Skip to main content
Top
Published in: Brain Structure and Function 4/2017

Open Access 01-05-2017 | Original Article

Cerebello-cerebral connectivity in the developing brain

Authors: Kay Pieterman, Dafnis Batalle, Jeroen Dudink, J-Donald Tournier, Emer J. Hughes, Madeleine Barnett, Manon J. Benders, A. David Edwards, Freek E. Hoebeek, Serena J. Counsell

Published in: Brain Structure and Function | Issue 4/2017

Login to get access

Abstract

Disrupted cerebellar development and injury is associated with impairments in both motor and non-motor domains. Methods to non-invasively characterize cerebellar afferent and efferent connections during early development are lacking. The aim of this study was to assess the feasibility of delineating cortico-ponto-cerebellar (CPC) and cerebello-thalamo-cortical (CTC) white matter tracts during brain development using high angular resolution diffusion imaging (HARDI). HARDI data were obtained in 24 infants born between 24+6 and 39 weeks gestational age (median 33+4 weeks) and scanned between 29+1 and 44 weeks postmenstrual age (PMA) (median 37+1 weeks). Probabilistic tractography of CPC and CTC fibers was performed using constrained spherical deconvolution. Connections between cerebellum and contralateral cerebral hemisphere were identified in all infants studied. Fractional anisotropy (FA) values of CTC and CPC pathways increased with increasing PMA at scan (p < 0.001). The supratentorial regions connecting to contralateral cerebellum in most subjects, irrespective of PMA at scan, included the precentral cortex, superior frontal cortex, supplementary motor area, insula, postcentral cortex, precuneus, and paracentral lobule. This study demonstrates the feasibility of assessing CTC and CPC white matter connectivity in vivo during the early stages of development. The ability to assess cerebellar connectivity during this critical developmental period may help improve our understanding of the role of the cerebellum in a wide range of neuromotor and neurocognitive disorders.
Appendix
Available only for authorised users
Literature
go back to reference Alexander DC, Barker GJ (2005) Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 27:357–367CrossRefPubMed Alexander DC, Barker GJ (2005) Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 27:357–367CrossRefPubMed
go back to reference Angaut P, Cicirata F, Serapide F (1985) Topographic organization of the cerebellothalamic projections in the rat. An autoradiographic study. Neuroscience 15:389–401CrossRefPubMed Angaut P, Cicirata F, Serapide F (1985) Topographic organization of the cerebellothalamic projections in the rat. An autoradiographic study. Neuroscience 15:389–401CrossRefPubMed
go back to reference Arnts H, Kleinnijenhuis M, Kooloos JG, Schepens-Franke AN, van Cappellen van Walsum AM (2014) Combining fiber dissection, plastination, and tractography for neuroanatomical education: revealing the cerebellar nuclei and their white matter connections. Anat Sci Educ 7:47–55CrossRefPubMed Arnts H, Kleinnijenhuis M, Kooloos JG, Schepens-Franke AN, van Cappellen van Walsum AM (2014) Combining fiber dissection, plastination, and tractography for neuroanatomical education: revealing the cerebellar nuclei and their white matter connections. Anat Sci Educ 7:47–55CrossRefPubMed
go back to reference Bamiou DE, Musiek FE, Luxon LM (2003) The insula (Island of Reil) and its role in auditory processing. Literature review. Brain Res Brain Res Rev 42:143–154CrossRefPubMed Bamiou DE, Musiek FE, Luxon LM (2003) The insula (Island of Reil) and its role in auditory processing. Literature review. Brain Res Brain Res Rev 42:143–154CrossRefPubMed
go back to reference Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507CrossRef Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507CrossRef
go back to reference Berquin PC, Giedd JN, Jacobsen LK, Hamburger SD, Krain AL, Rapoport JL, Castellanos FX (1998) Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology 50:1087–1093CrossRefPubMed Berquin PC, Giedd JN, Jacobsen LK, Hamburger SD, Krain AL, Rapoport JL, Castellanos FX (1998) Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology 50:1087–1093CrossRefPubMed
go back to reference Bledsoe JC, Semrud-Clikeman M, Pliszka SR (2011) Neuroanatomical and neuropsychological correlates of the cerebellum in children with attention-deficit/hyperactivity disorder–combined type. J Am Acad Child Adolesc Psychiatry 50:593–601CrossRefPubMedPubMedCentral Bledsoe JC, Semrud-Clikeman M, Pliszka SR (2011) Neuroanatomical and neuropsychological correlates of the cerebellum in children with attention-deficit/hyperactivity disorder–combined type. J Am Acad Child Adolesc Psychiatry 50:593–601CrossRefPubMedPubMedCentral
go back to reference Braga RM, Roze E, Ball G, Merchant N, Tusor N, Arichi T, Edwards D, Rueckert D, Counsell SJ (2015) Development of the corticospinal and callosal tracts from extremely premature birth up to 2 years of age. PLoS One 10:e0125681CrossRefPubMedPubMedCentral Braga RM, Roze E, Ball G, Merchant N, Tusor N, Arichi T, Edwards D, Rueckert D, Counsell SJ (2015) Development of the corticospinal and callosal tracts from extremely premature birth up to 2 years of age. PLoS One 10:e0125681CrossRefPubMedPubMedCentral
go back to reference Brooks JC, Zambreanu L, Godinez A, Craig AD, Tracey I (2005) Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. Neuroimage 27:201–209CrossRefPubMed Brooks JC, Zambreanu L, Godinez A, Craig AD, Tracey I (2005) Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. Neuroimage 27:201–209CrossRefPubMed
go back to reference Buckner RL (2013) The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80:807–815CrossRefPubMed Buckner RL (2013) The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80:807–815CrossRefPubMed
go back to reference Bui T, Daire JL, Chalard F, Zaccaria I, Alberti C, Elmaleh M, Garel C, Luton D, Blanc N, Sebag G (2006) Microstructural development of human brain assessed in utero by diffusion tensor imaging. Pediatr Radiol 36:1133–1140CrossRefPubMed Bui T, Daire JL, Chalard F, Zaccaria I, Alberti C, Elmaleh M, Garel C, Luton D, Blanc N, Sebag G (2006) Microstructural development of human brain assessed in utero by diffusion tensor imaging. Pediatr Radiol 36:1133–1140CrossRefPubMed
go back to reference Carper RA, Courchesne E (2000) Inverse correlation between frontal lobe and cerebellum sizes in children with autism. Brain 123(Pt 4):836–844CrossRefPubMed Carper RA, Courchesne E (2000) Inverse correlation between frontal lobe and cerebellum sizes in children with autism. Brain 123(Pt 4):836–844CrossRefPubMed
go back to reference Chang CH, Chang FM, Yu CH, Ko HC, Chen HY (2000) Assessment of fetal cerebellar volume using three-dimensional ultrasound. Ultrasound Med Biol 26:981–988CrossRefPubMed Chang CH, Chang FM, Yu CH, Ko HC, Chen HY (2000) Assessment of fetal cerebellar volume using three-dimensional ultrasound. Ultrasound Med Biol 26:981–988CrossRefPubMed
go back to reference Chouinard PA, Paus T (2006) The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12:143–152CrossRefPubMed Chouinard PA, Paus T (2006) The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12:143–152CrossRefPubMed
go back to reference Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL (1988) Hypoplasia of cerebellar vermal lobules VI and VII in autism. N Engl J Med 318:1349–1354CrossRefPubMed Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL (1988) Hypoplasia of cerebellar vermal lobules VI and VII in autism. N Engl J Med 318:1349–1354CrossRefPubMed
go back to reference Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70CrossRefPubMed Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70CrossRefPubMed
go back to reference Cutini S, Scatturin P, Menon E, Bisiacchi PS, Gamberini L, Zorzi M, Dell’Acqua R (2008) Selective activation of the superior frontal gyrus in task-switching: an event-related fNIRS study. Neuroimage 42:945–955CrossRefPubMed Cutini S, Scatturin P, Menon E, Bisiacchi PS, Gamberini L, Zorzi M, Dell’Acqua R (2008) Selective activation of the superior frontal gyrus in task-switching: an event-related fNIRS study. Neuroimage 42:945–955CrossRefPubMed
go back to reference D’Mello AM, Crocetti D, Mostofsky SH, Stoodley CJ (2015) Cerebellar gray matter and lobular volumes correlate with core autism symptoms. Neuroimage Clin 7:631–639CrossRefPubMedPubMedCentral D’Mello AM, Crocetti D, Mostofsky SH, Stoodley CJ (2015) Cerebellar gray matter and lobular volumes correlate with core autism symptoms. Neuroimage Clin 7:631–639CrossRefPubMedPubMedCentral
go back to reference du Boisgueheneuc F, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328CrossRefPubMed du Boisgueheneuc F, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328CrossRefPubMed
go back to reference Evarts EV, Thach WT (1969) Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annu Rev Physiol 31:451–498CrossRefPubMed Evarts EV, Thach WT (1969) Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annu Rev Physiol 31:451–498CrossRefPubMed
go back to reference Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A (2013) White matter fiber tractography: why we need to move beyond DTI. J Neurosurg 118:1367–1377CrossRefPubMed Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A (2013) White matter fiber tractography: why we need to move beyond DTI. J Neurosurg 118:1367–1377CrossRefPubMed
go back to reference Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, Chauhan A, Chauhan V, Dager SR, Dickson PE, Estes AM, Goldowitz D, Heck DH, Kemper TL, King BH, Martin LA, Millen KJ, Mittleman G, Mosconi MW, Persico AM, Sweeney JA, Webb SJ, Welsh JP (2012) Consensus paper: pathological role of the cerebellum in autism. Cerebellum 11:777–807CrossRefPubMedPubMedCentral Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, Chauhan A, Chauhan V, Dager SR, Dickson PE, Estes AM, Goldowitz D, Heck DH, Kemper TL, King BH, Martin LA, Millen KJ, Mittleman G, Mosconi MW, Persico AM, Sweeney JA, Webb SJ, Welsh JP (2012) Consensus paper: pathological role of the cerebellum in autism. Cerebellum 11:777–807CrossRefPubMedPubMedCentral
go back to reference Gao W, Lin W, Chen Y, Gerig G, Smith JK, Jewells V, Gilmore JH (2009) Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol 30:290–296CrossRefPubMed Gao W, Lin W, Chen Y, Gerig G, Smith JK, Jewells V, Gilmore JH (2009) Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol 30:290–296CrossRefPubMed
go back to reference Gao Y, Choe AS, Stepniewska I, Li X, Avison MJ, Anderson AW (2013) Validation of DTI tractography-based measures of primary motor area connectivity in the squirrel monkey brain. PLoS One 8:e75065CrossRefPubMedPubMedCentral Gao Y, Choe AS, Stepniewska I, Li X, Avison MJ, Anderson AW (2013) Validation of DTI tractography-based measures of primary motor area connectivity in the squirrel monkey brain. PLoS One 8:e75065CrossRefPubMedPubMedCentral
go back to reference Goldberg II, Harel M, Malach R (2006) When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 50:329–339CrossRefPubMed Goldberg II, Harel M, Malach R (2006) When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 50:329–339CrossRefPubMed
go back to reference Haines KM, Wang W, Pierson CR (2013) Cerebellar hemorrhagic injury in premature infants occurs during a vulnerable developmental period and is associated with wider neuropathology. Acta Neuropathol Commun 1:69CrossRefPubMedPubMedCentral Haines KM, Wang W, Pierson CR (2013) Cerebellar hemorrhagic injury in premature infants occurs during a vulnerable developmental period and is associated with wider neuropathology. Acta Neuropathol Commun 1:69CrossRefPubMedPubMedCentral
go back to reference Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2013) A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283–297CrossRefPubMedPubMedCentral Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2013) A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283–297CrossRefPubMedPubMedCentral
go back to reference Hubbard PL, Zhou FL, Eichhorn SJ, Parker GJ (2015) Biomimetic phantom for the validation of diffusion magnetic resonance imaging. Magn Reson Med 73:299–305CrossRefPubMed Hubbard PL, Zhou FL, Eichhorn SJ, Parker GJ (2015) Biomimetic phantom for the validation of diffusion magnetic resonance imaging. Magn Reson Med 73:299–305CrossRefPubMed
go back to reference Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590CrossRefPubMed Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590CrossRefPubMed
go back to reference Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254CrossRefPubMed Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254CrossRefPubMed
go back to reference Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM (2014a) Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219:269–281CrossRefPubMed Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM (2014a) Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219:269–281CrossRefPubMed
go back to reference Kamali A, Sair HI, Radmanesh A, Hasan KM (2014b) Decoding the superior parietal lobule connections of the superior longitudinal fasciculus/arcuate fasciculus in the human brain. Neuroscience 277:577–583CrossRefPubMed Kamali A, Sair HI, Radmanesh A, Hasan KM (2014b) Decoding the superior parietal lobule connections of the superior longitudinal fasciculus/arcuate fasciculus in the human brain. Neuroscience 277:577–583CrossRefPubMed
go back to reference Kersbergen KJ, Leemans A, Groenendaal F, van der Aa NE, Viergever MA, de Vries LS, Benders MJ (2014) Microstructural brain development between 30 and 40 weeks corrected age in a longitudinal cohort of extremely preterm infants. Neuroimage 103:214–224CrossRefPubMed Kersbergen KJ, Leemans A, Groenendaal F, van der Aa NE, Viergever MA, de Vries LS, Benders MJ (2014) Microstructural brain development between 30 and 40 weeks corrected age in a longitudinal cohort of extremely preterm infants. Neuroimage 103:214–224CrossRefPubMed
go back to reference Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29:14980–14986CrossRefPubMedPubMedCentral Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29:14980–14986CrossRefPubMedPubMedCentral
go back to reference Kucyi A, Hove MJ, Biederman J, Van Dijk KR, Valera EM (2015) Disrupted functional connectivity of cerebellar default network areas in attention-deficit/hyperactivity disorder. Hum Brain Mapp 36:3373–3386CrossRefPubMedPubMedCentral Kucyi A, Hove MJ, Biederman J, Van Dijk KR, Valera EM (2015) Disrupted functional connectivity of cerebellar default network areas in attention-deficit/hyperactivity disorder. Hum Brain Mapp 36:3373–3386CrossRefPubMedPubMedCentral
go back to reference Law N, Bouffet E, Laughlin S, Laperriere N, Briere ME, Strother D, McConnell D, Hukin J, Fryer C, Rockel C, Dickson J, Mabbott D (2011) Cerebello-thalamo-cerebral connections in pediatric brain tumor patients: impact on working memory. Neuroimage 56:2238–2248CrossRefPubMed Law N, Bouffet E, Laughlin S, Laperriere N, Briere ME, Strother D, McConnell D, Hukin J, Fryer C, Rockel C, Dickson J, Mabbott D (2011) Cerebello-thalamo-cerebral connections in pediatric brain tumor patients: impact on working memory. Neuroimage 56:2238–2248CrossRefPubMed
go back to reference Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ (2005a) Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics 116:717–724CrossRefPubMed Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ (2005a) Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics 116:717–724CrossRefPubMed
go back to reference Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ (2005b) Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 115:688–695CrossRefPubMed Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ (2005b) Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 115:688–695CrossRefPubMed
go back to reference Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ (2005c) Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 116:844–850CrossRefPubMed Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ (2005c) Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 116:844–850CrossRefPubMed
go back to reference Limperopoulos C, Bassan H, Gauvreau K, Robertson RL Jr, Sullivan NR, Benson CB, Avery L, Stewart J, Soul JS, Ringer SA, Volpe JJ, duPlessis AJ (2007) Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 120:584–593CrossRefPubMed Limperopoulos C, Bassan H, Gauvreau K, Robertson RL Jr, Sullivan NR, Benson CB, Avery L, Stewart J, Soul JS, Ringer SA, Volpe JJ, duPlessis AJ (2007) Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 120:584–593CrossRefPubMed
go back to reference Limperopoulos C, Robertson RL, Sullivan NR, Bassan H, du Plessis AJ (2009) Cerebellar injury in term infants: clinical characteristics, magnetic resonance imaging findings, and outcome. Pediatr Neurol 41:1–8CrossRefPubMed Limperopoulos C, Robertson RL, Sullivan NR, Bassan H, du Plessis AJ (2009) Cerebellar injury in term infants: clinical characteristics, magnetic resonance imaging findings, and outcome. Pediatr Neurol 41:1–8CrossRefPubMed
go back to reference Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ (2010) Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res 68:145–150CrossRefPubMed Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ (2010) Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res 68:145–150CrossRefPubMed
go back to reference Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ (2014) Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex 24:728–736CrossRefPubMed Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ (2014) Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex 24:728–736CrossRefPubMed
go back to reference Makropoulos A, Gousias IS, Ledig C, Aljabar P, Serag A, Hajnal JV, Edwards AD, Counsell SJ, Rueckert D (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE Trans Med Imaging 33:1818–1831CrossRefPubMed Makropoulos A, Gousias IS, Ledig C, Aljabar P, Serag A, Hajnal JV, Edwards AD, Counsell SJ, Rueckert D (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE Trans Med Imaging 33:1818–1831CrossRefPubMed
go back to reference Marko MK, Crocetti D, Hulst T, Donchin O, Shadmehr R, Mostofsky SH (2015) Behavioural and neural basis of anomalous motor learning in children with autism. Brain 138:784–797CrossRefPubMedPubMedCentral Marko MK, Crocetti D, Hulst T, Donchin O, Shadmehr R, Mostofsky SH (2015) Behavioural and neural basis of anomalous motor learning in children with autism. Brain 138:784–797CrossRefPubMedPubMedCentral
go back to reference Martin GF, Cabana T, Hazlett JC, Ho R, Waltzer R (1987) Development of brainstem and cerebellar projections to the diencephalon with notes on thalamocortical projections: studies in the North American opossum. J Comp Neurol 260:186–200CrossRefPubMed Martin GF, Cabana T, Hazlett JC, Ho R, Waltzer R (1987) Development of brainstem and cerebellar projections to the diencephalon with notes on thalamocortical projections: studies in the North American opossum. J Comp Neurol 260:186–200CrossRefPubMed
go back to reference Messerschmidt A, Fuiko R, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Weber M, Birnbacher R (2008) Disrupted cerebellar development in preterm infants is associated with impaired neurodevelopmental outcome. Eur J Pediatr 167:1141–1147CrossRefPubMed Messerschmidt A, Fuiko R, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Weber M, Birnbacher R (2008) Disrupted cerebellar development in preterm infants is associated with impaired neurodevelopmental outcome. Eur J Pediatr 167:1141–1147CrossRefPubMed
go back to reference Naidich TP, Duvernoy HM, Delman BN, Sorensen AG, Kollias SS, Haacke EM (2008) Duvernoy’s atlas of the human brain stem and cerebellum. Springer, Berlin Naidich TP, Duvernoy HM, Delman BN, Sorensen AG, Kollias SS, Haacke EM (2008) Duvernoy’s atlas of the human brain stem and cerebellum. Springer, Berlin
go back to reference Palesi F, Tournier JD, Calamante F, Muhlert N, Castellazzi G, Chard D, D’Angelo E, Wheeler-Kingshott CA (2015) Contralateral cerebello-thalamo-cortical pathways with prominent involvement of associative areas in humans in vivo. Brain Struct Funct 220:3369–3384CrossRefPubMed Palesi F, Tournier JD, Calamante F, Muhlert N, Castellazzi G, Chard D, D’Angelo E, Wheeler-Kingshott CA (2015) Contralateral cerebello-thalamo-cortical pathways with prominent involvement of associative areas in humans in vivo. Brain Struct Funct 220:3369–3384CrossRefPubMed
go back to reference Perrini P, Tiezzi G, Castagna M, Vannozzi R (2013) Three-dimensional microsurgical anatomy of cerebellar peduncles. Neurosurg Rev 36:215–224 (discussion 224–225) CrossRefPubMed Perrini P, Tiezzi G, Castagna M, Vannozzi R (2013) Three-dimensional microsurgical anatomy of cerebellar peduncles. Neurosurg Rev 36:215–224 (discussion 224–225) CrossRefPubMed
go back to reference Potgieser AR, de Jong BM, Wagemakers M, Hoving EW, Groen RJ (2014) Insights from the supplementary motor area syndrome in balancing movement initiation and inhibition. Front Hum Neurosci 8:960CrossRefPubMedPubMedCentral Potgieser AR, de Jong BM, Wagemakers M, Hoving EW, Groen RJ (2014) Insights from the supplementary motor area syndrome in balancing movement initiation and inhibition. Front Hum Neurosci 8:960CrossRefPubMedPubMedCentral
go back to reference Ranger M, Zwicker JG, Chau CM, Park MT, Chakravarthy MM, Poskitt K, Miller SP, Bjornson BH, Tam EW, Chau V, Synnes AR, Grunau RE (2015) Neonatal pain and infection relate to smaller cerebellum in very preterm children at school age. J Pediatr 167:292–298CrossRefPubMed Ranger M, Zwicker JG, Chau CM, Park MT, Chakravarthy MM, Poskitt K, Miller SP, Bjornson BH, Tam EW, Chau V, Synnes AR, Grunau RE (2015) Neonatal pain and infection relate to smaller cerebellum in very preterm children at school age. J Pediatr 167:292–298CrossRefPubMed
go back to reference Sander K, Scheich H (2005) Left auditory cortex and amygdala, but right insula dominance for human laughing and crying. J Cogn Neurosci 17:1519–1531CrossRefPubMed Sander K, Scheich H (2005) Left auditory cortex and amygdala, but right insula dominance for human laughing and crying. J Cogn Neurosci 17:1519–1531CrossRefPubMed
go back to reference Sawyer SF, Young SJ, Groves PM, Tepper JM (1994) Cerebellar-responsive neurons in the thalamic ventroanterior-ventrolateral complex of rats: in vivo electrophysiology. Neuroscience 63:711–724CrossRefPubMed Sawyer SF, Young SJ, Groves PM, Tepper JM (1994) Cerebellar-responsive neurons in the thalamic ventroanterior-ventrolateral complex of rats: in vivo electrophysiology. Neuroscience 63:711–724CrossRefPubMed
go back to reference Seehaus AK, Roebroeck A, Chiry O, Kim DS, Ronen I, Bratzke H, Goebel R, Galuske RA (2013) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex 23:442–450CrossRefPubMed Seehaus AK, Roebroeck A, Chiry O, Kim DS, Ronen I, Bratzke H, Goebel R, Galuske RA (2013) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex 23:442–450CrossRefPubMed
go back to reference Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M (2006) Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 27:573–579PubMed Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M (2006) Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 27:573–579PubMed
go back to reference Steggerda SJ, De Bruine FT, van den Berg-Huysmans AA, Rijken M, Leijser LM, Walther FJ, van Wezel-Meijler G (2013) Small cerebellar hemorrhage in preterm infants: perinatal and postnatal factors and outcome. Cerebellum 12:794–801CrossRefPubMed Steggerda SJ, De Bruine FT, van den Berg-Huysmans AA, Rijken M, Leijser LM, Walther FJ, van Wezel-Meijler G (2013) Small cerebellar hemorrhage in preterm infants: perinatal and postnatal factors and outcome. Cerebellum 12:794–801CrossRefPubMed
go back to reference Steinbrink C, Ackermann H, Lachmann T, Riecker A (2009) Contribution of the anterior insula to temporal auditory processing deficits in developmental dyslexia. Hum Brain Mapp 30:2401–2411CrossRefPubMed Steinbrink C, Ackermann H, Lachmann T, Riecker A (2009) Contribution of the anterior insula to temporal auditory processing deficits in developmental dyslexia. Hum Brain Mapp 30:2401–2411CrossRefPubMed
go back to reference Takahashi M, Iwamoto K, Fukatsu H, Naganawa S, Iidaka T, Ozaki N (2010) White matter microstructure of the cingulum and cerebellar peduncle is related to sustained attention and working memory: a diffusion tensor imaging study. Neurosci Lett 477:72–76CrossRefPubMed Takahashi M, Iwamoto K, Fukatsu H, Naganawa S, Iidaka T, Ozaki N (2010) White matter microstructure of the cingulum and cerebellar peduncle is related to sustained attention and working memory: a diffusion tensor imaging study. Neurosci Lett 477:72–76CrossRefPubMed
go back to reference Takahashi E, Hayashi E, Schmahmann JD, Grant PE (2014) Development of cerebellar connectivity in human fetal brains revealed by high angular resolution diffusion tractography. Neuroimage 96:326–333CrossRefPubMedPubMedCentral Takahashi E, Hayashi E, Schmahmann JD, Grant PE (2014) Development of cerebellar connectivity in human fetal brains revealed by high angular resolution diffusion tractography. Neuroimage 96:326–333CrossRefPubMedPubMedCentral
go back to reference Tavano A, Grasso R, Gagliardi C, Triulzi F, Bresolin N, Fabbro F, Borgatti R (2007) Disorders of cognitive and affective development in cerebellar malformations. Brain 130:2646–2660CrossRefPubMed Tavano A, Grasso R, Gagliardi C, Triulzi F, Bresolin N, Fabbro F, Borgatti R (2007) Disorders of cognitive and affective development in cerebellar malformations. Brain 130:2646–2660CrossRefPubMed
go back to reference Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ (2000) Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res 124:141–172CrossRefPubMed Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ (2000) Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res 124:141–172CrossRefPubMed
go back to reference Timmann D, Drepper J, Frings M, Maschke M, Richter S, Gerwig M, Kolb FP (2010) The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex 46:845–857CrossRefPubMed Timmann D, Drepper J, Frings M, Maschke M, Richter S, Gerwig M, Kolb FP (2010) The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex 46:845–857CrossRefPubMed
go back to reference Tomasi D, Volkow ND (2012) Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71:443–450CrossRefPubMed Tomasi D, Volkow ND (2012) Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71:443–450CrossRefPubMed
go back to reference Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35:1459–1472CrossRefPubMed Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35:1459–1472CrossRefPubMed
go back to reference Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008) Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42:617–625CrossRefPubMed Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008) Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42:617–625CrossRefPubMed
go back to reference Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53–66CrossRef Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53–66CrossRef
go back to reference Tournier JD, Calamante F, Connelly A (2013) Determination of the appropriate b value and number of gradient directions for high-angular-resolution diffusion-weighted imaging. NMR Biomed 26:1775–1786CrossRefPubMed Tournier JD, Calamante F, Connelly A (2013) Determination of the appropriate b value and number of gradient directions for high-angular-resolution diffusion-weighted imaging. NMR Biomed 26:1775–1786CrossRefPubMed
go back to reference Tristan-Vega A, Arribas JI (2007) A fast B-spline Pseudo-inversion algorithm for consistent image registration. In: Proceedings of the international conference on computer analysis images and patterns (CAIP), Vienna, Austria, pp 768–775 Tristan-Vega A, Arribas JI (2007) A fast B-spline Pseudo-inversion algorithm for consistent image registration. In: Proceedings of the international conference on computer analysis images and patterns (CAIP), Vienna, Austria, pp 768–775
go back to reference Tully LM, Lincoln SH, Liyanage-Don N, Hooker CI (2014) Impaired cognitive control mediates the relationship between cortical thickness of the superior frontal gyrus and role functioning in schizophrenia. Schizophr Res 152:358–364CrossRefPubMed Tully LM, Lincoln SH, Liyanage-Don N, Hooker CI (2014) Impaired cognitive control mediates the relationship between cortical thickness of the superior frontal gyrus and role functioning in schizophrenia. Schizophr Res 152:358–364CrossRefPubMed
go back to reference Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16:55–61CrossRefPubMed Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16:55–61CrossRefPubMed
go back to reference van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlaan J (2012) Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 36:1093–1106CrossRefPubMed van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlaan J (2012) Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 36:1093–1106CrossRefPubMed
go back to reference Wang X, Jiao Y, Tang T, Wang H, Lu Z (2013) Altered regional homogeneity patterns in adults with attention-deficit hyperactivity disorder. Eur J Radiol 82:1552–1557CrossRefPubMed Wang X, Jiao Y, Tang T, Wang H, Lu Z (2013) Altered regional homogeneity patterns in adults with attention-deficit hyperactivity disorder. Eur J Radiol 82:1552–1557CrossRefPubMed
go back to reference Wang J, Yang Y, Fan L, Xu J, Li C, Liu Y, Fox PT, Eickhoff SB, Yu C, Jiang T (2015) Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches. Hum Brain Mapp 36:238–257CrossRefPubMed Wang J, Yang Y, Fan L, Xu J, Li C, Liu Y, Fox PT, Eickhoff SB, Yu C, Jiang T (2015) Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches. Hum Brain Mapp 36:238–257CrossRefPubMed
go back to reference Warfield SK, Guimond A, Roche A, Bharatha A, Tei A, Talos F, Rexilius J, Ruiz-Alzola J, Westin C-F, Haker S, Angenent S, Tannenbaum A, Jolesz F, Kikinis R (2002) Advanced nonrigid registration algorithms for image fusion. In: Mazziotta AWTC (ed) Brain mapping: the methods, 2nd edn. Academic Press, San Diego, pp 661–690CrossRef Warfield SK, Guimond A, Roche A, Bharatha A, Tei A, Talos F, Rexilius J, Ruiz-Alzola J, Westin C-F, Haker S, Angenent S, Tannenbaum A, Jolesz F, Kikinis R (2002) Advanced nonrigid registration algorithms for image fusion. In: Mazziotta AWTC (ed) Brain mapping: the methods, 2nd edn. Academic Press, San Diego, pp 661–690CrossRef
go back to reference Wegiel J, Flory M, Kuchna I, Nowicki K, Ma SY, Imaki H, Wegiel J, Cohen IL, London E, Wisniewski T, Brown WT (2014) Stereological study of the neuronal number and volume of 38 brain subdivisions of subjects diagnosed with autism reveals significant alterations restricted to the striatum, amygdala and cerebellum. Acta Neuropathol Commun 2:141CrossRefPubMedPubMedCentral Wegiel J, Flory M, Kuchna I, Nowicki K, Ma SY, Imaki H, Wegiel J, Cohen IL, London E, Wisniewski T, Brown WT (2014) Stereological study of the neuronal number and volume of 38 brain subdivisions of subjects diagnosed with autism reveals significant alterations restricted to the striatum, amygdala and cerebellum. Acta Neuropathol Commun 2:141CrossRefPubMedPubMedCentral
go back to reference Zayek MM, Benjamin JT, Maertens P, Trimm RF, Lal CV, Eyal FG (2012) Cerebellar hemorrhage: a major morbidity in extremely preterm infants. J Perinatol 32:699–704CrossRefPubMed Zayek MM, Benjamin JT, Maertens P, Trimm RF, Lal CV, Eyal FG (2012) Cerebellar hemorrhage: a major morbidity in extremely preterm infants. J Perinatol 32:699–704CrossRefPubMed
Metadata
Title
Cerebello-cerebral connectivity in the developing brain
Authors
Kay Pieterman
Dafnis Batalle
Jeroen Dudink
J-Donald Tournier
Emer J. Hughes
Madeleine Barnett
Manon J. Benders
A. David Edwards
Freek E. Hoebeek
Serena J. Counsell
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1296-8

Other articles of this Issue 4/2017

Brain Structure and Function 4/2017 Go to the issue