Thalamic alterations in preterm neonates and their relation to ventral striatum disturbances revealed by a combined shape and pose analysis

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• 作者：Yi Lao ; Yalin Wang ; Jie Shi ; Rafael Ceschin…
• 关键词：Frontal ; subcortical circuits ; Pose ; Prematurity ; Subcortical structures ; Tensor ; based morphometry
• 刊名：Brain Structure and Function
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：221
• 期：1
• 页码：487-506
• 全文大小：3,939 KB
• 参考文献：Aggleton JP, Brown MW (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22:425–444PubMed
  Aggleton JP, O’Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal–anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31:2292–2307PubMedCentral CrossRef PubMed
  Alexander GE, Crutcher MD, DeLong MR (1991) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146CrossRef
  Allin M, Henderson M, Suckling J, Nosarti C, Rushe T, Fearon P, Stewart AL, Bullmore E, Rifkin L, Murray R (2004) Effects of very low birthweight on brain structure in adulthood. Dev Med Child Neurol 46:46–53CrossRef PubMed
  Arsigny V, Commowick O, Pennec X, Ayache N (2006) A log-euclidean framework for statistics on diffeomorphisms. In: Medical Image Computing and Computer-Assisted Intervention–MICCAI 2006. Springer, Berlin, pp 924–931
  Ball G, Boardman JP, Rueckert D, Aljabar P, Arichi T, Merchant N, Gousias IS, Edwards AD, Counsell SJ (2012) The effect of preterm birth on thalamic and cortical development. Cereb Cortex 22:1016–1024PubMedCentral CrossRef PubMed
  Bechara A, Tranel D, Damasio H (2000) Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123:2189–2202CrossRef PubMed
  Behrens TEJ, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CAM, Boulby PA et al (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750–757CrossRef PubMed
  Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand K (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm. JAMA 288:728–737CrossRef PubMed
  Boardman JP, Counsell SJ, Rueckert D, Kapellou O, Bhatia KK, Aljabar P, Hajnal J, Allsop JM, Rutherford MA, Edwards AD (2006) Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage 32:70–78CrossRef PubMed
  Boardman JP, Craven C, Valappil S, Counsell SJ, Dyet L, Rueckert D, Aljabar P, Rutherford MA, Chew A, Allsop JM et al (2010) A common neonatal image phenotype predicts adverse neurodevelopmental outcome in children born preterm. Neuroimage 52:409–414CrossRef PubMed
  Bossa MN, Olmos S (2006) Statistical model of similarity transformations: building a multi-object pose model of brain structures. In: IEEE Comput. Soc. Workshop Math. Methods Biomed. Image Anal, p 59
  Bossa M, Zacur E, Olmos S (2011) Statistical analysis of relative pose information of subcortical nuclei: application on ADNI data. Neuroimage 55:999–1008PubMedCentral CrossRef PubMed
  Buchmayer S, Johansson S, Johansson A, Hultman CM, Sparén P, Cnattingius S (2009) Can association between preterm birth and autism be explained by maternal or neonatal morbidity? Pediatrics 124:e817–e825CrossRef PubMed
  Caravale B, Tozzi C, Albino G, Vicari S (2005) Cognitive development in low risk preterm infants at 3–4 years of life. Arch Dis Child Fetal Neonatal Ed 90:F474–F479PubMedCentral CrossRef PubMed
  Casanova MF, El-Baz AS, Kamat SS, Dombroski BA, Khalifa F, Elnakib A, Soliman A, Allison-McNutt A, Switala AE (2013) Focal cortical dysplasias in autism spectrum disorders. Acta Neuropathol Commun 1:67PubMedCentral CrossRef PubMed
  Cheon KA, Kim YS, Oh SH, Park SY, Yoon HW, Herrington J, Nair A, Koh YJ, Jang DP, Kim YB et al (2011) Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: a diffusion tensor imaging study. Brain Res 1417:77–86CrossRef PubMed
  Counsell SJ, Allsop JM, Harrison MC, Larkman DJ, Kennea NL, Kapellou O, Cowan FM, Hajnal JV, Edwards AD, Rutherford MA (2003) Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 112:1–7CrossRef PubMed
  Counsell SJ, Shen Y, Boardman JP, Larkman DJ, Kapellou O, Ward P, Allsop JM, Cowan FM, Hajnal JV, Edwards AD et al (2006) Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 117:376–386CrossRef PubMed
  Cummings JL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol 50:873CrossRef PubMed
  De Jong L, Van Der Hiele K, Veer I, Houwing J, Westendorp R, Bollen E, De Bruin P, Middelkoop H, Van Buchem M, Van Der Grond J (2008) Strongly reduced volumes of putamen and thalamus in Alzheimer’s disease: an MRI study. Brain 131:3277–3285PubMedCentral CrossRef PubMed
  Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, Church JA et al (2010) Prediction of individual brain maturity using fMRI. Science 329(5997):1358–1361PubMedCentral CrossRef PubMed
  Draganski B, Kherif F, Klöppel S, Cook PA, Alexander DC, Parker GJ, Deichmann R, Ashburner J, Frackowiak RS (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28:7143–7152CrossRef PubMed
  Dryden I, Mardia K (1998) Statistical analysis of shape. Wiley, London
  Erbetta A, Mandelli ML, Savoiardo M, Grisoli M, Bizzi A, Soliveri P, Chiapparini L, Prioni S, Bruzzone MG, Girotti F (2009) Diffusion tensor imaging shows different topographic involvement of the thalamus in progressive supranuclear palsy and corticobasal degeneration. AJNR Am J Neuroradiol 30:1482–1487CrossRef PubMed
  Fily A, Pierrat V, Delporte V, Breart G, Truffert P et al (2006) Factors associated with neurodevelopmental outcome at 2 years after very preterm birth: the population-based Nord-Pas-de-Calais EPIPAGE cohort. Pediatrics 117:357–366CrossRef PubMed
  Flamand VH, Nadeau L, Schneider C (2012) Brain motor excitability and visuomotor coordination in 8-year-old children born very preterm. Clin Neurophysiol 123:1191–1199CrossRef PubMed
  Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123(7):1293–1326CrossRef PubMed
  Golden JA, Harding BN (2010) Cortical malformations: unfolding polymicrogyria. Nat Rev Neurol 6:471–472CrossRef PubMed
  Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. Compr Physiol 373–417. doi:10.​1002/​cphy.​cp010509
  Goodall C (1991) Procrustes methods in the statistical analysis of shape. J R Stat Soc. Ser B (Methodol) 53(2):285–339
  Gorczowski K, Styner M, Jeong JY, Marron J, Piven J, Hazlett HC, Pizer SM, Gerig G (2010) Multi-object analysis of volume, pose, and shape using statistical discrimination. Pattern Analysis and Machine Intelligence, IEEE Transactions on 32, 652–661
  Groenewegen HJ, Berendse HW (1994) The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci 17:52–57CrossRef PubMed
  Grunau RE, Whitfield MF, Davis C (2002) Pattern of learning disabilities in children with extremely low birth weight and broadly average intelligence. Arch Pediatr Adolesc Med 156:615CrossRef PubMed
  Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317–330CrossRef PubMed
  Hart AR, Whitby EW, Griffiths PD, Smith MF (2008) Magnetic resonance imaging and developmental outcome following preterm birth: review of current evidence. Dev Med Child Neurol 50:655–663CrossRef PubMed
  Hotelling H (1931) The generalization of student’s ratio. Ann Math Stat 2:360–378CrossRef
  Hutsler J, Galuske RA (2003) Hemispheric asymmetries in cerebral cortical networks. Trends Neurosci 26:429–435CrossRef PubMed
  Inder TE, Warfield SK, Wang H, Hüppi PS, Volpe JJ (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286–294CrossRef PubMed
  Isaacs EB, Lucas A, Chong WK, Wood SJ, Johnson CL, Marshall C, Vargha-Khadem F, Gadian DG (2000) Hippocampal volume and everyday memory in children of very low birth weight. Pediatr Res 47:713–720CrossRef PubMed
  Joseph RM, Tager-Flusberg H (2004) The relationship of theory of mind and executive functions to symptom type and severity in children with autism. Dev Psychopathol 16:137–155PubMedCentral CrossRef PubMed
  Karcher H (1977) Riemannian center of mass and mollifier smoothing. Commun Pure Appl Math 30:509–541CrossRef
  Kesler SR, Ment LR, Vohr B, Pajot SK, Schneider KC, Katz KH, Ebbitt TB, Duncan CC, Makuch RW, Reiss AL (2004) Volumetric analysis of regional cerebral development in preterm children. Pediatr Neurol 31:318–325PubMedCentral CrossRef PubMed
  Kesler SR, Reiss AL, Vohr B, Watson C, Schneider KC, Katz KH, Maller-Kesselman J, Silbereis J, Constable RT, Makuch RW et al (2008) Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. J Pediatrics 152:513–520CrossRef
  Kinney HC (2006) The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol 30(2):81–88CrossRef PubMed
  Klein JC, Rushworth MF, Behrens TE, Mackay CE, de Crespigny AJ, D’Arceuil H, Johansen-Berg H (2010) Topography of connections between human prefrontal cortex and mediodorsal thalamus studied with diffusion tractography. Neuroimage 51:555–564PubMedCentral CrossRef PubMed
  Kostovic I, Goldman-Rakic PS (1983) Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 219:431–447CrossRef PubMed
  Kostović I, Lukinović N, Judaš M, Bogdanović N, Mrzljak L, Zečević N, Kubat M (1989) Structural basis of the developmental plasticity in the human cerebral cortex: the role of the transient subplate zone. Metab Brain Dis 4:17–23CrossRef PubMed
  Kostović I, Judaš M, Sedmak G (2011) Developmental history of the subplate zone, subplate neurons and interstitial white matter neurons: relevance for schizophrenia. Int J Dev Neurosci 29:193–205CrossRef PubMed
  Lao Y, Shi J, Wang Y, Ceschin R, Hwang D, Nelson M, Panigrahy A, Lepore N (2013) Statistical analysis of relative pose of the thalamus in preterm neonates. In: Clinical Image-based Procedures. Translational research in medical imaging. LNCS 8361, 1–9. doi:10.​1007/​978-3-319-05666-1_​1 .
  Lepore N, Brun C, Chou YY, Chiang MC, Dutton RA, Hayashi KM, Luders E, Lopez OL, Aizenstein HJ, Toga AW et al (2008) Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans Med Imaging 27:129–141PubMedCentral CrossRef PubMed
  Limperopoulos C, Bassan H, Sullivan NR, Soul JS, Robertson RL, Moore M, Ringer SA, Volpe JJ, du Plessis AJ (2008) Positive screening for autism in ex-preterm infants: prevalence and risk factors. Pediatrics 121:758–765PubMedCentral CrossRef PubMed
  Lin Y, Okumura A, Hayakawa F, Kato T, Kuno K, Watanabe K (2001) Quantitative evaluation of thalami and basal ganglia in infants with periventricular leukomalacia. Dev Med Child Neurol 43:481–485CrossRef PubMed
  Lorensen WE, Cline HE (1987) Marching cubes: a high resolution 3D surface construction algorithm. SIGGRAPH Comput Graph 21(4):163–169CrossRef
  Marlow N, Wolke D, Bracewell MA, Samara M (2005) Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 352:9–19CrossRef PubMed
  Mega MS, Cummings JL (1994) Frontal-subcortical circuits and neuropsychiatric disorders. Neurosciences 6:358–370
  Metzger CD, van der Werf YD, Walter M (2013) Functional mapping of thalamic nuclei and their integration into cortico-striatal-thalamo-cortical loops via ultra-high resolution imaging—from animal anatomy to in vivo imaging in humans. Front Neurosci 7
  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):86–103CrossRef PubMed
  Mrzljak L, Uylings H, Kostovic I, van Eden CG (1988) Prenatal development of neurons in the human prefrontal cortex: I. a qualitative golgi study. J Comp Neurol 271:355–386CrossRef PubMed
  Nagasunder A, Kinney H, Blüml S, Tavaré C, Rosser T, Gilles F, Nelson M, Panigrahy A (2011) Abnormal microstructure of the atrophic thalamus in preterm survivors with periventricular leukomalacia. Am J Neuroradiol 32:185–191PubMedCentral PubMed
  Nichols TE, Holmes AP (2001) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25CrossRef
  Niemann K, Mennicken VR, Jeanmonod D, Morel A (2000) The Morel stereotactic atlas of the human thalamus: atlas-to-MR registration of internally consistent canonical model. Neuroimage 12:601–616CrossRef PubMed
  Pennec X, Fillard P, Ayache N (2006) A riemannian framework for tensor computing. Int J Comput Vis 66:41–66CrossRef
  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 284:1939–1947CrossRef PubMed
  Pizer SM, Fritsch DS, Yushkevich PA, Johnson VE, Chaney EL (1999) Segmentation, registration, and measurement of shape variation via image object shape. IEEE Trans Med Imaging 18:851–865CrossRef PubMed
  Prensa L, Richard S, Parent A (2003) Chemical anatomy of the human ventral striatum and adjacent basal forebrain structures. J Comp Neurol 460(3):345–367CrossRef PubMed
  Reijneveld SA, De Kleine M, van Baar AL, Kollée LA, Verhaak CM, Verhulst FC, Verloove-Vanhorick SP (2006) Behavioural and emotional problems in very preterm and very low birthweight infants at age 5 years. Arch Dis Child Fetal Neonatal Ed 91:F423–F428PubMedCentral CrossRef PubMed
  Robinson RG, Kubos KL, Starr LB, Rao K, Price TR (1984) Mood disorders in stroke patients: importance of location of lesion. Brain 107:81–93CrossRef PubMed
  Robinson S, Goddard L, Dritschel B, Wisley M, Howlin P (2009) Executive functions in children with autism spectrum disorders. Brain Cogn 71:362–368CrossRef PubMed
  Shi J, Wang Y, Ceschin R, An X, Nelson MD, Panigrahy A, Leporé N (2012) Surface fluid registration and multivariate tensor-based morphometry in newborns-the effects of prematurity on the putamen. In: Asia-Pacific Signal and Information Processing Association Annual Summit and Conference (APSIPA ASC). Hollywood, CA, USA. http://​gsl.​lab.​asu.​edu/​archive/​apsipa_​12.​pdf
  Shi J, Wang Y, Ceschin R, An X, Lao Y, Vanderbilt D, Nelson MD, Thompson PM, Panigrahy A, Leporé N (2013) A multivariate surface-based analysis of the putamen in premature newborns: regional differences within the ventral striatum. PLoS One 8:e66736PubMedCentral CrossRef PubMed
  Sonuga-Barke EJ (2002) Psychological heterogeneity in AD/HD—a dual pathway model of behaviour and cognition. Behav Brain Res 130:29–36CrossRef PubMed
  Srinivasan L, Dutta R, Counsell SJ, Allsop JM, Boardman JP, Rutherford MA, Edwards AD (2007) Quantification of deep gray matter in preterm infants at term-equivalent age using manual volumetry of 3-tesla magnetic resonance images. Pediatrics 119:759–765CrossRef PubMed
  Starkstein SE, Robinson RG, Price TR (1987) Comparison of cortical and subcortical lesions in the production of poststroke mood disorders. Brain 110:1045–1059CrossRef PubMed
  Starkstein SE, Robinson RG, Berthier ML, Parikh RM, Price TR (1988) Differential mood changes following basal ganglia vs thalamic lesions. Arch Neurol 45:725CrossRef PubMed
  Strand-Brodd K, Ewald U, Grönqvist H, Holmström G, Strömberg B, Grönqvist E, von Hofsten C, Rosander K (2011) Development of smooth pursuit eye movements in very preterm infants: 1. general aspects. Acta Paediatr 100:983–991PubMedCentral CrossRef PubMed
  Styner M, Oguz I, Xu S, Brechbühler C, Pantazis D, Gerig G (2006) Framework for the statistical shape analysis of brain structures using SPHARM-PDM. Insight J 1071:242PubMed
  Thompson PM, Hayashi KM, de Zubicaray GI, Janke AL, Rose SE, Semple J, Hong MS, Herman DH, Gravano D, Doddrell DM et al (2004) Mapping hippocampal and ventricular change in alzheimer disease. Neuroimage 22:1754–1766CrossRef PubMed
  Toplak ME, Jain U, Tannock R (2005) Executive and motivational processes in adolescents with attention-deficit-hyperactivity disorder (ADHD). Behav Brain Funct 1:8PubMedCentral CrossRef PubMed
  Van Der Werf YD, Jolles J, Witter MP, Uylings H (2003) Contributions of thalamic nuclei to declarative memory functioning. Cortex 39:1047–1062CrossRef PubMed
  Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110–124PubMedCentral CrossRef PubMed
  Wang Y, Zhang J, Gutman B, Chan TF, Becker JT, Aizenstein HJ, Lopez OL, Tamburo RJ, Toga AW, Thompson PM (2010) Multivariate tensor-based morphometry on surfaces: application to mapping ventricular abnormalities in HIV/AIDS. Neuroimage 49:2141–2157PubMedCentral CrossRef PubMed
  Wang Y, Panigrahy A, Ceschin R, Liu S, Thompson PM, Lepore N (2011a) Surface morphometry of subcortical structures in premature neonates. In: Proc Intl Soc Mag Reson Med, p 2585
  Wang Y, Song Y, Rajagopalan P, An T, Liu K, Chou YY, Gutman B, Toga AW, Thompson PM (2011b) Surface-based TBM boosts power to detect disease effects on the brain: an N = 804 ADNI study. Neuroimage 56:1993–2010PubMedCentral CrossRef PubMed
  Wang Y, Panigrahy A, Shi J, Ceschin R, Nelson M (2011b). Multivariate tensor based morphometry on premature neonates: a pilot study. In: Image Analysis of Human Brain Development (IAHBD). Toronto, Canada. http://​gsl.​lab.​asu.​edu/​archive/​IAHBD-PreMature.​pdf
  Wiegell MR, Tuch DS, Larsson HB, Wedeen VJ (2003) Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. Neuroimage 19:391–401CrossRef PubMed
  Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR (2000) Neurologic and developmental disability after extremely preterm birth. N Engl J Med 343:378–384CrossRef PubMed
  Zhang H, Yushkevich PA, Alexander DC, Gee JC et al (2006) Deformable registration of diffusion tensor mr images with explicit orientation optimization. Med image Anal 10:764–785CrossRef PubMed
  
• 作者单位：Yi Lao (1)
  Yalin Wang (2)
  Jie Shi (2)
  Rafael Ceschin (3)
  Marvin D. Nelson (1)
  Ashok Panigrahy (1) (3)
  Natasha Leporé (1)
  
  1. Department of Radiology, University of Southern California and Children’s Hospital, 4650 Sunset Blvd, MS#81, Los Angeles, CA, 90027, USA
  2. School of Computing, Informatics, and Decision Systems Engineering, Arizona State University, Tempe, AZ, 85281, USA
  3. Department of Radiology, Children’s Hospital of Pittsburgh UPMC, Pittsburgh, PA, USA
  
• 刊物主题：Neurosciences; Cell Biology; Neurology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1863-2661

文摘

Finding the neuroanatomical correlates of prematurity is vital to understanding which structures are affected, and to designing efficient prevention and treatment strategies. Converging results reveal that thalamic abnormalities are important indicators of prematurity. However, little is known about the localization of the abnormalities within the subnuclei of the thalamus, or on the association of altered thalamic development with other deep gray matter disturbances. Here, we aim to investigate the effect of prematurity on the thalamus and the putamen in the neonatal brain, and further investigate the associated abnormalities between these two structures. Using brain structural magnetic resonance imaging, we perform a novel combined shape and pose analysis of the thalamus and putamen between 17 preterm (41.12 ± 5.08 weeks) and 19 term-born (45.51 ± 5.40 weeks) neonates at term equivalent age. We also perform a set of correlation analyses between the thalamus and the putamen, based on the surface and pose results. We locate significant alterations on specific surface regions such as the anterior and ventral anterior (VA) thalamic nuclei, and significant relative pose changes of the left thalamus and the right putamen. In addition, we detect significant association between the thalamus and the putamen for both surface and pose parameters. The regions that are significantly associated include the VA, and the anterior and inferior putamen. We detect statistically significant surface deformations and pose changes on the thalamus and putamen, and for the first time, demonstrate the feasibility of using relative pose parameters as indicators for prematurity in neonates. Our methods show that regional abnormalities of the thalamus are associated with alterations of the putamen, possibly due to disturbed development of shared pre-frontal connectivity. More specifically, the significantly correlated regions in these two structures point to frontal-subcortical pathways including the dorsolateral prefrontal-subcortical circuit, the lateral orbitofrontal-subcortical circuit, the motor circuit, and the oculomotor circuit. These findings reveal new insight into potential subcortical structural covariates for poor neurodevelopmental outcomes in the preterm population. Keywords Frontal-subcortical circuits Pose Prematurity Subcortical structures Tensor-based morphometry