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Published in: Brain Structure and Function 8/2017

01-11-2017 | Original Article

Intrinsic functional organization of putative language networks in the brain following left cerebral hemispherectomy

Authors: Anna Ivanova, Eran Zaidel, Noriko Salamon, Susan Bookheimer, Lucina Q. Uddin, Stella de Bode

Published in: Brain Structure and Function | Issue 8/2017

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Abstract

In rare cases of severe and intractable epilepsy, cerebral hemispherectomy is performed to arrest seizure activity and improve quality of life. The remaining hemisphere is often capable of supporting many cognitive functions post-surgery, although the outcome depends on the underlying etiology, hemisphere removed, and age of resection. The mechanisms underlying this massive reorganization are at present unknown. Here we examined intrinsic functional connectivity of putative language brain networks in four children after left cerebral hemispherectomy using resting-state functional magnetic resonance imaging (rsfMRI). We compared these functional systems to intrinsic language networks in 15 neurotypical controls using region-of-interest (ROI)-based functional connectivity analyses. In three out of four hemispherectomy patients, the ROI placed in the right inferior gyrus revealed a functional network that strongly resembled the right-hemisphere intrinsic language network observed in controls. This network typically comprised inferior frontal gyrus, superior temporal sulcus, and premotor regions. Quantitative ROI-to-ROI analyses revealed that functional connectivity between major nodes of the language network was significantly altered in all 4 examined patients. Overall, our data demonstrate that the pattern of functional connectivity within language networks is at least partially preserved in the intact right hemisphere of patients who underwent left hemispherectomy.
Literature
go back to reference Althausen A, Gleissner U, Hoppe C, Sassen R, Buddewig S, von Lehe M, Helmstaedter C (2013) Long-term outcome of hemispheric surgery at different ages in 61 epilepsy patients. J Neurol Neurosurg Psychiatry 84(5):529–536. doi:10.1136/jnnp-2012-303811 CrossRefPubMed Althausen A, Gleissner U, Hoppe C, Sassen R, Buddewig S, von Lehe M, Helmstaedter C (2013) Long-term outcome of hemispheric surgery at different ages in 61 epilepsy patients. J Neurol Neurosurg Psychiatry 84(5):529–536. doi:10.​1136/​jnnp-2012-303811 CrossRefPubMed
go back to reference Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Prieto T (1997) Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 17(1):353–362PubMed Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Prieto T (1997) Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 17(1):353–362PubMed
go back to reference Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541CrossRefPubMed Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541CrossRefPubMed
go back to reference Cook SW, Nguyen ST, Hu B, Yudovin S, Shields WD, Vinters HV, Mathern GW (2004) Cerebral hemispherectomy in pediatric patients with epilepsy: comparison of three techniques by pathological substrate in 115 patients. J Neurosurg 100(2 Suppl Pediatrics):125–141. doi:10.3171/ped.2004.100.2.0125 PubMed Cook SW, Nguyen ST, Hu B, Yudovin S, Shields WD, Vinters HV, Mathern GW (2004) Cerebral hemispherectomy in pediatric patients with epilepsy: comparison of three techniques by pathological substrate in 115 patients. J Neurosurg 100(2 Suppl Pediatrics):125–141. doi:10.​3171/​ped.​2004.​100.​2.​0125 PubMed
go back to reference Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103(37):13848–13853CrossRefPubMedPubMedCentral Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103(37):13848–13853CrossRefPubMedPubMedCentral
go back to reference Di Martino A, Yan CG, Li Q, Denio E, Castellanos FX, Alaerts K, Milham MP (2014) The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry 19(6):659–667. doi:10.1038/mp.2013.78 CrossRefPubMed Di Martino A, Yan CG, Li Q, Denio E, Castellanos FX, Alaerts K, Milham MP (2014) The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry 19(6):659–667. doi:10.​1038/​mp.​2013.​78 CrossRefPubMed
go back to reference Dunn LM, Dunn DM (2007) Peabody picture vocabulary test, 4th edn. PsychCorp, San Antonio Dunn LM, Dunn DM (2007) Peabody picture vocabulary test, 4th edn. PsychCorp, San Antonio
go back to reference Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711CrossRefPubMed Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711CrossRefPubMed
go back to reference Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35(3):346–355CrossRefPubMed Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35(3):346–355CrossRefPubMed
go back to reference Gould L, Mickleborough MJ, Wu A, Tellez J, Ekstrand C, Lorentz E, Borowsky R (2016) Presurgical language mapping in epilepsy: using fMRI of reading to identify functional reorganization in a patient with long-standing temporal lobe epilepsy. Epilepsy Behav Case Rep 5:6–10. doi:10.1016/j.ebcr.2015.10.003 CrossRefPubMed Gould L, Mickleborough MJ, Wu A, Tellez J, Ekstrand C, Lorentz E, Borowsky R (2016) Presurgical language mapping in epilepsy: using fMRI of reading to identify functional reorganization in a patient with long-standing temporal lobe epilepsy. Epilepsy Behav Case Rep 5:6–10. doi:10.​1016/​j.​ebcr.​2015.​10.​003 CrossRefPubMed
go back to reference Hertz-Pannier L, Chiron C, Jambaque I, Renaux-Kieffer V, Van de Moortele PF, Delalande O, Le Bihan D (2002) Late plasticity for language in a child’s non-dominant hemisphere: a pre- and post-surgery fMRI study. Brain 125(Pt 2):361–372CrossRefPubMed Hertz-Pannier L, Chiron C, Jambaque I, Renaux-Kieffer V, Van de Moortele PF, Delalande O, Le Bihan D (2002) Late plasticity for language in a child’s non-dominant hemisphere: a pre- and post-surgery fMRI study. Brain 125(Pt 2):361–372CrossRefPubMed
go back to reference Jonas R, Nguyen S, Hu B, Asarnow RF, LoPresti C, Curtiss S, Mathern GW (2004) Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes. Neurology 62(10):1712–1721CrossRefPubMed Jonas R, Nguyen S, Hu B, Asarnow RF, LoPresti C, Curtiss S, Mathern GW (2004) Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes. Neurology 62(10):1712–1721CrossRefPubMed
go back to reference Moosa AN, Jehi L, Marashly A, Cosmo G, Lachhwani D, Wyllie E, Gupta A (2013) Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia 54(10):1771–1779. doi:10.1111/epi.12342 CrossRefPubMed Moosa AN, Jehi L, Marashly A, Cosmo G, Lachhwani D, Wyllie E, Gupta A (2013) Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia 54(10):1771–1779. doi:10.​1111/​epi.​12342 CrossRefPubMed
go back to reference Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, Weiller C (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 105(46):18035–18040CrossRefPubMedPubMedCentral Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, Weiller C (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 105(46):18035–18040CrossRefPubMedPubMedCentral
go back to reference Tie Y, Rigolo L, Norton IH, Huang RY, Wu W, Orringer D, Golby AJ (2014) Defining language networks from resting-state fMRI for surgical planning—a feasibility study. Hum Brain Mapp 35(3):1018–1030. doi:10.1002/hbm.22231 CrossRefPubMed Tie Y, Rigolo L, Norton IH, Huang RY, Wu W, Orringer D, Golby AJ (2014) Defining language networks from resting-state fMRI for surgical planning—a feasibility study. Hum Brain Mapp 35(3):1018–1030. doi:10.​1002/​hbm.​22231 CrossRefPubMed
go back to reference Voets NL, Adcock JE, Flitney DE, Behrens TE, Hart Y, Stacey R, Matthews PM (2006) Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 129(Pt 3):754–766. doi:10.1093/brain/awh679 CrossRefPubMed Voets NL, Adcock JE, Flitney DE, Behrens TE, Hart Y, Stacey R, Matthews PM (2006) Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 129(Pt 3):754–766. doi:10.​1093/​brain/​awh679 CrossRefPubMed
go back to reference Woodcock RW (2011) Woodcock reading mastery tests—III. American Guidance Service, Circle Pines Woodcock RW (2011) Woodcock reading mastery tests—III. American Guidance Service, Circle Pines
go back to reference Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8(8):665–670CrossRefPubMedPubMedCentral Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8(8):665–670CrossRefPubMedPubMedCentral
Metadata
Title
Intrinsic functional organization of putative language networks in the brain following left cerebral hemispherectomy
Authors
Anna Ivanova
Eran Zaidel
Noriko Salamon
Susan Bookheimer
Lucina Q. Uddin
Stella de Bode
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1434-y

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