Subcortical band heterotopia in rat offspring following maternal hypothyroxinaemia: Structural and functional characteristics

Journal of Neuroendocrinology

Volumn 26, Issue 8, 2014, Pages 528-541

  Gilbert, M E ^a   Ramos, R L ^b   Mccloskey, D P ^c   Goodman, J H ^d,e  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^e Downstate Health Sciences University   (United States)

Author keywords

Foetal brain; Hypothyroxinaemia; Neuronal migration; Thyroid hormone propylthiouracil

Indexed keywords

ANTITHYROID AGENT; DRINKING WATER; LIOTRIX; PROPYLTHIOURACIL; THYROID HORMONE; THYROXINE; LIOTHYRONINE; PENTETRAZOLE; THYROTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN REGION; CONTROLLED STUDY; CORPUS CALLOSUM; DOSE RESPONSE; ELECTRIC POTENTIAL; ENVIRONMENTAL EXPOSURE; EX VIVO STUDY; FEMALE; HYPOTHYROXINEMIA; MATERNAL SERUM; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROGENY; RAT; SEIZURE; SUBCORTICAL HETEROTOPIA; SYSTEMATIC REVIEW; ADVERSE EFFECTS; AGYRIA; ANIMAL; BLOOD; BRAIN; CHEMICALLY INDUCED; COMPLICATION; GLIA; HYPOTHYROIDISM; MEMBRANE POTENTIAL; NERVE CELL; NEUROANATOMICAL TRACT TRACING; PATHOLOGY; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; BRAIN; CLASSICAL LISSENCEPHALIES AND SUBCORTICAL BAND HETEROTOPIAS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HYPOTHYROIDISM; MATERNAL EXPOSURE; MEMBRANE POTENTIALS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEUROGLIA; NEURONS; PENTYLENETETRAZOLE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROPYLTHIOURACIL; RATS; SEIZURES; THYROTROPIN; THYROXINE; TRIIODOTHYRONINE;

EID: 84904538904     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12169     Document Type: Article

References (100)

1. Rovet J, Willoughby K. Maternal thyroid function during pregnancy: effects on the developing fetus. In: Zimmerman AW, Connors SL, eds. Maternal Influences on Fetal Neurodevelopment: Clinical and Research Aspects. New York, NY: Springer, 2010: 55-77.
2. Haddow JE, Palomaki GE, Allan WC, Williams JR, Knight GJ, Gagnon J, O'Heir CE, Mitchell ML, Hermos RJ, Waisbren SE, Faix JD, Klein RZ. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 1999; 341: 549-555.
3. Pop VJ, Brouwers EP, Vader HL, Vulsma T, van Baar AL, de Vijlder JJ. Maternal hypothyroxinaemia during early pregnancy and subsequent child development: a 3-year follow-up study. Clin Endocrinol (Oxf) 2003; 59: 282-288.
4. Willoughby KA, McAndrews MP, Rovet J. Effects of maternal hypothyroidism on offspring hippocampus and memory. Thyroid 2014; 24: 576-584.
5. Willoughby KA, McAndrews MP, Rovet J. Effects of early thyroid hormone deficiency on children's autobiographical memory performance. J Int Neuropsychol Soc 2013; 19: 419-429.
6. Henrichs J, Bongers-Schokking JJ, Schenk JJ, Ghassabian A, Schmidt HG, Visser TJ, Hooijkaas H, de Muinck Keizer-Schrama SM, Hofman A, Jaddoe VV, Visser W, Steegers EA, Verhulst FC, de Rijke YB, Tiemeier H. Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J Clin Endocrinol Metab 2010; 95: 4227-4234.
7. Anderson GW, Schoonover CM, Jones SA. Control of thyroid hormone action in the developing rat brain. Thyroid 2003; 13: 1039-1056.
8. Bernal J. Action of thyroid hormone in brain. J Endocrinol Invest 2002; 25: 268-288.
9. Brosvic GM, Taylor JN, Dihoff RE. Influences of early thyroid hormone manipulations: delays in pup motor and exploratory behavior are evident in adult operant performance. Physiol Behav 2002; 75: 697-715.
10. Davenport JW, Dorcey TP. Hypothyroidism: learning deficit induced in rats by early exposure to thiouracil. Horm Behav 1972; 3: 97-112.
11. Goldey ES, Kehn LS, Rehnberg GL, Crofton KM. Effects of developmental hypothyroidism on auditory and motor function in the rat. Toxicol Appl Pharmacol 1995; 135: 67-76.
12. Akaike M, Kato N, Ohno H, Kobayashi T. Hyperactivity and spatial maze learning impairment of adult rats with temporary neonatal hypothyroidism. Neurotoxicol Teratol 1991; 13: 317-322.
13. Darbra S, Garau A, Balada F, Sala J, Marti-Carbonell MA. Perinatal hypothyroidism effects on neuromotor competence, novelty-directed exploratory and anxiety-related behaviour and learning in rats. Behav Brain Res 2003; 143: 209-215.
14. Gilbert ME, Sui L. Dose-dependent reductions in spatial learning and synaptic function in the dentate gyrus of adult rats following developmental thyroid hormone insufficiency. Brain Res 2006; 1069: 10-22.
15. Axelstad M, Hansen PR, Boberg J, Bonnichsen M, Nellemann C, Lund SP, Hougaard KS. U H. Developmental neurotoxicity of propylthiouracil (ptu) in rats: relationship between transient hypothyroxinemia during development and long-lasting behavioural and functional changes. Toxicol Appl Pharmacol 2008; 232: 1-13.
16. Dong J, Yin H, Liu W, Wang P, Jiang Y, Chen J. Congenital iodine deficiency and hypothyroidism impair LTP and decrease C-fos and C-jun expression in rat hippocampus. Neurotoxicology 2005; 26: 417-426.
17. Sawin S, Brodish P, Carter CS, Stanton ME, Lau C. Development of cholinergic neurons in rat brain regions: dose-dependent effects of propylthiouracil-induced hypothyroidism. Neurotoxicol Teratol 1998; 20: 627-635.
18. Vara H, Martinez B, Santos A, Colino A. Thyroid hormone regulates neurotransmitter release in neonatal rat hippocampus. Neuroscience 2002; 110: 19-28.
19. Gilbert ME. Alterations in synaptic transmission and plasticity in area CA1 of adult hippocampus following developmental hypothyroidism. Brain Res Dev Brain Res 2004; 148: 11-18.
20. Gilbert ME, Paczkowski C. Propylthiouracil (PTU)-induced hypothyroidism in the developing rat impairs synaptic transmission and plasticity in the dentate gyrus of the adult hippocampus. Brain Res Dev Brain Res 2003; 145: 19-29.
21. Sui L, Gilbert ME. Pre- and postnatal propylthiouracil-induced hypothyroidism impairs synaptic transmission and plasticity in area CA1 of the neonatal rat hippocampus. Endocrinology 2003; 144: 4195-4203.
22. Opazo MC, Gianini A, Pancetti F, Azkcona G, Alarcón L, Lizana R, Noches V, Gonzalez PA, Marassi MP, Mora S, Rosenthal D, Eugenin E, Naranjo D, Bueno SM, Kalergis AM, Riedel CA. Maternal hypothyroxinemia impairs spatial learning and synaptic nature and function in the offspring. Endocrinology 2008; 149: 5097-5106.
23. Gilbert M, Zoeller R. Thyroid hormone - impact on the developing brain: possible mechanisms of neurotoxicity. In: Harry GJ, Tilson HA, eds. Neurotoxicology, 3rd edn, Vol. 3. New York, NY: Informa Healthcare USA, Inc., 2010: 79-111.
24. Stenzel D, Huttner WB. Role of maternal thyroid hormones in the developing neocortex and during human evolution. Front Neuroanat 2013; 7: 19.
25. Verrotti A, Spalice A, Ursitti F, Papetti L, Mariani R, Castronovo A, Mastrangelo M, Iannetti P. New trends in neuronal migration disorders. Eur J Paediatr Neurol 2010; 14: 1-12.
26. Croquelois A, Giuliani F, Savary C, Kielar M, Amiot C, Schenk F, Welker E. Characterization of the heco mutant mouse: a new model of subcortical band heterotopia associated with seizures and behavioral deficits. Cereb Cortex 2009; 19: 563-575.
27. Clark GD. The classification of cortical dysplasias through molecular genetics. Brain Dev 2004; 26: 351-362.
28. Dobyns WB, Truwit CL. Lissencephaly and other malformations of cortical development: 1995 update. Neuropediatrics 1995; 26: 132-147.
29. Auso E, Lavado-Autric R, Cuevas E, Del Rey FE, Morreale De Escobar G, Berbel P. A moderate and transient deficiency of maternal thyroid function at the beginning of fetal neocorticogenesis alters neuronal migration. Endocrinology 2004; 145: 4037-4047.
30. Berbel P, Navarro D, Auso E, Varea E, Rodriguez AE, Ballesta JJ, Salinas M, Flores E, Faura CC, de Escobar GM. Role of late maternal thyroid hormones in cerebral cortex development: an experimental model for human prematurity. Cereb Cortex 2010; 20: 1462-1475.
31. Cuevas E, Auso E, Telefont M, Morreale de Escobar G, Sotelo C, Berbel P. Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur J Neurosci 2005; 22: 541-551.
32. Lavado-Autric R, Auso E, Garcia-Velasco JV, Arufe Mdel C, Escobar del Rey F, Berbel P, Morreale de Escobar G. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 2003; 111: 1073-1082.
33. Goodman J, Gilbert M. Modest thyroid hormone insufficiency during development induces a cellular malformation in the corpus callosum: a model of cortical dysplasia. Endocrinology 2007; 148: 2593-2597.
34. Shiraki A, Akane H, Ohishi T, Wang L, Morita R, Suzuki K, Mitsumori K, Shibutani M. Similar distribution changes of GABAergic interneuron subpopulations in contrast to the different impact on neurogeneisis between developmetnal and adult-stage hypothyroidism in the hippocampal dentate gyrus in rats. Arch Toxicol 2012; 86: 1559-1569.
35. Shibutani M, Woo GH, Fujimoto H, Saegusa Y, Takahashi M, Inoue K, Hirose M, Nishikawa A. Assessment of developmental effects of hypothyroidism in rats from in utero and lactation exposure to anti-thyroid agents. Reprod Toxicol 2009; 28: 297-307.
36. Powell MH, Nguyen HV, Gilbert M, Parekh M, Colon-Perez LM, Mareci TH, Montie E. Magnetic resonance imaging and volumetric analysis: novel tools to study the effects of thyroid hormone disruption on white matter development. Neurotoxicology 2012; 33: 1322-1329.
37. Thibodeaux JR, Hanson RG, Rogers JM, Grey BE, Barbee BD, Richards JH, Butenhoff JL, Stevenson LA, Lau C. Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. I: maternal and prenatal evaluations. Toxicol Sci 2003; 74: 369-381.
38. de Olmos JS. An improved HRP method for the study of central nervous connections. Exp Brain Res 1977; 29: 541-551.
39. Ramos RL, Tam DM, Brumberg JC. Physiology and morphology of callosal projection neurons in mouse. Neuroscience 2008; 153: 654-663.
40. Ramos RL, Smith PT, DeCola C, Tam D, Corzo O, Brumberg JC. Cytoarchitecture and transcriptional profiles of neocortical malformations in inbred mice. Cereb Cortex 2008; 18: 2614-2628.
41. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd edn. New York, NY: Academic Press, 1986.
42. Gilbert ME, Lasley SM. Developmental thyroid hormone insufficiency and brain development: a role for brain-derived neurotrophic factor (BDNF)? Neuroscience 2013; 239: 253-270.
43. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972; 32: 281-294.
44. Johnstone AF, Gilbert ME, Aydin C, Grace CE, Hasegawa M, Gordon CJ. Thermoregulatory deficits in adult Long Evans rat exposed perinatally to the antithyroidal drug, propylthiouracil. Neurotoxicol Teratol 2013; 39: 1-8.
45. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 1996; 224: 855-862.
46. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. Microglia-specific localisation of a novel calcium binding protein, iba1. Brain Res Mol Brain Res 1998; 57: 1-9.
47. Bigl V, Woolf NJ, Butcher LL. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 1982; 8: 727-749.
48. Van Dine SE, Salem E, Patel DB, George E, Ramos RL. Axonal anatomy of molecular layer heterotopia of the cerebellar vermis. J Chem Neuroanat 2013; 47: 90-95.
49. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 1983; 214: 170-197.
50. Levey AI, Wainer BH, Rye DB, Mufson EJ, Mesulam MM. Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons. Neuroscience 1984; 13: 341-353.
51. Sur C, Betz H, Schloss P. Immunocytochemical detection of the serotonin transporter in rat brain. Neuroscience 1996; 73: 217-231.
52. Nielsen K, Brask D, Knudsen GM, Aznar S. Immunodetection of the serotonin transporter protein is a more valid marker for serotonergic fibers than serotonin. Synapse 2006; 59: 270-276.
53. Nagatsu T, Levitt M, Udenfriend S. Tyrosine hyodroylase. The intiaial step in norepinephrine biosynthesis. J Biol Chem 1964; 239: 2910-2917.
54. Mohan V, Sinha RA, Pathak A, Rastogi L, Kumar P, Pal A, Godbole MM. Maternal thyroid hormone deficiency affects the fetal neocorticogenesis by reducing the proliferating pool, rate of neurogenesis and indirect neurogenesis. Exp Neurol 2012; 237: 477-488.
55. Pathak A, Sinha RA, Mohan V, Mitra K, Godbole MM. Maternal thyroid hormone before the onset of fetal thyroid function regulates reelin and downstream signaling cascade affecting neocortical neuronal migration. Cereb Cortex 2011; 21: 11-21.
56. Waterhouse BD, Mihailoff GA, Baack JC, Woodward DJ. Topographical distribution of dorsal and median raphe neurons projecting to motor, sensorimotor, and visual cortical areas in the rat. J Comp Neurol 1986; 249: 460-476, 478-481.
57. Grzanna R, Fritschy JM. Efferent projections of different subpopulations of central noradrenaline neurons. Prog Brain Res 1991; 88: 89-101.
58. Loughlin SE, Foote SL, Fallon JH. Locus coeruleus projections to cortex: topography, morphology and collateralization. Brain Res Bull 1982; 9: 287-294.
59. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 2003; 42: 33-84.
60. Berger B, Gaspar P, Verney C. Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 1991; 14: 21-27.
61. Foote SL, Morrison JH. Development of the noradrenergic, serotonergic, and dopaminergic innervation of neocortex. Curr Top Dev Biol 1987; 21: 391-423.
62. Gilbert ME. Impact of low-level thyroid hormone disruption induced by propylthiouracil on brain development and function. Toxicol Sci 2011; 124: 432-445.
63. Van Middlesworth L, Norris CH. Audiogenic seizures and cochlear damage in rats after perinatal antithyroid treatment. Endocrinology 1980; 106: 1686-1690.
64. Hannan AJ, Servotte S, Katsnelson A, Sisodiya S, Blakemore C, Squier M, Molnar Z. Characterization of nodular neuronal heterotopia in children. Brain 1999; 122: 219-238.
65. Bilasy SE, Satoh T, Ueda S, Wei P, Kanemura H, Aiba A, Terashima T, Kataoka T. Dorsal telencephalon-specific RA-GEF-1 knockout mice develop heterotopic cortical mass and commissural fiber defect. Eur J Neurosci 2009; 29: 1994-2008.
66. Rosen GD, Azoulay NG, Griffin EG, Newbury A, Koganti L, Fujisaki N, Takahashi E, Grant PE, Truong DT, Fitch RH, Lu L, Williams RW. Bilateral subcortical heterotopia with partial callosal agenesis in a mouse mutant. Cereb Cortex 2013; 23: 859-872.
67. Royland JE, Parker JS, Gilbert ME. A genomic analysis of subclinical hypothyroidism in hippocampus and neocortex of the developing rat brain. J Neuroendocrinol 2008; 12: 1319-1338.
68. Gilbert ME, Sui L, Walker MJ, Anderson W, Thomas S, Smoller SN, Schon JP, Phani S, Goodman JH. Thyroid hormone insufficiency during brain development reduces parvalbumin immunoreactivity and inhibitory function in the hippocampus. Endocrinology 2007; 148: 92-102.
69. Berbel P, Marco P, Cerezo JR, DeFelipe J. Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats. Neurosci Lett 1996; 204: 65-68.
70. Bastian TW, Anderson JA, Fretham SJ, Prohaska JR, Georgieff MK, Anderson GW. Fetal and neonatal iron deficiency reduces thyroid hormone-responsive gene mrna levels in the neonatal rat hippocampus and cerebral cortex. Endocrinology 2012; 153: 5668-5680.
71. Bastian TW, Prohaska JR, Georgieff MK, Anderson GW. Fetal and neonatal iron deficiency exacerbates mild thyroid hormone insufficiency effects on male thyroid hormone levels and brain thyroid hormone-responsive gene expression. Endocrinology 2014; 155: 1157-1167.
72. Hadjab-Lallemend S, Wallis K, van Hogerlinden M, Dudazy S, Nordstrom K, Vennstrom B, Fisahn A. A mutant thyroid hormone receptor alpha1 alters hippocampal circuitry and reduces seizure susceptibility in mice. Neuropharmacology 2010; 58: 1130-1139.
73. Rorke LB. A perspective: the role of disordered genetic control of neurogenesis in the pathogenesis of migration disorders. J Neuropathol Exp Neurol 1994; 53: 105-117.
74. Rakic P, Ayoub AE, Breunig JJ, Dominguez MH. Decision by division: making cortical maps. Trends Neurosci 2009; 32: 291-301.
75. Behar TN, Dugich-Djordjevic MM, Li YX, Ma W, Somogyi R, Wen X, Brown E, Scott C, McKay RD, Barker JL. Neurotrophins stimulate chemotaxis of embryonic cortical neurons. Eur J Neurosci 1997; 9: 2561-2570.
76. Borghesani PR, Peyrin JM, Klein R, Rubin J, Carter AR, Schwartz PM, Luster A, Corfas G, Segal RA. Bdnf stimulates migration of cerebellar granule cells. Development 2002; 129: 1435-1442.
77. Williams GR. Neurodevelopmental and neurophysiological actions of thyroid hormone. J Neuroendocrinol 2008; 20: 784-794.
78. Sinha RA, Pathak A, Kumar A, Tiwari M, Shrivastava A, Godbole MM. Enhanced neuronal loss under perinatal hypothyroidism involves impaired neurotrophic signaling and increased proteolysis of p75(NTR). Mol Cell Neurosci 2009; 40: 354-364.
79. Martinez-Galan JR, Escobar del Rey F, Morreale de Escobar G, Santacana M, Ruiz-Marcos A. Hypothyroidism alters the development of radial glial cells in the term fetal and postnatal neocortex of the rat. Brain Res Dev Brain Res 2004; 153: 109-114.
80. Navarro D, Alvarado M, Morte B, Berbel D, Sesma J, Pacheco P, Morreale de Escobar G, Bernal J, Berbel P. Late maternal hypothyroidism alters the expression of Camk4 in neocortical subplate neurons: a comparison with Nurr1 labeling. Cereb Cortex 2013; May 24. [Epub ahead of print].
81. Saegusa Y, Woo GH, Fujimoto H, Inoue K, Takahashi M, Hirose M, Igarashi K, Kanno J, Mitsumori K, Nishikawa A, Shibutani M. Gene expression profiling and cellular distribution of molecules with altered expression in the hippocampal CA1 region after developmental exposure to anti-thyroid agents in rats. J Vet Med Sci 2010; 72: 187-195.
82. Saegusa Y, Woo GH, Fujimoto H, Kemmochi S, Shimamoto K, Hirose M, Mitsumori K, Nishikawa A, Shibutani M. Sustained production of Reelin-expressing interneurons in the hippocampal dentate hilus after developmental exposure to anti-thyroid agents in rats. Reprod Toxicol 2010; 29: 407-414.
83. Bastian TW, Prohaska JR, Georgieff MK, Anderson GW. Perinatal iron and copper deficiencies alter neonatal rat circulating and brain thyroid hormone concentrations. Endocrinology 2010; 151: 4055-4065.
84. Kobayashi K, Akune H, Sumida K, Saito K, Yoshioka T, Tsuji R. Perinatal exposure to PTU decreases expression of Arc, Homer 1, Egr 1 and Kcna 1 in the rat cerebral cortex and hippocampus. Brain Res 2009; 1264: 24-32.
85. Babu S, Sinha RA, Mohan V, Rao G, Pal A, Pathak A, Singh M, Godbole MM. Effect of hypothyroxinemia on thyroid hormone responsiveness and action during rat postnatal neocortical development. Exp Neurol 2011; 228: 91-98.
86. Coen L, Le Blay K, Rowe I, Demeneix BA. Caspase-9 regulates apoptosis/proliferation balance during metamorphic brain remodeling in Xenopus. Proc Natl Acad Sci USA 2007; 104: 8502-8507.
87. Rowe I, Le Blay K, Du Pasquier D, Palmier K, Levi G, Demeneix B, Coen L. Apoptosis of tail muscle during amphibian metamorphosis involves a caspase 9-dependent mechanism. Dev Dyn 2005; 233: 76-87.
88. Dong J, Wang Y, Wang Y, Wei W, Min H, Song B, Xi Q, Teng W, Chen J. Iodine deficiency increases apoptosis and decreases synaptotagmin-1 and PSD-95 in rat hippocampus. Nutr Neurosci 2013; 16: 135-141.
89. Wang Y, Zhong J, Xu H, Wei W, Dong J, Yu F, Wang Y, Gong J, Shan Z, Teng W, Chen J. Perinatal iodine deficiency and hypothyroidism increase cell apoptosis and alter doublecortin and reelin protein expressions in rat cerebellum. Arch Med Res 2012; 43: 255-264.
90. Sinha RA, Khare P, Rai A, Maurya SK, Pathak A, Mohan V, Nagar GK, Mudiam MK, Godbole MM, Bandyopadhyay S. Anti-apoptotic role of omega-3-fatty acids in developing brain: perinatal hypothyroid rat cerebellum as apoptotic model. Int J Dev Neurosci 2009; 27: 377-383.
91. Niquille M, Garel S, Mann F, Hornung JP, Otsmane B, Chevalley S, Parras C, Guillemot F, Gaspar P, Yanagawa Y, Lebrand C. Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol 2009; 7: e1000230.
92. Shu T, Li Y, Keller A, Richards LJ. The glial sling is a migratory population of developing neurons. Development 2003; 130: 2929-2937.
93. Riederer BM, Berbel P, Innocenti GM. Neurons in the corpus callosum of the cat during postnatal development. Eur J Neurosci 2004; 19: 2039-2046.
94. Ren T, Anderson A, Shen WB, Huang H, Plachez C, Zhang J, Mori S, Kinsman SL, Richards LJ. Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat Rec A Discov Mol Cell Evol Biol 2006; 288: 191-204.
95. Le Magueresse C, Alfonso J, Bark C, Eliava M, Khrulev S, Monyer H. Subventricular zone-derived neuroblasts use vasculature as a scaffold to migrate radially to the cortex in neonatal mice. Cereb Cortex 2012; 22: 2285-2296.
96. Zhang L, Cooper-Kuhn CM, Nannmark U, Blomgren K, Kuhn HG. Stimulatory effects of thyroid hormone on brain angiogenesis in vivo and in vitro. J Cereb Blood Flow Metab 2010; 30: 323-335.
97. Gilbert ME, Rovet J, Chen Z, Koibuchi N. Developmental thyroid hormone disruption: prevalence, environmental contaminants and neurodevelopmental consequences. Neurotoxicology 2012; 33: 842-852.
98. Gilbert ME, Sui L. Developmental exposure to perchlorate alters synaptic transmission in hippocampus of the adult rat. Environ Health Perspect 2008; 116: 752-760.
99. Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Is neuropsychological development related to maternal hypothyroidism or to maternal hypothyroxinemia? J Clin Endocrinol Metab 2000; 85: 3975-3987.
100. Zoeller RT, Rovet J. Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J Neuroendocrinol 2004; 16: 809-818.