Long-Term Functional Outcomes and Correlation with Regional Brain Connectivity by MRI Diffusion Tractography Metrics in a Near-Term Rabbit Model of Intrauterine Growth Restriction

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Illa, Miriam ^a,b   Eixarch, Elisenda ^a,b,c   Batalle, Dafnis ^b   Arbat Plana, Ariadna ^b   Muñoz Moreno, Emma ^b   Figueras, Francesc ^a,b,c   Gratacos, Eduard ^a,b,c  

^a HOSPITAL CLÍNIC   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; ATTENTION DISTURBANCE; BRAIN DEVELOPMENT; COGNITION; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FETUS; FUNCTIONAL ASSESSMENT; GRAY MATTER; IMAGE DISPLAY; INTRAUTERINE GROWTH RETARDATION; LEFT HEMISPHERE; MENTAL TASK; NERVE CELL NETWORK; NONHUMAN; OBJECT RECOGNITION TASK; OPEN FIELD BEHAVIOR; RABBIT; SHORT TERM MEMORY; VOXEL BASED MORPHOMETRY;

ANIMALS; ANXIETY; ATTENTION; BRAIN; COGNITION; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; MEMORY; NERVE NET; PREGNANCY; RABBITS;

EID: 84885451025     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076453     Document Type: Article

References (129)

1. Marsal K, (2002) Intrauterine growth restriction. Curr Opin Obstet Gynecol 14: 127-135.
2. Balasch J, Gratacos E, (2011) Delayed Childbearing: Effects on Fertility and the Outcome of Pregnancy. Fetal Diagn Ther 29: 263-273.
3. Rees S, Harding R, Walker D, (2007) An adverse intrauterine environment: implications for injury and altered development of the brain. Int J Dev Neurosci 26: 3-11.
4. Figueras F, Oros D, Cruz-Martinez R, Padilla N, Hernandez-Andrade E, et al. (2009) Neurobehavior in term, small-for-gestational age infants with normal placental function. Pediatrics 124: e934-941.
5. Bassan H, Stolar O, Geva R, Eshel R, Fattal-Valevski A, et al. (2011) Intrauterine growth-restricted neonates born at term or preterm: how different? Pediatr Neurol 44: 122-130.
6. Sanz-Cortés M, Figueras F, Bonet-Carne E, Padilla N, Tenorio V, et al. (2013) Fetal brain MRI texture analysis identifies different microstructural patterns in adequate and small for gestational age fetuses at term. Fetal Diagn Ther 33(2): 122-9.
7. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, et al. (2004) Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res 56: 132-138.
8. Lodygensky GA, Seghier ML, Warfield SK, Tolsa CB, Sizonenko S, et al. (2008) Intrauterine growth restriction affects the preterm infant's hippocampus. Pediatr Res 63: 438-443.
9. Dubois J, Benders M, Borradori-Tolsa C, Cachia a, Lazeyras F, et al. (2008) Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131: 2028-2041.
10. Aarnoudse-Moens CS, Weisglas-Kuperus N, van Goudoever JB, Oosterlaan J, (2009) Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics 124: 717-728.
11. Alati R, Najman JM, O'Callaghan M, Bor W, Williams GM, et al. (2009) Fetal growth and behaviour problems in early adolescence: findings from the Mater University Study of Pregnancy. Int J Epidemiol 38: 1390-1400.
12. Feldman R, Eidelman AI, (2006) Neonatal state organization, neuromaturation, mother-infant interaction, and cognitive development in small-for-gestational-age premature infants. Pediatrics 118: e869-878.
13. Geva R, Eshel R, Leitner Y, Fattal-Valevski A, Harel S, (2006) Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res 1117: 186-194.
14. Geva R, Eshel R, Leitner Y, Valevski AF, Harel S, (2006) Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics 118: 91-100.
15. Heinonen K, Raikkonen K, Pesonen AK, Andersson S, Kajantie E, et al. (2010) Behavioural symptoms of attention deficit/hyperactivity disorder in preterm and term children born small and appropriate for gestational age: a longitudinal study. BMC Pediatr 10: 91.
16. Larroque B, Bertrais S, Czernichow P, Leger J, (2001) School difficulties in 20-year-olds who were born small for gestational age at term in a regional cohort study. Pediatrics 108: 111-115.
17. Leitner Y, Fattal-Valevski A, Geva R, Eshel R, Toledano-Alhadef H, et al. (2007) Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol 22: 580-587.
18. McCarton CM, Wallace IF, Divon M, Vaughan HG Jr, (1996) Cognitive and neurologic development of the premature, small for gestational age infant through age 6: comparison by birth weight and gestational age. Pediatrics 98: 1167-1178.
19. Morsing E, Asard M, Ley D, Stjernqvist K, Marsal K, (2011) Cognitive function after intrauterine growth restriction and very preterm birth. Pediatrics 127: e874-882.
20. O'Keeffe MJ, O'Callaghan M, Williams GM, Najman JM, Bor W, (2003) Learning, cognitive, and attentional problems in adolescents born small for gestational age. Pediatrics 112: 301-307.
21. Pyhala R, Lahti J, Heinonen K, Pesonen AK, Strang-Karlsson S, et al. (2011) Neurocognitive abilities in young adults with very low birth weight. Neurology 77: 2052-2060.
22. Scherjon S, Briet J, Oosting H, Kok J, (2000) The discrepancy between maturation of visual-evoked potentials and cognitive outcome at five years in very preterm infants with and without hemodynamic signs of fetal brain-sparing. Pediatrics 105: 385-391.
23. Tideman E, Marsal K, Ley D, (2007) Cognitive function in young adults following intrauterine growth restriction with abnormal fetal aortic blood flow. Ultrasound Obstet Gynecol 29: 614-618.
24. Vasiliadis HM, Buka SL, Martin LT, Gilman SE, (2010) Fetal growth and the lifetime risk of generalized anxiety disorder. Depress Anxiety 27: 1066-1072.
25. Cubillo A, Halari R, Smith A, Taylor E, Rubia K, (2012) A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention. Cortex 48: 194-215.
26. Eichenbaum H, Yonelinas AP, Ranganath C, (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30: 123-152.
27. Kobel M, Bechtel N, Specht K, Klarhofer M, Weber P, et al. (2010) Structural and functional imaging approaches in attention deficit/hyperactivity disorder: does the temporal lobe play a key role? Psychiatry Res 183: 230-236.
28. Ment LR, Hirtz D, Huppi PS, (2009) Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol 8: 1042-1055.
29. Rees S, Harding R, Walker D, (2011) The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int J Dev Neurosci 29: 551-563.
30. Basser PJ, Pierpaoli C, (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111: 209-219.
31. Neil J, Miller J, Mukherjee P, Huppi PS, (2002) Diffusion tensor imaging of normal and injured developing human brain - a technical review. NMR Biomed 15: 543-552.
32. Nucifora PG, Verma R, Lee SK, Melhem ER, (2007) Diffusion-tensor MR imaging and tractography: exploring brain microstructure and connectivity. Radiology 245: 367-384.
33. Batalle D, Eixarch E, Figueras F, Munoz-Moreno E, Bargallo N, et al. (2012) Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome. Neuroimage 60: 1352-1366.
34. Eixarch E, Batalle D, Illa M, Munoz-Moreno E, Arbat-Plana A, et al. (2012) Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PLoS One 7: e31497.
35. Sanz-Cortes M, Figueras F, Bargallo N, Padilla N, Amat-Roldan I, et al. (2010) Abnormal brain microstructure and metabolism in small-for-gestational-age term fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 36: 159-165.
36. Berman JI, Hamrick SE, McQuillen PS, Studholme C, Xu D, et al. (2011) Diffusion-weighted imaging in fetuses with severe congenital heart defects. AJNR Am J Neuroradiol 32: E21-22.
37. de Zeeuw P, Mandl RC, Hulshoff Pol HE, van Engeland H, Durston S, (2011) Decreased frontostriatal microstructural organization in attention deficit/hyperactivity disorder. Hum Brain Mapp 33: 1941-51.
38. Shukla DK, Keehn B, Muller RA, (2011) Tract-specific analyzes of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. J Child Psychol Psychiatry 52: 286-295.
39. Rha DW, Chang WH, Kim J, Sim EG, Park ES, (2011) Comparing quantitative tractography metrics of motor and sensory pathways in children with periventricular leukomalacia and different levels of gross motor function. Neuroradiology 54: 615-621.
40. Thomas B, Eyssen M, Peeters R, Molenaers G, Van Hecke P, et al. (2005) Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 128: 2562-2577.
41. Hall FS, Perona MT, (2012) Have studies of the developmental regulation of behavioral phenotypes revealed the mechanisms of gene-environment interactions? Physiol Behav 107: 623-40.
42. D'Arceuil H, Liu C, Levitt P, Thompson B, Kosofsky B, et al. (2008) Three-dimensional high-resolution diffusion tensor imaging and tractography of the developing rabbit brain. Dev Neurosci 30: 262-275.
43. Bassan H, Trejo LL, Kariv N, Bassan M, Berger E, et al. (2000) Experimental intrauterine growth retardation alters renal development. Pediatr Nephrol 15: 192-195.
44. Derrick M, Drobyshevsky A, Ji X, Tan S, (2007) A model of cerebral palsy from fetal hypoxia-ischemia. Stroke 38: 731-735.
45. Eixarch E, Figueras F, Hernandez-Andrade E, Crispi F, Nadal A, et al. (2009) An experimental model of fetal growth restriction based on selective ligature of uteroplacental vessels in the pregnant rabbit. Fetal Diagn Ther 26: 203-211.
46. Eixarch E, Hernandez-Andrade E, Crispi F, Illa M, Torre I, et al. (2011) Impact on fetal mortality and cardiovascular Doppler of selective ligature of uteroplacental vessels compared with undernutrition in a rabbit model of intrauterine growth restriction. Placenta 32: 304-309.
47. Snook L, Plewes C, Beaulieu C, (2007) Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. Neuroimage 34: 243-252.
48. Moorman WJ, Cheever KL, Skaggs SR, Clark JC, Turner TW, et al. (2000) Male adolescent exposure to endocrine-disrupting pesticides: vinclozolin exposure in peripubertal rabbits. Andrologia 32: 285-293.
49. Bouet V, Gahery Y, Lacour M, (2003) Behavioural changes induced by early and long-term gravito-inertial force modification in the rat. Behav Brain Res 139: 97-104.
50. Kowalska D BP, Pietras M. (2008) Suitability of behavioural tests for determining the ways rabbits function in the environment and their relationship with some productive traits. Ethology and Welfare 2008. Presented at the 9th World Rabbit Congress - June 10-13, 2008 - Verona - Italy. The World Rabbit Science website. Available: http://www.world-rabbit-science.com/WRSA-Proceedings/Congress-2008-Verona/Papers/W-Kowalska.pdf. Accessed 2013 September 1.
51. Walsh RN, Cummins RA, (1975) Mechanisms mediating the production of environmentally induced brain changes. Psychol Bull 82: 986-1000.
52. Olton DS, Feustle WA, (1981) Hippocampal function required for nonspatial working memory. Exp Brain Res 41: 380-389.
53. Cowan N, Nugent LD, Elliott EM, Ponomarev I, Saults JS, (1999) The role of attention in the development of short-term memory: age differences in the verbal span of apprehension. Child Dev 70: 1082-1097.
54. Dere E, Kart-Teke E, Huston JP, De Souza Silva MA, (2006) The case for episodic memory in animals. Neurosci Biobehav Rev 30: 1206-1224.
55. Ennaceur A, Aggleton JP, (1997) The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat. Behav Brain Res 88: 181-193.
56. Mumby DG, (2001) Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats. Behav Brain Res 127: 159-181.
57. Treit D, Menard J, Royan C, (1993) Anxiogenic stimuli in the elevated plus-maze. Pharmacol Biochem Behav 44: 463-469.
58. Ennaceur A, Delacour J, (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31: 47-59.
59. Ennaceur A, (2010) One-trial object recognition in rats and mice: methodological and theoretical issues. Behav Brain Res 215: 244-254.
60. de Bruin N, Pouzet B, (2006) Beneficial effects of galantamine on performance in the object recognition task in Swiss mice: deficits induced by scopolamine and by prolonging the retention interval. Pharmacol Biochem Behav 85: 253-260.
61. Fillard P, Pennec X, Arsigny V, Ayache N, (2007) Clinical DT-MRI estimation, smoothing, and fiber tracking with log-Euclidean metrics. IEEE Transactions on Medical Imaging 26: 1472-1482.
62. Toussaint N, Souplet J-C, Fillard P (2007) MedINRIA: Medical Image Navigation and Research Tool by INRIA. Proc of MICCAI'07 Workshop on Interaction in medical image analysis and visualization. Brisbane, Australia.
63. Westin CF, Maier SE, Mamata H, Nabavi A, Jolesz FA, et al. (2002) Processing and visualization for diffusion tensor MRI. Med Image Anal 6: 93-108.
64. Descoteaux M, Angelino E, Fitzgibbons S, Deriche R, (2007) Regularized, fast, and robust analytical Q-ball imaging. Magn Reson Med 58: 497-510.
65. Munoz-Moreno E, Martin-Fernandez M, (2009) Characterization of the similarity between diffusion tensors for image registration. Comput Biol Med 39: 251-265.
66. Alexander DC, Pierpaoli C, Basser PJ, Gee JC, (2001) Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging 20: 1131-1139.
67. Lee JE, Chung MK, Lazar M, DuBray MB, Kim J, et al. (2009) A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis. Neuroimage 44: 870-883.
68. Van Hecke W, Leemans A, De Backer S, Jeurissen B, Parizel PM, et al. (2010) Comparing isotropic and anisotropic smoothing for voxel-based DTI analyzes: A simulation study. Hum Brain Mapp 31: 98-114.
69. Martin-Fernandez M, Alberola-Lopez C, Ruiz-Alzola J, Westin CF, (2007) Sequential anisotropic Wiener filtering applied to 3D MRI data. Magn Reson Imaging 25: 278-292.
70. Duncan GE, Knapp DJ, Breese GR, (1996) Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety. Brain Res 713: 79-91.
71. Merker B (2007) Consciousness without a cerebral cortex: a challenge for neuroscience and medicine. Behav Brain Sci 30: 63-81; discussion 81-134.
72. Butler RK, White LC, Frederick-Duus D, Kaigler KF, Fadel JR, et al. (2012) Comparison of the activation of somatostatin- and neuropeptide Y-containing neuronal populations of the rat amygdala following two different anxiogenic stressors. Exp Neurol 238: 52-63.
73. Daenen EW, Van der Heyden JA, Kruse CG, Wolterink G, Van Ree JM, (2001) Adaptation and habituation to an open field and responses to various stressful events in animals with neonatal lesions in the amygdala or ventral hippocampus. Brain Res 918: 153-165.
74. Orsini CA, Kim JH, Knapska E, Maren S, (2011) Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. J Neurosci 31: 17269-17277.
75. Haber SN, Calzavara R, (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78: 69-74.
76. Toft PB, (1999) Prenatal and perinatal striatal injury: a hypothetical cause of attention-deficit-hyperactivity disorder? Pediatr Neurol 21: 602-610.
77. Torta DM, Cauda F, (2011) Different functions in the cingulate cortex, a meta-analytic connectivity modeling study. Neuroimage 56: 2157-2172.
78. Tromp do PM, Grupe DW, Oathes DJ, McFarlin DR, Hernandez PJ, et al. (2012) Reduced structural connectivity of a major frontolimbic pathway in generalized anxiety disorder. Arch Gen Psychiatry 69: 925-934.
79. Papez JW, (1995) A proposed mechanism of emotion. 1937. J Neuropsychiatry Clin Neurosci 7: 103-112.
80. Squire LR, (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195-231.
81. VanElzakker M, Fevurly RD, Breindel T, Spencer RL, (2008) Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. Learn Mem 15: 899-908.
82. Battaglia FP, Pennartz CM, (2011) The construction of semantic memory: grammar-based representations learned from relational episodic information. Front Comput Neurosci 5: 36.
83. Zola-Morgan SM, Squire LR, (1990) The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 250: 288-290.
84. Otto T, Eichenbaum H, (1992) Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. Behav Neurosci 106: 762-775.
85. Brown MW, Warburton EC, Aggleton JP, (2010) Recognition memory: material, processes, and substrates. Hippocampus 20: 1228-1244.
86. Delatour B, Witter MP, (2002) Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur J Neurosci 15: 1400-1407.
87. Powell HW, Guye M, Parker GJ, Symms MR, Boulby P, et al. (2004) Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus. Neuroimage 22: 740-747.
88. Watanabe Y, Funahashi S, (2012) Thalamic mediodorsal nucleus and working memory. Neurosci Biobehav Rev 36: 134-142.
89. Royston P, (1993) A pocket-calculator algorithm for the Shapiro-Francia test for non-normality: an application to medicine. Stat Med 12: 181-184.
90. Robinson S, Petelenz K, Li Q, Cohen ML, Dechant A, et al. (2005) Developmental changes induced by graded prenatal systemic hypoxic-ischemic insults in rats. Neurobiol Dis 18: 568-581.
91. Koob GF, Heinrichs SC, Pich EM, Menzaghi F, Baldwin H, et al. (1993) The role of corticotropin-releasing factor in behavioural responses to stress. Ciba Found Symp 172: 277-289; discussion 290-275.
92. Spruijt BM, van Hooff JA, Gispen WH, (1992) Ethology and neurobiology of grooming behavior. Physiol Rev 72: 825-852.
93. Lubics A, Reglodi D, Tamas A, Kiss P, Szalai M, et al. (2005) Neurological reflexes and early motor behavior in rats subjected to neonatal hypoxic-ischemic injury. Behav Brain Res 157: 157-165.
94. Delcour M, Olivier P, Chambon C, Pansiot J, Russier M, et al. (2012) Neuroanatomical, sensorimotor and cognitive deficits in adult rats with white matter injury following prenatal ischemia. Brain Pathol 22: 1-16.
95. Delcour M, Russier M, Amin M, Baud O, Paban V, et al. (2012) Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behav Brain Res 232: 233-244.
96. Sizonenko SV, Camm EJ, Garbow JR, Maier SE, Inder TE, et al. (2007) Developmental changes and injury induced disruption of the radial organization of the cortex in the immature rat brain revealed by in vivo diffusion tensor MRI. Cereb Cortex 17: 2609-2617.
97. Wang S, Wu EX, Cai K, Lau HF, Cheung PT, et al. (2009) Mild hypoxic-ischemic injury in the neonatal rat brain: longitudinal evaluation of white matter using diffusion tensor MR imaging. AJNR Am J Neuroradiol 30: 1907-1913.
98. Larvaron P, Boespflug-Tanguy O, Renou JP, Bonny JM, (2007) In vivo analysis of the post-natal development of normal mouse brain by DTI. NMR Biomed 20: 413-421.
99. Paus T, Collins DL, Evans AC, Leonard G, Pike B, et al. (2001) Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull 54: 255-266.
100. Tolcos M, Bateman E, O'Dowd R, Markwick R, Vrijsen K, et al. (2011) Intrauterine growth restriction affects the maturation of myelin. Exp Neurol 232: 53-65.
101. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, et al. (2004) Regional dissociations within the hippocampus--memory and anxiety. Neurosci Biobehav Rev 28: 273-283.
102. Deacon RM, Croucher A, Rawlins JN, (2002) Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behav Brain Res 132: 203-213.
103. Emond V, Joyal C, Poissant H, (2009) Structural and functional neuroanatomy of attention-deficit hyperactivity disorder (ADHD). Encephale 35: 107-114.
104. Spampinato MV, Wood JN, De Simone V, Grafman J, (2009) Neural correlates of anxiety in healthy volunteers: a voxel-based morphometry study. J Neuropsychiatry Clin Neurosci 21: 199-205.
105. Miller MM, Morrison JH, McEwen BS, (2012) Basal anxiety-like behavior predicts differences in dendritic morphology in the medial prefrontal cortex in two strains of rats. Behav Brain Res 229: 280-288.
106. Vetere G, Restivo L, Cole CJ, Ross PJ, Ammassari-Teule M, et al. (2011) Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. Proc Natl Acad Sci U S A 108: 8456-8460.
107. Weible AP, Rowland DC, Monaghan CK, Wolfgang NT, Kentros CG, (2012) Neural correlates of long-term object memory in the mouse anterior cingulate cortex. J Neurosci 32: 5598-5608.
108. Weible AP, Rowland DC, Pang R, Kentros C, (2009) Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. J Neurophysiol 102: 2055-2068.
109. Zhao P, Zuo Z, (2005) Prenatal hypoxia-induced adaptation and neuroprotection that is inducible nitric oxide synthase-dependent. Neurobiology of disease 20: 871-880.
110. Einarsson EÖ, Nader K, (2012) Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory. Learn Mem 19: 449-452.
111. Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, et al. (2011) DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. Neuroimage 55: 880-890.
112. Hillary FG, Medaglia JD, Gates K, Molenaar PC, Slocomb J, et al. (2011) Examining working memory task acquisition in a disrupted neural network. Brain 134: 1555-1570.
113. Yin X, Han Y, Ge H, Xu W, Huang R, et al. (2011) Inferior frontal white matter asymmetry correlates with executive control of attention. Hum Brain Mapp doi: 10.1002/hbm.21477.
114. Kim MJ, Whalen PJ, (2009) The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J Neurosci 29: 11614-11618.
115. Modi S, Trivedi R, Singh K, Kumar P, Rathore RK, et al. (2013) Individual differences in trait anxiety are associated with white matter tract integrity in fornix and uncinate fasciculus: preliminary evidence from a DTI based tractography study. Behav Brain Res 238: 188-192.
116. Sarkar S, Craig MC, Catani M, Dell'acqua F, Fahy T, et al. (2012) Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study. Psychol Med 43: 401-411.
117. Tamm L, Barnea-Goraly N, Reiss AL, (2012) Diffusion tensor imaging reveals white matter abnormalities in Attention-Deficit/Hyperactivity Disorder. Psychiatry Res 202: 150-154.
118. Wang Y, Horst KK, Kronenberger WG, Hummer TA, Mosier KM, et al. (2012) White matter abnormalities associated with disruptive behavior disorder in adolescents with and without attention-deficit/hyperactivity disorder. Psychiatry Res 202: 245-251.
119. Ortibus E, Verhoeven J, Sunaert S, Casteels I, de Cock P, et al. (2012) Integrity of the inferior longitudinal fasciculus and impaired object recognition in children: a diffusion tensor imaging study. Dev Med Child Neurol 54: 38-43.
120. Rogalski EJ, Murphy CM, deToledo-Morrell L, Shah RC, Moseley ME, et al. (2009) Changes in parahippocampal white matter integrity in amnestic mild cognitive impairment: a diffusion tensor imaging study. Behav Neurol 21: 51-61.
121. Wang Y, West JD, Flashman LA, Wishart HA, Santulli RB, et al. (2012) Selective changes in white matter integrity in MCI and older adults with cognitive complaints. Biochim Biophys Acta 1822: 423-430.
122. Hardee JE, Thompson JC, Puce A, (2008) The left amygdala knows fear: laterality in the amygdala response to fearful eyes. Soc Cogn Affect Neurosci 3: 47-54.
123. Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, et al. (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci U S A 107: 19067-19072.
124. Salami M, Itami C, Tsumoto T, Kimura F, (2003) Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex. Proc Natl Acad Sci U S A 100: 6174-6179.
125. Roze E, Harris PA, Ball G, Elorza LZ, Braga RM, et al. (2011) Tractography of the corticospinal tracts in infants with focal perinatal injury: comparison with normal controls and to motor development. Neuroradiology 54: 507-516.
126. Son SM, Ahn YH, Sakong J, Moon HK, Ahn SH, et al. (2007) Diffusion tensor imaging demonstrates focal lesions of the corticospinal tract in hemiparetic patients with cerebral palsy. Neurosci Lett 420: 34-38.
127. Sun SW, Neil JJ, Song SK, (2003) Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med 50: 743-748.
128. Sun SW, Neil JJ, Liang HF, He YY, Schmidt RE, et al. (2005) Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn Reson Med 53: 1447-1451.
129. Institute of Medicine (US) Forum on Neuroscience and Nervous System Disorders. Sex Differences and Implications for Translational Neuroscience Research: Workshop Summary. Washington (DC): National Academies Press (US); 2011. Institute of Medicine Forum on Neuroscience and Nervous System Disorders website. Available: http://www.ncbi.nlm.nih.gov/books/NBK53390/. Accessed 2013 September.