means of a dedicated optimized tractographic protocol.

Methods

Fifteen healthy subjects were examined by means of an advanced magnetic resonance imaging-based probabilistic constrained spherical deconvolution tractographic protocol. Moreover, quantitative diffusion parameters were extracted by each reconstructed pathway.

Results

In this study, further imaging-based support on the possible existence in humans of contralateral cortico-claustral and inter-claustral connections was provided. These connections were found to involve almost all the superior portion of each claustrum, showing a topographical organization. Moreover, the detection of inter-claustral connections passing through the anterior commissure was reported, for the first time, in humans.

Conclusions

The possible existence of inter-claustral and cortico-claustral contralateral pathways might provide the morphological basis for the complex functional phenomena observed in previous studies. Furthermore, these connections might have several important clinical implications, since they might explain how the inter-hemispheric coordination governed by the claustrum, as well as the functional recovery subsequent to damages involving one claustrum, takes place.
Literature
1.
go back to reference Edelstein LR, Denaro FJ. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol (Noisy-le-grand). 2004;50(6):675–702. Edelstein LR, Denaro FJ. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol (Noisy-le-grand). 2004;50(6):675–702.
2.
go back to reference Pirone A, Cozzi B, Edelstein L, Peruffo A, Lenzi C, Quilici F, Antonini R, Castagna M. Topography of Gng2- and NetrinG2-expression suggests an insular origin of the human claustrum. PLoS One. 2012;7(9):e44745.CrossRefPubMedPubMedCentral Pirone A, Cozzi B, Edelstein L, Peruffo A, Lenzi C, Quilici F, Antonini R, Castagna M. Topography of Gng2- and NetrinG2-expression suggests an insular origin of the human claustrum. PLoS One. 2012;7(9):e44745.CrossRefPubMedPubMedCentral
3.
go back to reference Tanné-Gariépy J, Boussaoud D, Rouiller EM. Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. J Comp Neurol. 2002;454(2):140–57.CrossRefPubMed Tanné-Gariépy J, Boussaoud D, Rouiller EM. Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. J Comp Neurol. 2002;454(2):140–57.CrossRefPubMed
4.
go back to reference Edelstein LR, Denaro FJ. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol (Noisy-le-grand). 2004;50(6):675–702. Edelstein LR, Denaro FJ. The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. Cell Mol Biol (Noisy-le-grand). 2004;50(6):675–702.
5.
go back to reference LeVay S, Sherk H. The visual claustrum of the cat. I. Structure and connections. J Neurosci. 1981;1(9):956–80.PubMed LeVay S, Sherk H. The visual claustrum of the cat. I. Structure and connections. J Neurosci. 1981;1(9):956–80.PubMed
6.
go back to reference Sherk H, LeVay S. Visual claustrum: topography and receptive field properties in the cat. Science. 1981;212(4490):87–9.CrossRefPubMed Sherk H, LeVay S. Visual claustrum: topography and receptive field properties in the cat. Science. 1981;212(4490):87–9.CrossRefPubMed
8.
go back to reference Fernández-Miranda JC, Rhoton AL Jr., Kakizawa Y, Choi C, Alvarez-Linera J. The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg. 2008;108(4):764–74.CrossRefPubMed Fernández-Miranda JC, Rhoton AL Jr., Kakizawa Y, Choi C, Alvarez-Linera J. The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg. 2008;108(4):764–74.CrossRefPubMed
9.
go back to reference Torgerson CM, Irimia A, Goh SY, Van Horn JD. The DTI connectivity of the human claustrum. Hum Brain Mapp. 2015;36(3):827–38. Torgerson CM, Irimia A, Goh SY, Van Horn JD. The DTI connectivity of the human claustrum. Hum Brain Mapp. 2015;36(3):827–38.
10.
go back to reference Milardi D, Bramanti P, Milazzo C, Finocchio G, Arrigo A, Santoro G, Trimarchi F, Quartarone A, Anastasi G, Gaeta M. Cortical and subcortical connections of the human claustrum revealed in vivo by constrained spherical deconvolution tractography. Cereb Cortex. 2015;25(2):406–14.CrossRefPubMed Milardi D, Bramanti P, Milazzo C, Finocchio G, Arrigo A, Santoro G, Trimarchi F, Quartarone A, Anastasi G, Gaeta M. Cortical and subcortical connections of the human claustrum revealed in vivo by constrained spherical deconvolution tractography. Cereb Cortex. 2015;25(2):406–14.CrossRefPubMed
11.
go back to reference Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A. White matter fiber tractography: why we need to move beyond DTI. J Neurosurg. 2013;118(6):1367–77.CrossRefPubMed Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A. White matter fiber tractography: why we need to move beyond DTI. J Neurosurg. 2013;118(6):1367–77.CrossRefPubMed
12.
go back to reference Tournier JD, Calamante F, Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage. 2007;35(4):1459–72.CrossRefPubMed Tournier JD, Calamante F, Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage. 2007;35(4):1459–72.CrossRefPubMed
13.
go back to reference Arrigo A, Mormina E, Anastasi GP, Gaeta M, Calamuneri A, Quartarone A, De Salvo S, Bruschetta D, Rizzo G, Trimarchi F, Milardi D. Constrained spherical deconvolution analysis of the limbic network in human, with emphasis on a direct cerebello-limbic pathway. Front Hum Neurosci. 2014;8:987.CrossRefPubMedPubMedCentral Arrigo A, Mormina E, Anastasi GP, Gaeta M, Calamuneri A, Quartarone A, De Salvo S, Bruschetta D, Rizzo G, Trimarchi F, Milardi D. Constrained spherical deconvolution analysis of the limbic network in human, with emphasis on a direct cerebello-limbic pathway. Front Hum Neurosci. 2014;8:987.CrossRefPubMedPubMedCentral
14.
go back to reference Mormina E, Arrigo A, Calamuneri A, Granata F, Quartarone A, Ghilardi MF, Inglese M, Di Rocco A, Milardi D, Anastasi GP, Gaeta M. Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease. Neuroradiology. 2015;57(3):327–34.CrossRefPubMed Mormina E, Arrigo A, Calamuneri A, Granata F, Quartarone A, Ghilardi MF, Inglese M, Di Rocco A, Milardi D, Anastasi GP, Gaeta M. Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease. Neuroradiology. 2015;57(3):327–34.CrossRefPubMed
15.
go back to reference Milardi D, Gaeta M, Marino S, Arrigo A, Vaccarino G, Mormina E, Rizzo G, Milazzo C, Finocchio G, Baglieri A, Anastasi G, Quartarone A. Basal ganglia network by constrained spherical deconvolution: a possible cortico-pallidal pathway? Mov Disord. 2015;30(3):342–9.CrossRefPubMed Milardi D, Gaeta M, Marino S, Arrigo A, Vaccarino G, Mormina E, Rizzo G, Milazzo C, Finocchio G, Baglieri A, Anastasi G, Quartarone A. Basal ganglia network by constrained spherical deconvolution: a possible cortico-pallidal pathway? Mov Disord. 2015;30(3):342–9.CrossRefPubMed
16.
go back to reference Mormina E, Arrigo A, Calamuneri A, Granata F, Quartarone A, Ghilardi MF, Inglese M, Di Rocco A, Milardi D, Anastasi GP, Gaeta M. Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease. Neuroradiology. 2015;57(3):327–34.CrossRefPubMed Mormina E, Arrigo A, Calamuneri A, Granata F, Quartarone A, Ghilardi MF, Inglese M, Di Rocco A, Milardi D, Anastasi GP, Gaeta M. Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease. Neuroradiology. 2015;57(3):327–34.CrossRefPubMed
17.
go back to reference Mormina E, Longo M, Arrigo A, Alafaci C, Tomasello F, Calamuneri A, Marino S, Gaeta M, Vinci SL, Granata F. MRI tractography of corticospinal tract and arcuate fasciculus in high grade gliomas performed by constrained spherical deconvolution: qualitative and quantitative analysis. AJNR Am J Neuroradiol. 2015;36(10):1853–8. Mormina E, Longo M, Arrigo A, Alafaci C, Tomasello F, Calamuneri A, Marino S, Gaeta M, Vinci SL, Granata F. MRI tractography of corticospinal tract and arcuate fasciculus in high grade gliomas performed by constrained spherical deconvolution: qualitative and quantitative analysis. AJNR Am J Neuroradiol. 2015;36(10):1853–8.
18.
go back to reference Jones DK, Catani M, Pierpaoli C, Reeves SJ, Shergill SS, O’Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, Williams SC, Howard RJ. Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp. 2006;27(3):230–8.CrossRefPubMed Jones DK, Catani M, Pierpaoli C, Reeves SJ, Shergill SS, O’Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, Williams SC, Howard RJ. Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp. 2006;27(3):230–8.CrossRefPubMed
19.
go back to reference Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325–35.CrossRefPubMed Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325–35.CrossRefPubMed
20.
go back to reference Tournier JD, Calamante F, Connelly A. MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol. 2012;22:53–66.CrossRef Tournier JD, Calamante F, Connelly A. MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol. 2012;22:53–66.CrossRef
21.
go back to reference Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP. Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage. 2008;42(2):617–25.CrossRefPubMed Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP. Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage. 2008;42(2):617–25.CrossRefPubMed
22.
go back to reference Smith JB, Alloway KD. Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J Neurosci. 2010;30(50):16832–44.CrossRefPubMedPubMedCentral Smith JB, Alloway KD. Functional specificity of claustrum connections in the rat: interhemispheric communication between specific parts of motor cortex. J Neurosci. 2010;30(50):16832–44.CrossRefPubMedPubMedCentral
23.
go back to reference Smith JB, Alloway KD. Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front Syst Neurosci. 2014;8:93.PubMedPubMedCentral Smith JB, Alloway KD. Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front Syst Neurosci. 2014;8:93.PubMedPubMedCentral
24.
go back to reference Kunzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975;88:195–209.CrossRefPubMed Kunzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975;88:195–209.CrossRefPubMed
25.
go back to reference Norita M. Demonstration of bilateral claustro-cortical connections in the cat with the method of retrograde axonal transport of horseradish peroxidase. Arch Histol Jpn. 1977;40:1–10.CrossRefPubMed Norita M. Demonstration of bilateral claustro-cortical connections in the cat with the method of retrograde axonal transport of horseradish peroxidase. Arch Histol Jpn. 1977;40:1–10.CrossRefPubMed
26.
go back to reference Druga R. Claustro-neocortical connections in the cat and rat demonstrated by HRP tracing technique. J Hirnforsch. 1982;23:191–202.PubMed Druga R. Claustro-neocortical connections in the cat and rat demonstrated by HRP tracing technique. J Hirnforsch. 1982;23:191–202.PubMed
27.
go back to reference Cortimiglia R, Crescimanno G, Salerno MT, Amato G. The role of the claustrum in the bilateral control of frontal oculomotor neurons in the cat. Exp Brain Res. 1991;84:471–7.CrossRefPubMed Cortimiglia R, Crescimanno G, Salerno MT, Amato G. The role of the claustrum in the bilateral control of frontal oculomotor neurons in the cat. Exp Brain Res. 1991;84:471–7.CrossRefPubMed
28.
29.
go back to reference Thivierge JP, Marcus GF. The topographic brain: from neural connectivity to cognition. Trends Neurosci. 2007;30(6):251–9.CrossRefPubMed Thivierge JP, Marcus GF. The topographic brain: from neural connectivity to cognition. Trends Neurosci. 2007;30(6):251–9.CrossRefPubMed
30.
go back to reference Crescimanno G, Salerno MT, Cortimiglia R, Amato G. Claustral influence on ipsi- and contralateral motor cortical areas, in the cat. Brain Res Bull. 1989;22(5):839–43.CrossRefPubMed Crescimanno G, Salerno MT, Cortimiglia R, Amato G. Claustral influence on ipsi- and contralateral motor cortical areas, in the cat. Brain Res Bull. 1989;22(5):839–43.CrossRefPubMed
31.
go back to reference Bosman LW, Houweling AR, Owens CB, Tanke N, Shevchouk OT, Rahmati N, Teunissen WH, Ju C, Gong W, Koekkoek SK, De Zeeuw CI. Anatomical pathways involved in generating and sensing rhythmic whisker movements. Front Integr Neurosci. 2011;5:53.CrossRefPubMedPubMedCentral Bosman LW, Houweling AR, Owens CB, Tanke N, Shevchouk OT, Rahmati N, Teunissen WH, Ju C, Gong W, Koekkoek SK, De Zeeuw CI. Anatomical pathways involved in generating and sensing rhythmic whisker movements. Front Integr Neurosci. 2011;5:53.CrossRefPubMedPubMedCentral
32.
33.
go back to reference Kalaitzakis ME, Pearce RK, Gentleman SM. Clinical correlates of pathology in the claustrum in Parkinson’s disease and dementia with Lewy bodies. Neurosci Lett. 2009;461(1):12–5.CrossRefPubMed Kalaitzakis ME, Pearce RK, Gentleman SM. Clinical correlates of pathology in the claustrum in Parkinson’s disease and dementia with Lewy bodies. Neurosci Lett. 2009;461(1):12–5.CrossRefPubMed
34.
go back to reference Sperner J, Sander B, Lau S, Krude H, Scheffner D. Severe transitory encephalopathy with reversible lesions of the claustrum. Pediatr Radiol. 1996;26:769–71.CrossRefPubMed Sperner J, Sander B, Lau S, Krude H, Scheffner D. Severe transitory encephalopathy with reversible lesions of the claustrum. Pediatr Radiol. 1996;26:769–71.CrossRefPubMed
35.
go back to reference Wada JA, Kudo T. Involvement of the claustrum in the convulsive evolution of temporal limbic seizure in feline amygdaloid kindling. Electroencephalogr Clin Neurophysiol. 1997;103(2):249–56.CrossRefPubMed Wada JA, Kudo T. Involvement of the claustrum in the convulsive evolution of temporal limbic seizure in feline amygdaloid kindling. Electroencephalogr Clin Neurophysiol. 1997;103(2):249–56.CrossRefPubMed
36.
go back to reference Zhang X, Hannesson DK, Saucier DM, Wallace AE, Howland J, Corcoran ME. Susceptibility to kindling and neuronal connections of the anterior claustrum. J Neurosci. 2001;21(10):3674–87.PubMed Zhang X, Hannesson DK, Saucier DM, Wallace AE, Howland J, Corcoran ME. Susceptibility to kindling and neuronal connections of the anterior claustrum. J Neurosci. 2001;21(10):3674–87.PubMed
37.
go back to reference Duffau H, Mandonnet E, Gatignol P, Capelle L. Functional compensation of the claustrum: lessons from low-grade glioma surgery. J Neurooncol. 2007;81:327–9.CrossRefPubMed Duffau H, Mandonnet E, Gatignol P, Capelle L. Functional compensation of the claustrum: lessons from low-grade glioma surgery. J Neurooncol. 2007;81:327–9.CrossRefPubMed
38.
go back to reference Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010;23:803–20.CrossRefPubMed Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 2010;23:803–20.CrossRefPubMed
39.
go back to reference Descoteaux M, Deriche R, Knösche TR, Anwander A. Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging. 2009;28:269–86.CrossRefPubMed Descoteaux M, Deriche R, Knösche TR, Anwander A. Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging. 2009;28:269–86.CrossRefPubMed
40.
go back to reference Tournier JD, Calamante F, Connelly A. Effect of step size on probabilistic streamlines: implications for the interpretation of connectivity analysis. Proc Intl Soc Mag Reson Med. 2011;19:2019. Tournier JD, Calamante F, Connelly A. Effect of step size on probabilistic streamlines: implications for the interpretation of connectivity analysis. Proc Intl Soc Mag Reson Med. 2011;19:2019.
41.
go back to reference Chung HW, Chou MC, Chen CY. Principles and limitations of computational algorithms in clinical diffusion tensor MR tractography. AJNR Am J Neuroradiol. 2011;32:3–13.CrossRefPubMed Chung HW, Chou MC, Chen CY. Principles and limitations of computational algorithms in clinical diffusion tensor MR tractography. AJNR Am J Neuroradiol. 2011;32:3–13.CrossRefPubMed
Metadata
Title
Inter-hemispheric Claustral Connections in Human Brain: A Constrained Spherical Deconvolution-Based Study
Authors
A. Arrigo
E. Mormina
A. Calamuneri
M. Gaeta
F. Granata
S. Marino
G. P. Anastasi
D. Milardi
A. Quartarone
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 3/2017
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-015-0492-x

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