Injury to the premature cerebellum: Outcome is related to remote cortical development

Cerebral Cortex

Volumn 24, Issue 3, 2014, Pages 728-736

  Limperopoulos, Catherine ^a,b   Chilingaryan, Gevorg ^c   Sullivan, Nancy ^d   Guizard, Nicolas ^f   Robertson, Richard L ^e   Du Plessis, Adré J ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c JEWISH REHABILITATION HOSPITAL   (Canada)

^d Division of Developmental Medicine   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f MCGILL UNIVERSITY   (Canada)

Author keywords

cerebellum; cerebral cortex; magnetic resonance imaging; outcome; preterm

Indexed keywords

CEREBELLUM; CEREBRAL CORTEX; MAGNETIC RESONANCE IMAGING; OUTCOME; PRETERM;

BRAIN MAPPING; CEREBELLAR DISEASES; CEREBRAL CORTEX; CHILD; CHILD, PRESCHOOL; DEVELOPMENTAL DISABILITIES; FEMALE; FOLLOW-UP STUDIES; FUNCTIONAL LATERALITY; HUMANS; INFANT; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PROSPECTIVE STUDIES; RETROSPECTIVE STUDIES;

EID: 84894265209     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs354     Document Type: Article

References (62)

1. Barbas H, Mesulam MM. 1985. Cortical afferent input to the principals region of the rhesus monkey. Neuroscience. 15(3):619-637.
2. Beebe DW, Ris MD, Armstrong FD, Fontanesi J, Mulhern R, Holmes E, Wisoff JH. 2005. Cognitive and adaptive outcome in low-grade pediatric cerebellar astrocytomas: evidence of diminished cognitive and adaptive functioning in National Collaborative Research Studies (CCG 9891/POG 9130). J Clin Oncol. 23(22):5198-5204.
3. Biran V, Bodiou AM, Zana E, Gaudin A, Farnoux C, Hovhannisyan S, Alison M, Elmaleh M, Oury JF, Maury L et al. 2011. Cerebellar injury in premature infants less than 30 weeks of gestation. Arch Pediatr. 18(3):261-266.
4. Bloedel JR, Bracha V, Larson PS. 1993. Real time operations of the cerebellar cortex. Can J Neurol Sci. 20(Suppl 3):S7-S18.
5. Bolduc ME, Du Plessis AJ, Evans A, Guizard N, Zhang X, Robertson RL, Limperopoulos C. 2011. Cerebellar malformations alter regional cerebral development. Dev Med Child Neurol. 53 (12):1128-1134.
6. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 9 (2):110-122.
7. Cavada C, Goldman-Rakic PS. 1989. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol. 287(4):422-445.
8. Chechlacz M, Rotshtein P, Hansen PC, Riddoch JM, Deb S, Humphreys GW. 2012. The neural underpinings of simultanagnosia: disconnecting the visuospatial attention network. J Cogn Neurosci. 24(3):718-735.
9. Chugani HT, Phelps ME, Mazziotta JC. 1987. Positron emission tomography study of human brain functional development. Ann Neurol. 22(4):487-497.
10. Clower DM, West RA, Lynch JC, Strick PL. 2001. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 21(16):6283-6291.
11. Dubois J, Benders M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF, Huppi PS. 2008. Primary cortical folding in the human newborn: an early marker of later functional development. Brain. 131(Pt 8):2028-2041.
12. Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, Duggan PJ, Harrison M, Allsop JM, Hajnal J, Herlihy AH et al. 2006. Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics. 118(2):536-548.
13. Eblen F, Graybiel AM. 1995. Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci. 15 (9):5999-6013.
14. Evans AC, Collins DL, Mills SR, Brown ED, Kelly RL, Peters TM. 1993. 3D statistical neuroanatomical models from 305 MRI volumes. Proc IEEE Nucl Sci Symp Med Imaging Conf. 1813-1817.
15. Folio R, Fewell R. 1983. Peabody development motor scales and activity cards. Austin (TX): DLM Teaching Resources.
16. Gesierich B, Jovicich J, Riello M, Adriani M, Monti A, Brentari V, Robinson SD, Wilson SM, Fairhall SL, Gorno-Tempini ML. 2012. Distinct neural substrates for semantic knowledge and naming in the temporoparietal network. Cereb Cortex. 22(10):2217-2226.
17. Giovagnoli AR, Aresi A, Reati F, Riva A, Gobbo C, Bizzi A. 2009. The neuropsychological and neuroradiological correlates of slowly progressive visual agnosia. Neurol Sci. 30(2):123-131.
18. Gottwald B, Wilde B, Mihajlovic Z, Mehdorn HM. 2004. Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry. 75(11):1524-1531.
19. Himmelmann K, Hagberg G, Beckung E, Hagberg B, Uvebrant P. 2005. The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth-year period 1995-1998.
20. Acta Paediatr. 94(3):287-294.
21. Hoekstra RE, Ferrara TB, Couser RJ, Payne NR, Connett JE. 2004. Survival and long-term neurodevelopmental outcome of extremely premature infants born at 23-26 weeks' gestational age at a tertiary center. Pediatrics. 113(1 Pt 1):e1-e6.
22. Ito M. 2008. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 9(4):304-313.
23. Kelly RM, Strick PL. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 23 (23):8432-8444.
24. Kent AL, Wright IM, Abdel-Latif ME; New South Wales and Australian Capital Territory Neonatal Intensive Care Units Audit Group. 2012. Mortality and adverse neurologic outcomes are greater in preterm male infants. Paediatrics. 129(1):124-131.
25. Kesler SR, Reiss AL, Vohr B, Watson C, Schneider KC, Katz KH, Maller-Kesselman J, Silbereis J, Constable RT, Makuch RWet al. 2008. Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. J Pediatr. 152(4):513-520, 520 e511.
26. Levisohn L, Cronin-Golomb A, Schmahmann JD. 2000. Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain. 123(Pt 5):1041-1050.
27. Limperopoulos C, Bassan H, Gauvreau K, Robertson RL Jr, Sullivan NR, Benson CB, Avery L, Stewart J, Soul JS, Ringer SA et al. 2007. Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics. 120(3):584-593.
28. Limperopoulos C, Bassan H, Sullivan NR, Soul JS, Robertson RL Jr, Moore M, Ringer SA, Volpe JJ, du Plessis AJ. 2008. Positive screening for autism in ex-preterm infants: prevalence and risk factors. Pediatrics. 121(4):758-765.
29. Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ. 2005. Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics. 116(3):717-724.
30. 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(2):145-150.
31. Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ et al. 2005. Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics. 116(4):844-850.
32. Lynch JC, Hoover JE, Strick PL. 1994. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res. 100(1):181-186.
33. Maddalena P, Gibbins S. 2008. Cerebellar hemorrhage in extremely low birth weight infants: incidence, risk factors, and impact on long-term outcomes. Neonatal Netw. 27(6):387-396.
34. McCarthy LK, Donoghue V, Murphy JF. 2011. Ultrasonically detectable cerebellar haemorrhage in preterm infants. Arch Dis Child Fetal Neonatal Ed. 96(4):F281-F285.
35. 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 (10):1141-1147.
36. Middleton FA, Strick PL. 1994. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 266(5184):458-461.
37. Middleton FA, Strick PL. 2001. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 21(2):700-712.
38. Middleton FA, Strick PL. 1998. The cerebellum: an overview. Trends Neurosci. 21(9):367-369.
39. Msall ME. 2006. Neurodevelopmental surveillance in the first 2 years after extremely preterm birth: evidence, challenges, and guidelines. Early Hum Dev. 82(3):157-166.
40. Mullen E. 1995. Mullen scales of early learning. Circle Pines (MN): American Guidance Services, Inc.
41. Peacock JL, Marston L, Marlow N, Calvert SA, Greenough A. 2012. Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res. 71(3):305-310.
42. Peterson BS, Anderson AW, Ehrenkranz R, Staib LH, Tageldin M, Colson E, Gore JC, Duncan CC, Makuch R, Ment LR. 2003. Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics. 111(5 Pt 1):939-948.
43. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW et al. 2000. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA. 284(15):1939-1947.
44. Ramnani N. 2006. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 7(7):511-522.
45. Reiss AL, Kesler SR, Vohr B, Duncan CC, Katz KH, Pajot S, Schneider KC, Makuch RW, Ment LR. 2004. Sex differences in cerebral volumes of 8-year-olds born preterm. J Pediatr. 145(2):242-249.
46. Robins DL, Fein D, Barton ML, Green JA. 2001. The Modified Checklist for Autism in Toddlers: an initial study investigating the early detection of autism and pervasive developmental disorders. J Autism Dev Disord. 31:131-144.
47. Schmahmann JD. 2004. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 16(3):367-378.
48. Schmahmann JD, Pandya DN. 1997b. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci. 17(1):438-458.
49. Schmahmann JD, Pandya DN. 1997a. The cerebrocerebellar system. Int Rev Neurobiol. 41:31-60.
50. Schmahmann JD, Pandya DN. 1993. Prelunate, occipitotemporal, and parahippocampal projections to the basis pontis in rhesus monkey. J Comp Neurol. 337(1):94-112.
51. Schmahmann JD, Pandya DN. 1991. Projections to the basis pontis from the superior temporal sulcus and superior temporal region in the rhesus monkey. J Comp Neurol. 308(2):224-248.
52. Schmahmann JD, Sherman JC. 1998. The cerebellar cognitive affective syndrome. Brain. 121(Pt 4):561-579.
53. Scott RB, Stoodley CJ, Anslow P, Paul C, Stein JF, Sugden EM, Mitchell CD. 2001. Lateralized cognitive deficits in children following cerebellar lesions. Dev Med Child Neurol. 43(10):685-691.
54. Smith GC, Gutovich J, Smyser C, Pineda R, Newnham C, Tjoeng TH, Vavasseur C, Wallendorf M, Neil J, Inder T. 2011. Neonatal intensive care unit stress is associated with brain development in preterm infants. Ann Neurol. 70(4):541-549.
55. Steggerda SJ, Leijser LM, Wiggers-de Bruine FT, van der Grond J, Walther FJ, van Wezel-Meijler G. 2009. Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology. 252(1):190-199.
56. Tam EW, Rosenbluth G, Rogers EE, Ferriero DM, Glidden D, Goldstein RB, Glass HC, Piecuch RE, Barkovich AJ. 2011. Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatr. 158 (2):245-250.
57. Tankus A, Fried I. 2012. Visuomotor coordination and motor representation by human temporal lobe neurons. J Cogn Neurosci. 24 (3):600-610.
58. 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(Pt 10):2646-2660.
59. Thompson DK, Warfield SK, Carlin JB, Pavlovic M, Wang HX, Bear M, Kean MJ, Doyle LW, Egan GF, Inder TE. 2007. Perinatal risk factors altering regional brain structure in the preterm infant. Brain. 130(Pt 3):667-677.
60. van Kooij BJ, van Pul C, Benders MJ, van Haastert IC, de Vries LS, Groenendaal F. 2011. Fiber tracking at term displays gender differences regarding cognitive and motor outcome at 2 years of age in preterm infants. Pediatr Res. 70(6):626-32.
61. Volpe JJ. 2009. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 8(1):110-124.
62. Zijdenbos AP, Dawant BM. 1994. Brain segmentation and white matter lesion detection in MR images. Crit Rev Biomed Eng. 22(5-6):401-465.