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Published in: The Cerebellum 2/2017

01-04-2017 | Original Paper

Diffusion Tensor Tractography of the Cerebellar Peduncles in Prematurely Born 7-Year-Old Children

Authors: Eilon Shany, Terrie E. Inder, Sharon Goshen, Iris Lee, Jeffrey J. Neil, Christopher D. Smyser, Lex W. Doyle, Peter J. Anderson, Joshua S. Shimony

Published in: The Cerebellum | Issue 2/2017

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Abstract

The objective of this study was to correlate neurodevelopmental outcome of preterm-born children and their perinatal clinical and imaging characteristics with diffusion magnetic resonance imaging (MRI) measures of the three cerebellar peduncles at age 7. Included in this prospective longitudinal study were 140 preterm-born children (<30 weeks gestation) who underwent neurodevelopmental assessment (IQ, motor, language, working memory) and diffusion-weighted imaging (DWI) at age 7 years. White matter tracts in the superior, middle, and inferior cerebellar peduncles were delineated using regions of interest drawn on T2-weighted images and fractional anisotropy (FA) maps. Diffusion measures (mean diffusivity (MD) and FA) and tract volumes were calculated. Linear regression was used to assess relationships with outcome. The severity of white matter injury in the neonatal period was associated with lower FA in the right superior cerebellar peduncle (SCP) and lower tract volumes of both SCPs and middle cerebellar peduncles (MCPs). In the MCP, higher IQ was associated with lower MD in the whole group and higher FA in right-handed children. In the SCP, lower motor scores were associated with higher MD and higher language scores were associated with higher FA. These associations remained significant in multivariable models. This study adds to the body of literature detailing the importance of cerebellar involvement in cognitive function related to reciprocal connections with supratentorial structures.
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Literature
1.
go back to reference Manto M. The cerebellum, cerebellar disorders, and cerebellar research—two centuries of discoveries. Cerebellum. 2008;7:505–16.CrossRefPubMed Manto M. The cerebellum, cerebellar disorders, and cerebellar research—two centuries of discoveries. Cerebellum. 2008;7:505–16.CrossRefPubMed
2.
go back to reference Salmi J, Pallesen KJ, Neuvonen T, Brattico E, Korvenoja A, Salonen O, et al. Cognitive and motor loops of the human cerebro-cerebellar system. J Cogn Neurosci. 2010;22:2663–76.CrossRefPubMed Salmi J, Pallesen KJ, Neuvonen T, Brattico E, Korvenoja A, Salonen O, et al. Cognitive and motor loops of the human cerebro-cerebellar system. J Cogn Neurosci. 2010;22:2663–76.CrossRefPubMed
3.
5.
6.
7.
go back to reference Ghez C, Thach WT, The Cerebellum. In: Principles of Neural sciences, 4th Ed. Editors: Kandel RK, Swartz JH, Jessel TM. Mc Graw Hill. 2000: 832–852. Ghez C, Thach WT, The Cerebellum. In: Principles of Neural sciences, 4th Ed. Editors: Kandel RK, Swartz JH, Jessel TM. Mc Graw Hill. 2000: 832–852.
9.
go back to reference Xue R, van Zijl PC, Crain BJ, Solaiyappan M, Mori S. In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn Reson Med. 1999;42:1123–7.CrossRefPubMed Xue R, van Zijl PC, Crain BJ, Solaiyappan M, Mori S. In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn Reson Med. 1999;42:1123–7.CrossRefPubMed
10.
go back to reference Tam EW, Miller SP, Studholme C, Chau V, Glidden D, Poskitt KJ, et al. Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. J Pediatr. 2011;158:366–71.CrossRefPubMed Tam EW, Miller SP, Studholme C, Chau V, Glidden D, Poskitt KJ, et al. Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. J Pediatr. 2011;158:366–71.CrossRefPubMed
11.
go back to reference Tam EW, Ferriero DM, Xu D, Berman JI, Vigneron DB, Barkovich AJ, et al. Cerebellar development in the preterm neonate: effect of supratentorial brain injury. Pediatr Res. 2009;66:102–6.CrossRefPubMedPubMedCentral Tam EW, Ferriero DM, Xu D, Berman JI, Vigneron DB, Barkovich AJ, et al. Cerebellar development in the preterm neonate: effect of supratentorial brain injury. Pediatr Res. 2009;66:102–6.CrossRefPubMedPubMedCentral
12.
go back to reference Limperopoulos C, Bassan H, Gauvreau K, Robertson Jr RL, Sullivan NR, Benson CB, et al. Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics. 2007;120:584–93.CrossRefPubMed Limperopoulos C, Bassan H, Gauvreau K, Robertson Jr RL, Sullivan NR, Benson CB, et al. Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics. 2007;120:584–93.CrossRefPubMed
13.
go back to reference Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ. Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res. 2010;68:145–50.CrossRefPubMed Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ. Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res. 2010;68:145–50.CrossRefPubMed
14.
go back to reference Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ. Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex. 2014;24:728–36.CrossRefPubMed Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ. Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex. 2014;24:728–36.CrossRefPubMed
15.
go back to reference Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006;51:527–39.CrossRefPubMed Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006;51:527–39.CrossRefPubMed
16.
go back to reference Mukherjee P, Miller JH, Shimony JS, Conturo TE, Lee BC, Almli CR, et al. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology. 2001;221:349–58.CrossRefPubMed Mukherjee P, Miller JH, Shimony JS, Conturo TE, Lee BC, Almli CR, et al. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology. 2001;221:349–58.CrossRefPubMed
17.
go back to reference Hüppi PS, Dubois J. Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med. 2006;11:489–97.CrossRefPubMed Hüppi PS, Dubois J. Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med. 2006;11:489–97.CrossRefPubMed
18.
go back to reference Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C. Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage. 2012;60:340–52.CrossRefPubMed Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C. Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage. 2012;60:340–52.CrossRefPubMed
19.
go back to reference Hüppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD, et al. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics. 2001;107:455–60.CrossRefPubMed Hüppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD, et al. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics. 2001;107:455–60.CrossRefPubMed
20.
go back to reference Murakami A, Morimoto M, Yamada K, Kizu O, Nishimura A, Nishimura T, et al. Fiber-tracking techniques can predict the degree of neurologic impairment for periventricular leukomalacia. Pediatrics. 2008;122:500–6.CrossRefPubMed Murakami A, Morimoto M, Yamada K, Kizu O, Nishimura A, Nishimura T, et al. Fiber-tracking techniques can predict the degree of neurologic impairment for periventricular leukomalacia. Pediatrics. 2008;122:500–6.CrossRefPubMed
21.
go back to reference Eluvathingal TJ, Chugani HT, Behen ME, Juhász C, Muzik O, Maqbool M, et al. Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics. 2006;117:2093–100.CrossRefPubMed Eluvathingal TJ, Chugani HT, Behen ME, Juhász C, Muzik O, Maqbool M, et al. Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics. 2006;117:2093–100.CrossRefPubMed
22.
go back to reference Nagel BJ, Bathula D, Herting M, Schmitt C, Kroenke CD, Fair D, et al. Altered white matter microstructure in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 2011;50:283–92.CrossRefPubMedPubMedCentral Nagel BJ, Bathula D, Herting M, Schmitt C, Kroenke CD, Fair D, et al. Altered white matter microstructure in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 2011;50:283–92.CrossRefPubMedPubMedCentral
23.
go back to reference Bechtel N, Kobel M, Penner IK, Klarhöfer M, Scheffler K, Opwis K, et al. Decreased fractional anisotropy in the middle cerebellar peduncle in children with epilepsy and/or attention deficit/hyperactivity disorder: a preliminary study. Epilepsy Behav. 2009;15:294–8.CrossRefPubMed Bechtel N, Kobel M, Penner IK, Klarhöfer M, Scheffler K, Opwis K, et al. Decreased fractional anisotropy in the middle cerebellar peduncle in children with epilepsy and/or attention deficit/hyperactivity disorder: a preliminary study. Epilepsy Behav. 2009;15:294–8.CrossRefPubMed
24.
go back to reference Anderson P, Doyle LW, Victorian Infant Collaborative Study Group. Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA. 2003;289:3264–72.CrossRefPubMed Anderson P, Doyle LW, Victorian Infant Collaborative Study Group. Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA. 2003;289:3264–72.CrossRefPubMed
25.
go back to reference Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C, et al. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet. 2008;371:813–20.CrossRefPubMed Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C, et al. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet. 2008;371:813–20.CrossRefPubMed
26.
go back to reference Aarnoudse-Moens CS, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J. Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics. 2009;124:717–28.CrossRefPubMed Aarnoudse-Moens CS, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J. Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics. 2009;124:717–28.CrossRefPubMed
27.
go back to reference Steggerda SJ, Leijser LM, Wiggers-de Bruïne FT, van der Grond J, Walther FJ, van Wezel-Meijler G. Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology. 2009;252(1):190–9.CrossRefPubMed Steggerda SJ, Leijser LM, Wiggers-de Bruïne FT, van der Grond J, Walther FJ, van Wezel-Meijler G. Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology. 2009;252(1):190–9.CrossRefPubMed
28.
go back to reference Thompson DK, Warfield SK, Carlin JB, Pavlovic M, Wang HX, Bear M, et al. Perinatal risk factors altering regional brain structure in the preterm infant. Brain. 2007;130:667–77.CrossRefPubMed Thompson DK, Warfield SK, Carlin JB, Pavlovic M, Wang HX, Bear M, et al. Perinatal risk factors altering regional brain structure in the preterm infant. Brain. 2007;130:667–77.CrossRefPubMed
29.
go back to reference Mathur AM, Neil JJ, McKinstry RC, Inder TE. Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol. 2008;38:260–4.CrossRefPubMed Mathur AM, Neil JJ, McKinstry RC, Inder TE. Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol. 2008;38:260–4.CrossRefPubMed
30.
go back to reference Kidokoro H, Neil JJ, Inder TE. New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR Am J Neuroradiol. 2013;34:2208–14.CrossRefPubMedPubMedCentral Kidokoro H, Neil JJ, Inder TE. New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR Am J Neuroradiol. 2013;34:2208–14.CrossRefPubMedPubMedCentral
31.
go back to reference Wechsler D. Wechsler Abbreviated Scale of Intelligence (WASI). 1999; The Psychological Corporation. Wechsler D. Wechsler Abbreviated Scale of Intelligence (WASI). 1999; The Psychological Corporation.
32.
go back to reference Henderson SE, Sugden DA, Barnett AL. Movement Assessment Battery for Children e Second Edition (Movement ABC-2). London: The Psychological Corporation; 2007. Henderson SE, Sugden DA, Barnett AL. Movement Assessment Battery for Children e Second Edition (Movement ABC-2). London: The Psychological Corporation; 2007.
33.
go back to reference Semel E, Wiig EH, Secord WA. Clinical Evaluation of Language Fundamentals, Fourth Edition (CELF-4). Toronto: The Psychological Corporation/A Harcourt Assessment Company; 2003. Semel E, Wiig EH, Secord WA. Clinical Evaluation of Language Fundamentals, Fourth Edition (CELF-4). Toronto: The Psychological Corporation/A Harcourt Assessment Company; 2003.
34.
go back to reference Baddeley AD, Hitch G. Working memory. In G. Bower (Ed.), The psychology of learning and motivation (Vol. 8, pp. 47–90). 1974; New York: Academic Press. Baddeley AD, Hitch G. Working memory. In G. Bower (Ed.), The psychology of learning and motivation (Vol. 8, pp. 47–90). 1974; New York: Academic Press.
35.
go back to reference Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39:214–23.CrossRefPubMed Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39:214–23.CrossRefPubMed
36.
go back to reference Treyvaud K, Ure A, Doyle LW, Lee KJ, Rogers CE, Kidokoro H, et al. Psychiatric outcomes at age seven for very preterm children: rates and predictors. J Child Psychol Psychiatry. 2013;54:772–9.CrossRefPubMed Treyvaud K, Ure A, Doyle LW, Lee KJ, Rogers CE, Kidokoro H, et al. Psychiatric outcomes at age seven for very preterm children: rates and predictors. J Child Psychol Psychiatry. 2013;54:772–9.CrossRefPubMed
37.
go back to reference Goodman R, Ford T, Richards H, Gatward R, Meltzer H. The development and well-being assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. J Child Psychol Psychiatry. 2000;41:645–55.CrossRefPubMed Goodman R, Ford T, Richards H, Gatward R, Meltzer H. The development and well-being assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. J Child Psychol Psychiatry. 2000;41:645–55.CrossRefPubMed
38.
go back to reference Roberts G, Howard K, Spittle AJ, Brown NC, Anderson PJ, Doyle LW. J Rates of early intervention services in very preterm children with developmental disabilities at age 2 years. Paediatr Child Health. 2008;44:276–80.CrossRef Roberts G, Howard K, Spittle AJ, Brown NC, Anderson PJ, Doyle LW. J Rates of early intervention services in very preterm children with developmental disabilities at age 2 years. Paediatr Child Health. 2008;44:276–80.CrossRef
39.
go back to reference Estep ME, Smyser CD, Anderson PJ, Ortinau CM, Wallendorf M, Katzman CS, et al. Diffusion tractography and neuromotor outcome in very preterm children with white matter abnormalities. Pediatr Res. 2014;76:86–92.CrossRefPubMedPubMedCentral Estep ME, Smyser CD, Anderson PJ, Ortinau CM, Wallendorf M, Katzman CS, et al. Diffusion tractography and neuromotor outcome in very preterm children with white matter abnormalities. Pediatr Res. 2014;76:86–92.CrossRefPubMedPubMedCentral
40.
go back to reference Shimony JS, Burton H, Epstein AA, McLaren DG, Sun SW, Snyder AZ. Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb Cortex. 2006;16:1653–61.CrossRefPubMed Shimony JS, Burton H, Epstein AA, McLaren DG, Sun SW, Snyder AZ. Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb Cortex. 2006;16:1653–61.CrossRefPubMed
41.
go back to reference Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A. 1999;96:10422–7.CrossRefPubMedPubMedCentral Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A. 1999;96:10422–7.CrossRefPubMedPubMedCentral
42.
go back to reference Bender R, Lange S. Adjusting for multiple testing—when and how? J Clin Epidemiol. 2001;54:343–9.CrossRefPubMed Bender R, Lange S. Adjusting for multiple testing—when and how? J Clin Epidemiol. 2001;54:343–9.CrossRefPubMed
43.
go back to reference Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, et al. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain. 2001;124:60–6.CrossRefPubMed Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, et al. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain. 2001;124:60–6.CrossRefPubMed
44.
go back to reference van Kooij BJ, Benders MJ, Anbeek P, Van Haastert IC, De Vries LS, Groenendaal F. Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol. 2012;54:260–6.CrossRefPubMed van Kooij BJ, Benders MJ, Anbeek P, Van Haastert IC, De Vries LS, Groenendaal F. Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol. 2012;54:260–6.CrossRefPubMed
45.
go back to reference Constable RT, Ment LR, Vohr BR, Kesler SR, Fulbright RK, Lacadie C, et al. Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: an investigation of group and gender effects. Pediatrics. 2008;121:306–16.CrossRefPubMed Constable RT, Ment LR, Vohr BR, Kesler SR, Fulbright RK, Lacadie C, et al. Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: an investigation of group and gender effects. Pediatrics. 2008;121:306–16.CrossRefPubMed
46.
go back to reference van Kooij BJ, van Pul C, Benders MJ, van Haastert IC, de Vries LS, Groenendaal F. Fiber tracking at term displays gender differences regarding cognitive and motor outcome at 2 years of age in preterm infants. Pediatr Res. 2011;70:626–32.CrossRefPubMed van Kooij BJ, van Pul C, Benders MJ, van Haastert IC, de Vries LS, Groenendaal F. Fiber tracking at term displays gender differences regarding cognitive and motor outcome at 2 years of age in preterm infants. Pediatr Res. 2011;70:626–32.CrossRefPubMed
47.
go back to reference Allin MP, Kontis D, Walshe M, Wyatt J, Barker GJ, Kanaan RA, et al. White matter and cognition in adults who were born preterm. PLoS One. 2011;6, e24525.CrossRefPubMedPubMedCentral Allin MP, Kontis D, Walshe M, Wyatt J, Barker GJ, Kanaan RA, et al. White matter and cognition in adults who were born preterm. PLoS One. 2011;6, e24525.CrossRefPubMedPubMedCentral
48.
go back to reference Counsell SJ, Edwards AD, Chew AT, Anjari M, Dyet LE, Srinivasan L, et al. Specific relations between neurodevelopmental abilities and white matter microstructure in children born preterm. Brain. 2008;131:3201–8.CrossRefPubMed Counsell SJ, Edwards AD, Chew AT, Anjari M, Dyet LE, Srinivasan L, et al. Specific relations between neurodevelopmental abilities and white matter microstructure in children born preterm. Brain. 2008;131:3201–8.CrossRefPubMed
49.
go back to reference Hanaie R, Mohri I, Kagitani-Shimono K, Tachibana M, Azuma J, Matsuzaki J, et al. Altered microstructural connectivity of the superior cerebellar peduncle is related to motor dysfunction in children with autistic spectrum disorders. Cerebellum. 2013;12:645–56.CrossRefPubMed Hanaie R, Mohri I, Kagitani-Shimono K, Tachibana M, Azuma J, Matsuzaki J, et al. Altered microstructural connectivity of the superior cerebellar peduncle is related to motor dysfunction in children with autistic spectrum disorders. Cerebellum. 2013;12:645–56.CrossRefPubMed
50.
go back to reference Gelinas JN, Fitzpatrick KP, Kim HC, Bjornson BH. Cerebellar language mapping and cerebral language dominance in pediatric epilepsy surgery patients. Neuroimage Clin. 2014;12:296–306.CrossRef Gelinas JN, Fitzpatrick KP, Kim HC, Bjornson BH. Cerebellar language mapping and cerebral language dominance in pediatric epilepsy surgery patients. Neuroimage Clin. 2014;12:296–306.CrossRef
51.
go back to reference Beaulieu C. The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed. 2002;15:435–55.CrossRefPubMed Beaulieu C. The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed. 2002;15:435–55.CrossRefPubMed
52.
go back to reference Szaflarski JP, Rajagopal A, Altaye M, Byars AW, Jacola L, Schmithorst VJ, et al. Left-handedness and language lateralization in children. Brain Res. 2012;1433:85–97.CrossRefPubMed Szaflarski JP, Rajagopal A, Altaye M, Byars AW, Jacola L, Schmithorst VJ, et al. Left-handedness and language lateralization in children. Brain Res. 2012;1433:85–97.CrossRefPubMed
53.
go back to reference Johnson RT, Yeatman JD, Wandell BA, Buonocore MH, Amaral DG, Nordahl CW. Diffusion properties of major white matter tracts in young, typically developing children. NeuroImage. 2014;88:143–54.CrossRefPubMed Johnson RT, Yeatman JD, Wandell BA, Buonocore MH, Amaral DG, Nordahl CW. Diffusion properties of major white matter tracts in young, typically developing children. NeuroImage. 2014;88:143–54.CrossRefPubMed
54.
go back to reference Trivedi R, Agarwal S, Rathore RK, Saksena S, Tripathi RP, Malik GK, et al. Understanding development and lateralization of major cerebral fiber bundles in pediatric population through quantitative diffusion tensor tractography. Pediatr Res. 2009;66:636–41.CrossRefPubMed Trivedi R, Agarwal S, Rathore RK, Saksena S, Tripathi RP, Malik GK, et al. Understanding development and lateralization of major cerebral fiber bundles in pediatric population through quantitative diffusion tensor tractography. Pediatr Res. 2009;66:636–41.CrossRefPubMed
55.
go back to reference Sivaswamy L, Kumar A, Rajan D, Behen M, Muzik O, Chugani D, et al. A diffusion tensor imaging study of the cerebellar pathways in children with autism spectrum disorder. J Child Neurol. 2010;25:1223–31.CrossRefPubMed Sivaswamy L, Kumar A, Rajan D, Behen M, Muzik O, Chugani D, et al. A diffusion tensor imaging study of the cerebellar pathways in children with autism spectrum disorder. J Child Neurol. 2010;25:1223–31.CrossRefPubMed
56.
go back to reference Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, et al. Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain. 2008;131:1344–51.CrossRefPubMed Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, et al. Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain. 2008;131:1344–51.CrossRefPubMed
Metadata
Title
Diffusion Tensor Tractography of the Cerebellar Peduncles in Prematurely Born 7-Year-Old Children
Authors
Eilon Shany
Terrie E. Inder
Sharon Goshen
Iris Lee
Jeffrey J. Neil
Christopher D. Smyser
Lex W. Doyle
Peter J. Anderson
Joshua S. Shimony
Publication date
01-04-2017
Publisher
Springer US
Published in
The Cerebellum / Issue 2/2017
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-016-0796-7

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