Hostname: page-component-77c89778f8-9q27g Total loading time: 0 Render date: 2024-07-18T22:16:36.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of combined IUGR and prenatal stress on the development of the hippocampus in a fetal guinea pig model

Published online by Cambridge University Press:  15 May 2017

A. L. Cumberland ,
H. K. Palliser ,
P. Rani ,
D. W. Walker  and
J. J. Hirst
A. L. Cumberland*
Affiliation:
School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia Mothers and Babies Research Centre, Hunter Medical Research Institute, Newcastle, NSW, Australia
H. K. Palliser
Affiliation:
School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia Mothers and Babies Research Centre, Hunter Medical Research Institute, Newcastle, NSW, Australia
P. Rani
Affiliation:
School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia Mothers and Babies Research Centre, Hunter Medical Research Institute, Newcastle, NSW, Australia
D. W. Walker
Affiliation:
Monash Medical Centre, Hudson Institute of Medical Research, Clayton, VIC, Australia
J. J. Hirst
Affiliation:
School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia Mothers and Babies Research Centre, Hunter Medical Research Institute, Newcastle, NSW, Australia
*
*Address for correspondence: A. L. Cumberland, School of Biomedical Sciences and Pharmacy, University of Newcastle 2308, NSW, Australia. (Email: Angela.Cumberland@uon.edu.au)
Get access Rights & Permissions [Opens in a new window]

Abstract

Intrauterine growth restriction (IUGR) and maternal stress during pregnancy are two compromises that negatively impact neurodevelopment and increase the risk of developing later life neuropsychiatric disorders such as schizophrenia, depression and behavioural disorders. Neurosteroids, particularly allopregnanolone, are important in protecting the developing brain and promoting many essential neurodevelopmental processes. Individually, IUGR and prenatal stress (PS) reduce myelination and neurogenesis within affected fetal brains, however less information is available on the combined effects of these two disorders on the term fetal brain. This study aimed to investigate how IUGR and PS impairs the neurosteroid pathway when combined using a guinea pig model, and how these then disrupt the neurodevelopment of the fetus. Uterine artery blood flow restriction was performed at GA30-35 to induce growth restriction, whilst PS was induced by exposure of the dam to a strobe light during gestation commencing GA40 and repeated every 5 days. Exposure in this model caused reductions in hippocampal CA1 MBP immunostaining of male fetuses in both IUGR alone and IUGR+PS paradigms but only by IUGR in the subcortical white mater, compared with control males. Plasma allopregnanolone was reduced by both stressors irrespective of sex, whereas GFAP or MAP2 expression were not affected by either stressor. Female neurodevelopment, as assessed by these markers, was unimpeded by these compromises. The addition of prenatal stress did not further compound these deficits.

Keywords

allopregnanoloneintrauterine growth restrictionmyelinationneurodevelopmentprenatal stress
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 5: Themed Issue: Australian Perspectives: Outcomes from the 2016 ANZ , October 2017 , pp. 584 - 596
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Bernstein, IM, Horbar, JD, Badger, GJ, Ohlsson, A, Golan, A. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. Am J Obstet Gynecol. 2000; 182, 198–206.Google Scholar
2. Tideman, E, Maršál, K, Ley, D. Cognitive function in young adults following intrauterine growth restriction with abnormal fetal aortic blood flow. Ultrasound Obstet Gynecol. 2007; 29, 614–618.Google Scholar
3. Jacobsson, B, Francis, A, Hagberg, G, Hagberg, H, Gardosi, J. Cerebral palsy is strongly associated with severe intrauterine growth restriction in term but not in preterm cases. Am J Obstet Gynecol. 2003; 189, S74.CrossRefGoogle Scholar
4. Campbell, S, Thoms, A. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. BJOG. 1977; 84, 165–174.CrossRefGoogle ScholarPubMed
5. Leitner, Y, Fattal-Valevski, A, Geva, R, et al. Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol. 2007; 22, 580–587.Google Scholar
6. Geva, R, Eshel, R, Leitner, Y, Valevski, AF, Harel, S. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics. 2006; 118, 91–100.CrossRefGoogle ScholarPubMed
7. Guedeney, A, Marchand-Martin, L, Cote, SJ, Larroque, B. Perinatal risk factors and social withdrawal behaviour. Eur Child Adolesc Psychiatry. 2012; 21, 185–191.CrossRefGoogle ScholarPubMed
8. Heinonen, K, Räikkönen, K, Pesonen, A-K, et al. Behavioural symptoms of attention deficit/hyperactivity disorder in preterm and term children born small and appropriate for gestational age: a longitudinal study. BMC Pediatr. 2010; 10.CrossRefGoogle ScholarPubMed
9. Savchev, S, Sanz-Cortes, M, Cruz-Martinez, R, et al. Neurodevelopmental outcome of full-term small-for-gestational-age infants with normal placental function. Ultrasound Obstet Gynecol. 2013; 42, 201–206.Google Scholar
10. Paz, I, Gale, R, Laor, A, et al. The cognitive outcome of full-term small for gestational age infants at late adolescence. Obstet Gynecol. 1995; 85, 452–456.Google ScholarPubMed
11. Paz, I, Laor, A, Gale, R, et al. Term infants with fetal growth restriction are not at increased risk for low intelligence scores at age 17 years. J Pediatr. 2001; 138, 87–91.Google Scholar
12. Eixarch, E, Batalle, D, Illa, M, et al. Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PLoS One. 2012; 7, e31497.Google Scholar
13. Mallard, C, Loeliger, M, Copolov, D, Rees, S. Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction. Neuroscience. 2000; 100, 327–333.Google Scholar
14. Nitsos, I, Rees, S. The effects of intrauterine growth retardation on the development of neuroglia in fetal guinea pigs. An immunohistochemical and an ultrastructural study. Int J Dev Neurosci. 1990; 8, 233–244.Google Scholar
15. Kelleher, MA, Palliser, HK, Walker, DW, Hirst, JJ. Sex-dependent effect of a low neurosteroid environment and intrauterine growth restriction on fetal guinea pig brain development. J Endocrinol. 2011; 208, 301–309.Google Scholar
16. Castellanos, F, Lee, PP, Sharp, W, et al. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA. 2002; 288, 1740–1748.Google Scholar
17. Hamilton, LS, Levitt, JG, O’Neill, J, et al. Reduced white matter integrity in attention-deficit hyperactivity disorder. Neuroreport. 2008; 19, 1705–1708.Google Scholar
18. Olivier, P, Baud, O, Bouslama, M, et al. Moderate growth restriction: deleterious and protective effects on white matter damage. Neurobiol Dis. 2007; 26, 253–263.Google Scholar
19. Olivier, P, Baud, O, Evrard, P, Gressens, P, Verney, C. Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol. 2005; 64, 998–1006.CrossRefGoogle ScholarPubMed
20. Trejo, JL, Cuchillo, I, Machín, C, Rúa, C. Maternal adrenalectomy at the early onset of gestation impairs the postnatal development of the rat hippocampal formation: effects on cell numbers and differentiation, connectivity and calbindin-D28k immunoreactivity. J Neurosci Res. 2000; 62, 644–667.Google Scholar
21. Matthews, SG. Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res. 2000; 47, 291–300.Google Scholar
22. Kraszpulski, M, Dickerson, PA, Salm, AK. Prenatal stress affects the developmental trajectory of the rat amygdala. Stress. 2006; 9, 85–95.Google Scholar
23. Lemaire, V, Koehl, M, Le Moal, M, Abrous, DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci. 2000; 97, 11032–11037.Google Scholar
24. Martínez-Téllez, RI, Hernández-Torres, E, Gamboa, C, Flores, G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 2009; 63, 794–804.Google Scholar
25. Bennett, GA, Palliser, HK, Saxby, B, Walker, DW, Hirst, JJ. Effects of prenatal stress on fetal neurodevelopment and responses to maternal neurosteroid treatment in guinea pigs. Dev Neurosci. 2013; 35, 416–426.Google Scholar
26. Bennett, GA, Palliser, HK, Shaw, JC, Walker, D, Hirst, JJ. Prenatal stress alters hippocampal neuroglia and increases anxiety in childhood. Dev Neurosci. 2015; 37, 533–545.CrossRefGoogle ScholarPubMed
27. Laplante, DP, Barr, RG, Brunet, A, et al. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res. 2004; 56, 400–410.Google Scholar
28. Laplante, DP, Zelazo, PR, Brunet, A, King, S. Functional play at 2 years of age: effects of prenatal maternal stress. Infancy. 2007; 12, 69–93.Google Scholar
29. Dancause, KN, Laplante, DP, Oremus, C, et al. Disaster-related prenatal maternal stress influences birth outcomes: Project Ice Storm. Early Hum Dev. 2011; 87, 813–820.Google Scholar
30. Beversdorf, DQ, Manning, SE, Hillier, A, et al. Timing of prenatal stressors and autism. J Autism Dev Disord. 2005; 35, 471–478.CrossRefGoogle ScholarPubMed
31. de Weerth, C, van Hees, Y, Buitelaar, JK. Prenatal maternal cortisol levels and infant behavior during the first 5 months. Early Hum Dev. 2003; 74, 139–151.Google Scholar
32. Niederhofer, H, Reiter, A. Prenatal maternal stress, prenatal fetal movements and perinatal temperament factors influence behavior and school marks at the age of 6 years. Fetal Diagn Ther. 2004; 19, 160–162.Google Scholar
33. Brouwers, EPM, van Baar, AL, Pop, VJM. Maternal anxiety during pregnancy and subsequent infant development. Infant Behav Dev. 2001; 24, 95–106.Google Scholar
34. Kleinhaus, K, Harlap, S, Perrin, M, et al. Prenatal stress and affective disorders in a population birth cohort. Bipolar Disord. 2013; 15, 92–99.Google Scholar
35. Walder, DJ, Laplante, DP, Sousa-Pires, A, et al. Prenatal maternal stress predicts autism traits in $6\raise.5ex\hbox{$\scriptstyle 1$}\kern-.1em/ \kern-.15em\lower.25ex\hbox{$\scriptstyle 2$} $ year-old children: Project Ice Storm. Psychiatry Res. 2014; 219, 353–360.Google Scholar
36. Zhu, P, Hao, J-H, Tao, R-X, et al. Sex-specific and time-dependent effects of prenatal stress on the early behavioral symptoms of ADHD: a longitudinal study in China. Eur Child Adolesc Psychiatry. 2015; 24, 1139–1147.Google Scholar
37. van Os, J, Selten, JP. Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of the Netherlands. Br J Psychiatry. 1998; 172, 324–326.Google Scholar
38. Coe, CL, Kramer, M, Czéh, B, et al. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry. 2003; 54, 1025–1034.Google Scholar
39. Kapoor, A, Matthews, SG. Short periods of prenatal stress affect growth, behaviour and hypothalamo–pituitary–adrenal axis activity in male guinea pig offspring. J Physiol. 2005; 566, 967–977.CrossRefGoogle ScholarPubMed
40. Kapoor, A, Matthews, SG. Prenatal stress modifies behavior and hypothalamic-pituitary-adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle. Endocrinology. 2008; 149, 6406–6415.Google Scholar
41. Gilbert Evans, SE, Ross, LE, Sellers, EM, Purdy, RH, Romach, MK. 3α-reduced neuroactive steroids and their precursors during pregnancy and the postpartum period. Gynecol Endocrinol. 2005; 21, 268–279.Google Scholar
42. Ghoumari, AM, Ibanez, C, El-Etr, M, et al. Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. J Neurochem. 2003; 86, 848–859.Google Scholar
43. Xilouri, M, Papazafiri, P. Anti-apoptotic effects of allopregnanolone on P19 neurons. Eur J Neurosci. 2006; 23, 43–54.Google Scholar
44. Yawno, T, Yan, EB, Walker, DW, Hirst, JJ. Inhibition of neurosteroid synthesis increases asphyxia-induced brain injury in the late gestation fetal sheep. Neuroscience. 2007; 146, 1726–1733.Google Scholar
45. Belelli, D, Lambert, JJ. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci. 2005; 6, 565–575.CrossRefGoogle ScholarPubMed
46. Nguyen, PN, Yan, EB, Castillo-Melendez, M, Walker, DW, Hirst, JJ. Increased allopregnanolone levels in the fetal sheep brain following umbilical cord occlusion. J Physiol. 2004; 560, 593–602.CrossRefGoogle ScholarPubMed
47. Barbaccia, ML, Roscetti, G, Trabucchi, M, et al. Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroendocrinology. 1996; 63, 166–172.Google Scholar
48. Bennett, GA, Palliser, HK, Walker, D, Hirst, J. Severity and timing: how prenatal stress exposure affects glial developmental, emotional behavioural and plasma neurosteroid responses in guinea pig offspring. Psychoneuroendocrinology. 2016; 70, 47–57.Google Scholar
49. Nguyen, PN, Billiards, SS, Walker, DW, Hirst, JJ. Changes in 5alpha-pregnane steroids and neurosteroidogenic enzyme expression in fetal sheep with umbilicoplacental embolization. Pediatr Res. 2003; 54, 840–847.CrossRefGoogle ScholarPubMed
50. Bowers, G, Cullinan, WE, Herman, JP. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci. 1998; 18, 5938–5947.Google Scholar
51. Gilabert-Juan, J, Castillo-Gomez, E, Pérez-Rando, M, Moltó, MD, Nacher, J. Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. Exp Neurol. 2011; 232, 33–40.Google Scholar
52. Varea, E, Guirado, R, Gilabert-Juan, J, et al. Expression of PSA-NCAM and synaptic proteins in the amygdala of psychiatric disorder patients. J Psychiatr Res. 2012; 46, 189–197.Google Scholar
53. Yip, J, Soghomonian, J-J, Blatt, GJ. Decreased GAD67 mRNA levels in cerebellar Purkinje cells in autism: pathophysiological implications. Acta Neuropathol (Berl). 2007; 113, 559–568.Google Scholar
54. Herrera, EA, Alegría, R, Farias, M, et al. Assessment of in vivo fetal growth and placental vascular function in a novel intrauterine growth restriction model of progressive uterine artery occlusion in guinea pigs. J Physiol. 2016; 594, 1553–1561.Google Scholar
55. McKendry, AA, Palliser, HK, Yates, DM, Walker, DW, Hirst, JJ. The effect of betamethasone treatment on neuroactive steroid synthesis in a fetal guinea pig model of growth restriction. J Neuroendocrinol. 2010; 22, 166–174.Google Scholar
56. Bayer, SA, Altman, J, Russo, RJ, Zhang, X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 1993; 14, 83–144.Google Scholar
57. Tau, GZ, Peterson, BS. Normal development of brain circuits. Neuropsychopharmacology. 2009; 35, 147–168.Google Scholar
58. Dobbing, J, Sands, J. Growth and development of the brain and spinal cord of the guinea pig. Brain Res. 1970; 17, 115–123.Google Scholar
59. Dyson, RM, Palliser, HK, Kelleher, MA, Hirst, JJ, Wright, IMR. The guinea pig as an animal model for studying perinatal changes in microvascular function. Pediatr Res. 2011; 71, 20–24.Google Scholar
60. Kelleher, MA, Hirst, JJ, Palliser, HK. Changes in neuroactive steroid concentrations after preterm delivery in the guinea pig. Reprod Sci. 2013; 20, 1365–1375.Google Scholar
61. Shaw, JC, Palliser, HK, Dyson, RM, Hirst, JJ, Berry, MJ. Long-term effects of preterm birth on behavior and neurosteroid sensitivity in the guinea pig. Pediatr Res. 2016; 80, 275–283.Google Scholar
62. Thompson, JA, Gros, R, Richardson, BS, Piorkowska, K, Regnault, TRH. Central stiffening in adulthood linked to aberrant aortic remodeling under suboptimal intrauterine conditions. Am J Physiol. 2011; 301, R1731–R1737.Google Scholar
63. Piorkowska, K, Thompson, J, Nygard, K, et al. Synaptic development and neuronal myelination are altered with growth restriction in fetal guinea pigs. Dev Neurosci. 2014; 36, 465–476.Google Scholar
64. Thompson, JA, Sarr, O, Piorkowska, K, Gros, R, Regnault, TRH. Low birth weight followed by postnatal over-nutrition in the guinea pig exposes a predominant player in the development of vascular dysfunction. J Physiol. 2014; 592, 5429–5443.Google Scholar
65. Shaw, JC, Palliser, HK, Walker, DW, Hirst, JJ. Preterm birth affects GABAA receptor subunit mRNA levels during the foetal-to-neonatal transition in guinea pigs. J Dev Orig Health Dis. 2015; 6, 250–260.Google Scholar
66. Etkin, A, Wager, TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry. 2007; 164, 1476–1488.Google Scholar
67. Gale, GD, Anagnostaras, SG, Godsil, BP, et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci. 2004; 24, 3810–3815.Google Scholar
68. Walf, AA, Sumida, K, Frye, CA. Inhibiting 5α-reductase in the amygdala attenuates antianxiety and antidepressive behavior of naturally receptive and hormone-primed ovariectomized rats. Psychopharmacology (Berl). 2006; 186, 302–311.Google Scholar
69. Xu, J, Yang, B, Yan, C, et al. Effects of duration and timing of prenatal stress on hippocampal myelination and synaptophysin expression. Brain Res. 2013; 1527, 57–66.Google Scholar
70. Tolcos, M, Bateman, E, O’Dowd, R, et al. Intrauterine growth restriction affects the maturation of myelin. Exp Neurol. 2011; 232, 53–65.Google Scholar
71. Flynn, SW, Lang, DJ, Mackay, AL, et al. Abnormalities of myelination in schizophrenia detected in vivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Mol Psychiatry. 2003; 8, 811–820.Google Scholar
72. Aleman, A, Kahn, RS, Selten, J. Sex differences in the risk of schizophrenia: evidence from meta-analysis. Arch Gen Psychiatry. 2003; 60, 565–571.Google Scholar
73. Iacono, W, Beirser, M. Are males more likely than females to develop schizophrenia? Am J Psychiatry. 1992; 149, 1070–1074.Google Scholar
74. Tham, MW, Woon, PS, Sum, MY, Lee, T-S, Sim, K. White matter abnormalities in major depression: evidence from post-mortem, neuroimaging and genetic studies. J Affect Disord. 2011; 132, 26–36.Google Scholar
75. Bergman, K, Sarkar, P, O’Connor, TG, Modi, N, Glover, V. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry. 2007; 46, 1454–1463.Google Scholar
76. Van den Bergh, BRH, Marcoen, A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev. 2004; 75, 1085–1097.Google Scholar
77. Van den Bergh, BR, Mennes, M, Oosterlaan, J, et al. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev. 2005; 29, 259–269.Google Scholar
78. Watson, JB, Mednick, SA, Huttunen, M, Wang, X. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol. 1999; 11, 457–466.Google Scholar
79. Lockhart, EM, Warner, DS, Pearlstein, RD, et al. Allopregnanolone attenuates N-methyl-d-aspartate-induced excitotoxicity and apoptosis in the human NT2 cell line in culture. Neurosci Lett. 2002; 328, 33–36.CrossRefGoogle ScholarPubMed
80. Droogleever Fortuyn, HA, van Broekhoven, F, Span, PN, et al. Effects of PhD examination stress on allopregnanolone and cortisol plasma levels and peripheral benzodiazepine receptor density. Psychoneuroendocrinology. 2004; 29, 1341–1344.Google Scholar
81. Rasmusson, AM, Pinna, G, Paliwal, P, et al. Decreased cerebrospinal fluid allopregnanolone levels in women with posttraumatic stress disorder. Biol Psychiatry. 2006; 60, 704–713.Google Scholar
82. Follesa, P, Serra, M, Cagetti, E, et al. Allopregnanolone synthesis in cerebellar granule cells: roles in regulation of GABAA receptor expression and function during progesterone treatment and withdrawal. Mol Pharmacol. 2000; 57, 1262–1270.Google Scholar
83. Maguire, JL, Stell, BM, Rafizadeh, M, Mody, I. Ovarian cycle-linked changes in GABAA receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci. 2005; 8, 797–804.Google Scholar
84. Reddy, DS, Jian, K. The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. J Pharmacol Exp Ther. 2010; 334, 1031–1041.Google Scholar
85. Reddy, DS, Rogawski, MA. Stress-induced deoxycorticosterone-derived neurosteroids modulate GABAA receptor function and seizure susceptibility. J Neurosci. 2002; 22, 3795–3805.Google Scholar
86. Mellon, SH. Synthesis, Enzyme Localization, and Regulation of Neurosteroids. Neurosteroid Effects in the Central Nervous System: The Role of the GABAA Receptor. Boca Raton, FL, US: CRC Press, 2004; pp. 1–46.Google Scholar
87. Dauprat, P, Monin, G, Dalle, M, Delost, P. The effects of psychosomatic stress at the end of pregnancy on maternal and fetal plasma cortisol levels and liver glycogen in guinea-pigs. Reprod Nutr Dev. 1984; 24, 45–51.Google Scholar
88. Nilsson, E, Stålberg, G, Lichtenstein, P, et al. Fetal growth restriction and schizophrenia: a Swedish twin study. Twin Res Hum Genet. 2005; 8, 402–408.Google Scholar
89. Batalle, D, Eixarch, E, Figueras, F, et al. Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome. Neuroimage. 2012; 60, 1352–1366.CrossRefGoogle ScholarPubMed
90. Wang, L, Zhu, C, He, Y, et al. Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder. Hum Brain Mapp. 2009; 30, 638–649.Google Scholar
91. Alexander-Bloch, AF, Gogtay, N, Meunier, D, et al. Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci. 2010; 4.Google Scholar
92. Dickinson, H, Miller, S, Nitsos, I, et al. Reduced uterine blood flow induces asymmetric growth restriction in spiny mouse fetuses. Fetal and Neonatal Physiological Society. Saint Vincent, Italy 2014.Google Scholar
93. Lafeber, HN, Rolph, TP, Jones, CT. Studies on the growth of the fetal guinea pig. The effects of ligation of the uterine artery on organ growth and development. J Dev Physiol. 1984; 6, 441–459.Google Scholar
94. Turner, AJ, Trudinger, BJ. A modification of the uterine artery restriction technique in the guinea pig fetus produces asymmetrical ultrasound growth. Placenta. 2009; 30, 236–240.Google Scholar
95. Dieni, S, Rees, S. Dendritic morphology is altered in hippocampal neurons following prenatal compromise. J Neurobiol. 2003; 55, 41–52.Google Scholar
Supplementary material: File

Cumberland supplementary material

Table S1

Download Cumberland supplementary material(File)
File 110 KB