All Title Author
Keywords Abstract

PLOS ONE  2013 

A Multivariate Surface-Based Analysis of the Putamen in Premature Newborns: Regional Differences within the Ventral Striatum

DOI: 10.1371/journal.pone.0066736

Full-Text   Cite this paper   Add to My Lib


Many children born preterm exhibit frontal executive dysfunction, behavioral problems including attentional deficit/hyperactivity disorder and attention related learning disabilities. Anomalies in regional specificity of cortico-striato-thalamo-cortical circuits may underlie deficits in these disorders. Nonspecific volumetric deficits of striatal structures have been documented in these subjects, but little is known about surface deformation in these structures. For the first time, here we found regional surface morphological differences in the preterm neonatal ventral striatum. We performed regional group comparisons of the surface anatomy of the striatum (putamen and globus pallidus) between 17 preterm and 19 term-born neonates at term-equivalent age. We reconstructed striatal surfaces from manually segmented brain magnetic resonance images and analyzed them using our in-house conformal mapping program. All surfaces were registered to a template with a new surface fluid registration method. Vertex-based statistical comparisons between the two groups were performed via four methods: univariate and multivariate tensor-based morphometry, the commonly used medial axis distance, and a combination of the last two statistics. We found statistically significant differences in regional morphology between the two groups that are consistent across statistics, but more extensive for multivariate measures. Differences were localized to the ventral aspect of the striatum. In particular, we found abnormalities in the preterm anterior/inferior putamen, which is interconnected with the medial orbital/prefrontal cortex and the midline thalamic nuclei including the medial dorsal nucleus and pulvinar. These findings support the hypothesis that the ventral striatum is vulnerable, within the cortico-stiato-thalamo-cortical neural circuitry, which may underlie the risk for long-term development of frontal executive dysfunction, attention deficit hyperactivity disorder and attention-related learning disabilities in preterm neonates.


[1]  Lou HC (1996) Etiology and pathogenesis of attention-de_cit hyperactivity disorder (ADHD): significance of prematurity and perinatal hypoxic-haemodynamic encephalopathy. Acta Paediatr 85(11): 1266–71.
[2]  Powell KB, Voeller KKS (2004) Prefrontal executive function syndromes in children. J Child Neurol 19: 785–797.
[3]  Nagasunder AC, Kinney HC, Bluml S, Tavare CJ, Rosser T, et al. (2011) Abnormal microstructure of the atrophic thalamus in preterm survivors with periventricular leukomalacia. Am J Neuroradiol 32(1): 185–191.
[4]  Wang Y, Panigrahy A, Shi J, Ceschin R, Nelson MD, et al.. (2011a) Surface Multivariate Tensor based Morphometry on premature neonates: a pilot study. Proceedings of the MICCAI workshop on Image Analysis of Human Brain Development (IAHBD 2011).
[5]  Peterson BS, Vohr B, Staib LH, Dolberg A, Schneider KC, et al. (2000) Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA-J Am Med Assoc 284(15): 1939–1947.
[6]  Abernethy LJ, Cooke RWI, Foulder-Hughes L (2004) Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatric Res 55(5): 884–893.
[7]  Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, 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.
[8]  Boardman JP, Counsell SJ, Rueckert D, Kapellou O, Bhatia KK, et al. (2006) Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. NeuroImage 32(1): 70–78.
[9]  Nosarti C, Giouroukou E, Healy E, Rifkin L, Walshe M, et al. (2008) Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain 131(1): 205–217.
[10]  Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115(2): 286–294.
[11]  Wang Y, Panigrahy A, Shi J, Ceschin R, Nie Z, et al.. (2012a) 3D vs. 2D Surface Shape Analysis of the Corpus Callosum in Neonates–Application to Prematurity. MICCAI workshop on Perinatal and Paediatric Imaging (PaPI 2012).
[12]  Shi J, Wang Y, Ceschin R, An X, Nelson MD, et al.. (2012) Surface uid registration and multivariate tensor-based morphometry in newborns - the effects of prematurity on the putamen. Asia Pacific Signal and Information Processing Association (APSIPA2012).
[13]  Mercuri E, Atkinson J, Braddick O, Anker S, Cowan F, et al. (1997) Basal ganglia damage and impaired visual function in the newborn infant. Arch Dis Child 77(2): F111–F114.
[14]  Wang Y, Lui LM, Gu X, Hayashi KM, Chan TF, et al. (2007) Brain surface conformal parameterization using Riemann surface structure. IEEE Trans Med Imag 26(6): 853–865.
[15]  Shi J, Thompson PM, Gutman B, Wang Y (2013) Surface uid registration of conformal representation: application to detect disease effect and genetic inuence on hippocampus. NeuroImage, in press.
[16]  Wang Y, Song Y, Rajagopalan P, An T, Liu K, et al. (2011b) Surface-based TBM boosts power to detect disease effects on the brain: an N = 804 ADNI study. NeuroImage 56(4): 1993–2010.
[17]  Wang Y, Zhang J, Gutman B, Chan TF, Becker JT, et al. (2010) Multivariate tensor-based morphometry on surfaces: application to mapping ventricular abnormalities in HIV/AIDS. NeuroImage 49(3): 2141–2157.
[18]  Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, et al. (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. NeuroImage 31(3): 1116–1128.
[19]  Presna L, Richard S, Parent A (2003) Chemical Anatomy of the Human Ventral Striatum and Adjacent Forebrain Structures. J Comp Neurol 460(3): 345–367.
[20]  Morel A, Loup F, Magnin M, Jeanmonod D (2002) Neurochemical organization of the human basal ganglia: Anatomofunctional territories defined by the distributions of calcium-binding proteins and SMI-32. J Comp Neurol 443(1): 86–103.
[21]  Thompson PM, Giedd JN, Woods RP, MacDonald D, Evans AC, et al. (2000) Growth patterns in the developing human brain detected using continuum-mechanical tensor mapping. Nature 404(6774): 190–193.
[22]  Davatzikos C (1996) Spatial normalization of 3D brain images using deformable models. J Comp Assist Tomogr 20(4): 656–665.
[23]  Aris R. (1999) Vectors, tensors, and the basic equations of uid mechanics. Ed. Dover.
[24]  Stam J (2003) Flows on surfaces of arbitrary topology. Proceedings of SIGGRAPH 2003: 724–731.
[25]  Lepore N, Brun C, Chou YY, Chiang MC, Dutton RA, et al. (2008) Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans Med Imag 27(1): 129–141.
[26]  Arsigny V, Fillard P, Pennec X, Ayache N (2006) Log-Euclidean metrics for fast and simple calculus on diffusion tensors. Magn Reson Med 56(2): 411–421.
[27]  Pizer S, Fritsch D, Yushkevich P, Johnson V, Chaney E (1999) Segmentation, registration, and measurement of shape variation via image object shape. IEEE Trans Med Imag 18(10): 851–865.
[28]  Thompson PM, Hayashi KM, de Zubicaray GI, Janke AL, Rose SE, et al. (2004) Mapping hippocampal and ventricular change in Alzheimer disease. NeuroImage 22(4): 1754–1766.
[29]  Hotelling H (1931) The generalization of Student’s ratio. Ann Math Statist 2(3): 360–378.
[30]  Nichols TE, Holmes AP (2009) Non parametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 25(1): 1–25.
[31]  Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57(1): 289–300.
[32]  Voorn P, Vanderschuren LJMJ, Groenewegen HJ, Robbins TW, Pennartz CMA (2004) Putting a spin on the dorsalventral divide of the striatum. Trends Neurosci 27(8): 468–474.
[33]  Draganski B, Kherif F, Kloppel S, Cook PA, Alexander DC, et al. (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28(28): 7143–7152.
[34]  Ball G, Boardman JP, Rueckert D, Aljabar P, Arichi T, et al. (2012) The effect of preterm birth on thalamic and cortical development. Cereb Cortex 22(5): 1016–1024.
[35]  Boardman JP, Craven C, Valappil S, Counsell SJ, Dyet LE, et al. (2010) A common neonatal image phenotype predicts adverse neurodevelopmental outcome in children born preterm. NeuroImage 52(2): 409–414.
[36]  Ligam P, Hayes RL, Folkerth RD, Liu L, Yang M, et al. (2009) Thalamic Damage in Periventricular Leukomalacia: novel pathologic observations relevant to cognitive deficits in survivors of prematurity. Pediatric Res 65(5): 524–529.
[37]  Nosarti C, Shergill SS, Allin MP, Walse M, Rifkin L, et al. (2009) Neural substrates of letter uency processing in young adults who were very preterm: alterations in frontal and striatal regions. NeuroImage 47(4): 1904–1913.
[38]  Cauda F, Cavanna AE, D’agata F, Sacco K, Duca S, et al. (2011) Functional connectivity and coactivation of the nucleus accumbens: a combined functional connectivity and structure-based metaanalysis. J of Cog Neurosci 23(10): 2864–2877.
[39]  Pierson CR, Folkerth RD, Billiards SS, Trachtenberg FL, Drinkwater ME, et al. (2007) Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 114(6): 619–631.
[40]  Volpe JJ (2009) The encephalopathy of prematurity-brain injury and impaired brain development inextricably intertwined. Seminar Pediatr Neurol 16(4): 167–78.
[41]  Van de Weijer-Bergsma E, Wijnroks L, Jongmans MJ (2008) Attention development in infants and preschool children born preterm: a review. Infant Behav Dev 31(3): 333–351.
[42]  Frodl T, Skokauskas N (2012) Meta-analysis of structural MRI studies in children and adults with attention deficit hyperactivity disorder indicates treatment effects. Acta Psychiatr Scand 125(2): 114–126.
[43]  Sobel LJ, Bansal R, Maia TV, Sanchez J, Mazzone L, et al. (2010) Basal ganglia surface morphology and the effects of stimulant medications in youth with attention deficit hyperactivity disorder. Am J Psychiatry 167(8): 977–86.
[44]  Pangelinan MM, Zhang G, VanMeter JW, Clark JE, Hatfield BD, et al. (2011) Beyond age and gender: relationships between cortical and subcortical brain volume and cognitive-motor abilities in school-age children. NeuroImage 54(4): 3093–3100.
[45]  Biederman J, Ball SW, Monuteaux MC, Mick E, Spencer TJ, et al. (2008) New insights into the comorbidity between ADHD and major depression in adolescent and young adult females. J Am Acad Child Adolesc Psychiatry 47(4): 426–434.


comments powered by Disqus