Alterations of neocortical development and maturation in autism: Insight from valproic acid exposure and animal models of autism

Neurotoxicology and Teratology

Volumn 36, Issue , 2013, Pages 57-66

  Chomiak, Taylor ^a   Hu, Bin ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Autism; Development; Neocortex; Neuron; Overgrowth; Valproic acid

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; SEROTONIN; VALPROIC ACID;

ARTICLE; AUTISM; BRAIN MALFORMATION; BRAIN MATURATION; CELL COMMUNICATION; CELL COUNT; CELL MATURATION; CELL TYPE; COLUMNAR EPITHELIUM; DEVELOPMENTAL DISORDER; HUMAN; HYPERDOPAMINERGIA; HYPERSEROTONEMIA; METABOLIC DISORDER; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NEUROPATHOLOGY; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; SEROTONIN BLOOD LEVEL; SEROTONIN SYNDROME; THALAMUS INTRALAMINAR NUCLEUS;

ANIMALS; AUTISTIC DISORDER; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHILD; DISEASE MODELS, ANIMAL; HUMANS; VALPROIC ACID;

ANIMALIA;

EID: 84875673487     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2012.08.005     Document Type: Article

References (231)

1. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 2008, 9:341-355.
2. Abramson R.K., Wright H.H., Carpenter R., Brennan W., Lumpuy O., Cole E., et al. Elevated blood serotonin in autistic probands and their first-degree relatives. J Autism Dev Disord 1989, 19:397-407.
3. Abrous D.N., Koehl M., Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005, 85:523-569.
4. Adolphs R. The neurobiology of social cognition. Curr Opin Neurobiol 2001, 11:231-239.
5. Aitken A.R., Tork I. Early development of serotonin-containing neurons and pathways as seen in wholemount preparations of the fetal rat brain. J Comp Neurol 1988, 274:32-47.
6. Akhtar M.W., Raingo J., Nelson E.D., Montgomery R.L., Olson E.N., Kavalali E.T., et al. Histone deacetylases 1 and 2 form a developmental switch that controls excitatory synapse maturation and function. J Neurosci 2009, 29:8288-8297.
7. Amaral D. The anatomical organization of the central nervous system. Principles of neural science 2000, 317-336. McGraw-Hill, New York. E. Kandel, J. Schwartz, T. Jessell (Eds.).
8. Amaral D.G., Schumann C.M., Nordahl C.W. Neuroanatomy of autism. Trends Neurosci 2008, 31:137-145.
9. Ameis S.H., Fan J., Rockel C., Voineskos A.N., Lobaugh N.J., Soorya L., et al. Impaired structural connectivity of socio-emotional circuits in autism spectrum disorders: a diffusion tensor imaging study. PLoS One 2011, 6:e28044.
10. Anderson G.M., Freedman D.X., Cohen D.J., Volkmar F.R., Hoder E.L., McPhedran P., et al. Whole blood serotonin in autistic and normal subjects. J Child Psychol Psychiatry 1987, 28:885-900.
11. Anderson S.W., Damasio H., Jones R.D., Tranel D. Wisconsin card sorting test performance as a measure of frontal lobe damage. J Clin Exp Neuropsychol 1991, 13:909-922.
12. Anderson J.S., Druzgal T.J., Froehlich A., DuBray M.B., Lange N., Alexander A.L., et al. Decreased interhemispheric functional connectivity in autism. Cereb Cortex 2010, 21:1134-1146.
13. Arndt T.L., Stodgell C.J., Rodier P.M. The teratology of autism. Int J Dev Neurosci 2005, 23:189-199.
14. Austin L.S., Lydiard R.B., Ballenger J.C., Cohen B.M., Laraia M.T., Zealberg J.J., et al. Dopamine blocking activity of clomipramine in patients with obsessive-compulsive disorder. Biol Psychiatry 1991, 30:225-232.
15. Azmitia E.C., Singh J.S., Whitaker-Azmitia P.M. Increased serotonin axons (immunoreactive to 5-ht transporter) in postmortem brains from young autism donors. Neuropharmacology 2011, 60:1347-1354.
16. Bacci A., Huguenard J.R., Prince D.A. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 2004, 431:312-316.
17. Bailey A., Luthert P., Dean A., Harding B., Janota I., Montgomery M., et al. A clinicopathological study of autism. Brain 1998, 121(Pt 5):889-905.
18. Balasubramaniyan V., Boddeke E., Bakels R., Kust B., Kooistra S., Veneman A., et al. Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells. Neuroscience 2006, 143:939-951.
19. Bambini-Junior V., Rodrigues L., Behr G.A., Moreira J.C., Riesgo R., Gottfried C. Animal model of autism induced by prenatal exposure to valproate: behavioral changes and liver parameters. Brain Res 2011, 1408:8-16.
20. Bannister A.P. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci Res 2005, 53:95-103.
21. Bao S., Chan V.T., Merzenich M.M. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 2001, 412:79-83.
22. Bauman M.L., Kemper T.L. Structural brain anatomy in autism: what is the evidence. The neurobiology of autism 2005, 121-135. The Johns Hopkins University Press, Baltimore. M.L. Bauman, T.L. Kemper (Eds.).
23. Belmonte M.K., Allen G., Beckel-Mitchener A., Boulanger L.M., Carper R.A., Webb S.J. Autism and abnormal development of brain connectivity. J Neurosci 2004, 24:9228-9231.
24. Belzung C., Leman S., Vourc'h P., Andres C. Rodent models for autism: a critical review. Drug Discov Today Dis Models 2005, 2:93-101.
25. Ben Bashat D., Kronfeld-Duenias V., Zachor D.A., Ekstein P.M., Hendler T., Tarrasch R., et al. Accelerated maturation of white matter in young children with autism: a high b value DWI study. Neuroimage 2007, 37:40-47.
26. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 2002, 3:728-739.
27. Bennett G.D., Wlodarczyk B., Calvin J.A., Craig J.C., Finnell R.H. Valproic acid-induced alterations in growth and neurotrophic factor gene expression in murine embryos [corrected]. Reprod Toxicol 2000, 14:1-11.
28. Berger B., Verney C., Gaspar P., Febvret A. Transient expression of tyrosine hydroxylase immunoreactivity in some neurons of the rat neocortex during postnatal development. Brain Res 1985, 355:141-144.
29. Bernier P.J., Parent A. Bcl-2 protein as a marker of neuronal immaturity in postnatal primate brain. J Neurosci 1998, 18:2486-2497.
30. Betancourt A.M., Filipov N.M., Carr R.L. Alteration of neurotrophins in the hippocampus and cerebral cortex of young rats exposed to chlorpyrifos and methyl parathion. Toxicol Sci 2007, 100:445-455.
31. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy: too much of a good thing?. Trends Neurosci 2001, 24:47-53.
32. Binkerd P.E., Rowland J.M., Nau H., Hendrickx A.G. Evaluation of valproic acid (vpa) developmental toxicity and pharmacokinetics in Sprague-Dawley rats. Fundam Appl Toxicol 1988, 11:485-493.
33. Brodmann K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues 1909, Johann Ambrosius Barth Verlag, Leipzig.
34. Bryson S.E. The autistic mind. The neurobiology of autism 2005, 34-44. The Johns Hopkins University Press, Baltimore, Maryland. M.L. Bauman, T.L. Kemper (Eds.).
35. Buxhoeveden D.P., Semendeferi K., Buckwalter J., Schenker N., Switzer R., Courchesne E. Reduced minicolumns in the frontal cortex of patients with autism. Neuropathol Appl Neurobiol 2006, 32:483-491.
36. Cancedda L., Fiumelli H., Chen K., Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 2007, 27:5224-5235.
37. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 2003, 6:507-518.
38. Casanova M.F., Buxhoeveden D.P., Switala A.E., Roy E. Minicolumnar pathology in autism. Neurology 2002, 58:428-432.
39. Casanova M.F., van Kooten I.A., Switala A.E., van Engeland H., Heinsen H., Steinbusch H.W., et al. Minicolumnar abnormalities in autism. Acta Neuropathol 2006, 112:287-303.
40. Cases O., Vitalis T., Seif I., De Maeyer E., Sotelo C., Gaspar P. Lack of barrels in the somatosensory cortex of monoamine oxidase a-deficient mice: role of a serotonin excess during the critical period. Neuron 1996, 16:297-307.
41. Cauli B., Audinat E., Lambolez B., Angulo M.C., Ropert N., Tsuzuki K., et al. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 1997, 17:3894-3906.
42. Chomiak T., Peters S., Hu B. Functional architecture and spike timing properties of corticofugal projections from rat ventral temporal cortex. J Neurophysiol 2008, 100:327-335.
43. Chomiak T., Karnik V., Block E., Hu B. Altering the trajectory of early postnatal cortical development can lead to structural and behavioural features of autism. BMC Neurosci 2010, 11:102.
44. Christianson A.L., Chesler N., Kromberg J.G. Fetal valproate syndrome: clinical and neuro-developmental features in two sibling pairs. Dev Med Child Neurol 1994, 36:361-369.
45. Chubakov A.R., Gromova E.A., Konovalov G.V., Sarkisova E.F., Chumasov E.I. The effects of serotonin on the morpho-functional development of rat cerebral neocortex in tissue culture. Brain Res 1986, 369:285-297.
46. Chugani D.C., Muzik O., Rothermel R., Behen M., Chakraborty P., Mangner T., et al. Altered serotonin synthesis in the dentatothalamocortical pathway in autistic boys. Ann Neurol 1997, 42:666-669.
47. Chugani D.C., Muzik O., Behen M., Rothermel R., Janisse J.J., Lee J., et al. Developmental changes in brain serotonin synthesis capacity in autistic and nonautistic children. Ann Neurol 1999, 45:287-295.
48. Courchesne E., Carper R., Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. JAMA 2003, 290:337-344.
49. Courchesne E., Pierce K., Schumann C.M., Redcay E., Buckwalter J.A., Kennedy D.P., et al. Mapping early brain development in autism. Neuron 2007, 56:399-413.
50. Courchesne E., Mouton P.R., Calhoun M.E., Semendeferi K., Ahrens-Barbeau C., Hallet M.J., et al. Neuron number and size in prefrontal cortex of children with autism. JAMA 2011, 306:2001-2010.
51. Cruikshank S.J., Rose H.J., Metherate R. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 2002, 87:361-384.
52. Cruikshank S.J., Lewis T.J., Connors B.W. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 2007, 10:462-468.
53. De Keyser J., Ebinger G., Vauquelin G. Evidence for a widespread dopaminergic innervation of the human cerebral neocortex. Neurosci Lett 1989, 104:281-285.
54. Decker M.J., Rye D.B. Neonatal intermittent hypoxia impairs dopamine signaling and executive functioning. Sleep Breath 2002, 6:205-210.
55. DeFelipe J. Cortical interneurons: from Cajal to 2001. Prog Brain Res 2002, 136:215-238.
56. Descarries L., Lemay B., Doucet G., Berger B. Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 1987, 21:807-824.
57. Dinstein I., Pierce K., Eyler L., Solso S., Malach R., Behrmann M., et al. Disrupted neural synchronization in toddlers with autism. Neuron 2011, 70:1218-1225.
58. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997, 17:5046-5061.
59. Doyle C.A., McDougle C.J. Pharmacotherapy to control behavioral symptoms in children with autism. Expert Opin Pharmacother 2012, 13:1615-1629.
60. Dufour-Rainfray D., Vourc'h P., Le Guisquet A.M., Garreau L., Ternant D., Bodard S., et al. Behavior and serotonergic disorders in rats exposed prenatally to valproate: a model for autism. Neurosci Lett 2010, 470:55-59.
61. Elman J.L. Learning and development in neural networks: the importance of starting small. Cognition 1993, 48:71-99.
62. Friedman W.J., Olson L., Persson H. Cells that express brain-derived neurotrophic factor mRNA in the developing postnatal rat brain. Eur J Neurosci 1991, 3:688-697.
63. Fukuchi M., Nii T., Ishimaru N., Minamino A., Hara D., Takasaki I., et al. Valproic acid induces up- or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neurosci Res 2009, 65:35-43.
64. Gao W., Lin W., Chen Y., Gerig G., Smith J.K., Jewells V., et al. Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol 2009, 30:290-296.
65. Gaspar P., Berger B., Febvret A., Vigny A., Krieger-Poulet M., Borri-Voltattorni C. Tyrosine hydroxylase-immunoreactive neurons in the human cerebral cortex: a novel catecholaminergic group?. Neurosci Lett 1987, 80:257-262.
66. Geier C.F., Garver K., Terwilliger R., Luna B. Development of working memory maintenance. J Neurophysiol 2009, 101:84-99.
67. Geurts H.M., Corbett B., Solomon M. The paradox of cognitive flexibility in autism. Trends Cogn Sci 2009, 13:74-82.
68. Gillberg C., Svennerholm L. CSF monoamines in autistic syndromes and other pervasive developmental disorders of early childhood. Br J Psychiatry 1987, 151:89-94.
69. Glasson E.J., Bower C., Petterson B., de Klerk N., Chaney G., Hallmayer J.F. Perinatal factors and the development of autism: a population study. Arch Gen Psychiatry 2004, 61:618-627.
70. Golarai G., Ghahremani D.G., Whitfield-Gabrieli S., Reiss A., Eberhardt J.L., Gabrieli J.D., et al. Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat Neurosci 2007, 10:512-522.
71. Gonchar Y., Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 1997, 7:347-358.
72. Goodman C.S., Spitzer N.C. The development of electrical properties of identified neurones in grasshopper embryos. J Physiol 1981, 313:385-403.
73. Goodman C.S., Pearson K.G., Spitzer N.C. Electrical excitability: a spectrum of properties in the progeny of a single embryonic neuroblast. Proc Natl Acad Sci U S A 1980, 77:1676-1680.
74. Gould E., Reeves A.J., Graziano M.S., Gross C.G. Neurogenesis in the neocortex of adult primates. Science 1999, 286:548-552.
75. Halabisky B., Shen F., Huguenard J.R., Prince D.A. Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 2006, 96:834-845.
76. Haug T., Storm J.F. Protein kinase a mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. J Neurophysiol 2000, 83:2071-2079.
77. Hazlett H.C., Poe M.D., Gerig G., Styner M., Chappell C., Smith R.G., et al. Early brain overgrowth in autism associated with an increase in cortical surface area before age 2years. Arch Gen Psychiatry 2011, 68:467-476.
78. Hefti B.J., Smith P.H. Anatomy, physiology, and synaptic responses of rat layer v auditory cortical cells and effects of intracellular GABA(a) blockade. J Neurophysiol 2000, 83:2626-2638.
79. Hisada M. The paraneuronal nature of neurons: nonspiking communication in the crayfish central nervous system. Arch Histol Cytol 1989, 52:139-146. [Suppl.].
80. Hishida R., Kamatani D., Kitaura H., Kudoh M., Shibuki K. Functional local connections with differential activity-dependence and critical periods surrounding the primary auditory cortex in rat cerebral slices. Neuroimage 2007, 34:679-693.
81. Hong S., Ke X., Tang T., Hang Y., Chu K., Huang H., et al. Detecting abnormalities of corpus callosum connectivity in autism using magnetic resonance imaging and diffusion tensor tractography. Psychiatry Res 2011, 194:333-339.
82. Horch H.W., Katz L.C. Bdnf release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 2002, 5:1177-1184.
83. Horton J.C., Adams D.L. The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci 2005, 360:837-862.
84. Hsieh J., Gage F.H. Epigenetic control of neural stem cell fate. Curr Opin Genet Dev 2004, 14:461-469.
85. Hsieh J., Gage F.H. Chromatin remodeling in neural development and plasticity. Curr Opin Cell Biol 2005, 17:664-671.
86. Hsieh J., Nakashima K., Kuwabara T., Mejia E., Gage F.H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 2004, 101:16659-16664.
87. Hubel D.H., Wiesel T.N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J Neurophysiol 1965, 28:229-289.
88. Hubel D.H., Wiesel T.N. Receptive fields and functional architecture of monkey striate cortex. J Physiol 1968, 195:215-243.
89. Hultman C.M., Sparen P., Cnattingius S. Perinatal risk factors for infantile autism. Epidemiology 2002, 13:417-423.
90. Ingalhalikar M., Parker D., Bloy L., Roberts T.P., Verma R. Diffusion based abnormality markers of pathology: toward learned diagnostic prediction of ASD. Neuroimage 2011, 57:918-927.
91. Jacobs F.M., van Erp S., van der Linden A.J., von Oerthel L., Burbach J.P., Smidt M.P. Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 2009, 136:531-540.
92. Jacot-Descombes S., Uppal N., Wicinski B., Santos M., Schmeidler J., Giannakopoulos P., et al. Decreased pyramidal neuron size in brodmann areas 44 and 45 in patients with autism. Acta Neuropathol 2012, 124:67-69.
93. Janusonis S., Gluncic V., Rakic P. Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 2004, 24:1652-1659.
94. Jeong M.R., Hashimoto R., Senatorov V.V., Fujimaki K., Ren M., Lee M.S., et al. Valproic acid, a mood stabilizer and anticonvulsant, protects rat cerebral cortical neurons from spontaneous cell death: a role of histone deacetylase inhibition. FEBS Lett 2003, 542:74-78.
95. Jou R.J., Jackowski A.P., Papademetris X., Rajeevan N., Staib L.H., Volkmar F.R. Diffusion tensor imaging in autism spectrum disorders: preliminary evidence of abnormal neural connectivity. Aust N Z J Psychiatry 2011, 45:153-162.
96. Kageyama R., Nakanishi S. Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr Opin Genet Dev 1997, 7:659-665.
97. Kahne D., Tudorica A., Borella A., Shapiro L., Johnstone F., Huang W., et al. Behavioral and magnetic resonance spectroscopic studies in the rat hyperserotonemic model of autism. Physiol Behav 2002, 75:403-410.
98. Kaisho Y., Shintani A., Ono Y., Kato K., Igarashi K. Regional expression of the nerve growth factor gene family in rat brain during development. Biochem Biophys Res Commun 1991, 174:379-385.
99. Kanner L. Autistic disturbances of affective contact. Nerv Child 1943, 2:217-250.
100. Karege F., Schwald M., Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett 2002, 328:261-264.
101. Kasper E.M., Larkman A.U., Lubke J., Blakemore C. Pyramidal neurons in layer 5 of the rat visual cortex. II. Development of electrophysiological properties. J Comp Neurol 1994, 339:475-494.
102. Keller T.A., Kana R.K., Just M.A. A developmental study of the structural integrity of white matter in autism. Neuroreport 2007, 18:23-27.
103. Kemper T.L., Bauman M.L. The contribution of neuropathologic studies to the understanding of autism. Neurol Clin 1993, 11:175-187.
104. Kemper T.L., Bauman M. Neuropathology of infantile autism. J Neuropathol Exp Neurol 1998, 57:645-652.
105. Kim K.C., Kim P., Go H.S., Choi C.S., Yang S.I., Cheong J.H., et al. The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol Lett 2011, 201:137-142.
106. King B.H., Hollander E., Sikich L., McCracken J.T., Scahill L., Bregman J.D., et al. Lack of efficacy of citalopram in children with autism spectrum disorders and high levels of repetitive behavior: citalopram ineffective in children with autism. Arch Gen Psychiatry 2009, 66:583-590.
107. Knudsen E.I., Heckman J.J., Cameron J.L., Shonkoff J.P. Economic, neurobiological, and behavioral perspectives on building America's future workforce. Proc Natl Acad Sci U S A 2006, 103:10155-10162.
108. Koketsu D., Mikami A., Miyamoto Y., Hisatsune T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 2003, 23:937-942.
109. Kornack D.R., Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 2001, 294:2127-2130.
110. Kourtzi Z., Augath M., Logothetis N.K., Movshon J.A., Kiorpes L. Development of visually evoked cortical activity in infant macaque monkeys studied longitudinally with fMRI. Magn Reson Imaging 2006, 24:359-366.
111. Kramer O.H., Zhu P., Ostendorff H.P., Golebiewski M., Tiefenbach J., Peters M.A., et al. The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J 2003, 22:3411-3420.
112. Kumar M., Kim S., Pickup S., Chen R., Fairless A.H., Ittyerah R., et al. Longitudinal in-vivo diffusion tensor imaging for assessing brain developmental changes in BALB/cJ mice, a model of reduced sociability relevant to autism. Brain Res 2012, 1455:56-67.
113. Kuwagata M., Ogawa T., Shioda S., Nagata T. Observation of fetal brain in a rat valproate-induced autism model: a developmental neurotoxicity study. Int J Dev Neurosci 2009, 27:399-405.
114. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., et al. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
115. Landrigan P.J. What causes autism? Exploring the environmental contribution. Curr Opin Pediatr 2010, 22:219-225.
116. Lauder J.M. Ontogeny of the serotonergic system in the rat: serotonin as a developmental signal. Ann N Y Acad Sci 1990, 600:297-313. [discussion 314].
117. Leboyer M., Philippe A., Bouvard M., Guilloud-Bataille M., Bondoux D., Tabuteau F., et al. Whole blood serotonin and plasma beta-endorphin in autistic probands and their first-degree relatives. Biol Psychiatry 1999, 45:158-163.
118. Lee J.E. Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol 1997, 7:13-20.
119. Lee S.H., Cox C.L. Excitatory actions of vasoactive intestinal peptide on mouse thalamocortical neurons are mediated by VPAC2 receptors. J Neurophysiol 2006, 96:858-871.
120. Lee J.E., Hollenberg S.M., Snider L., Turner D.L., Lipnick N., Weintraub H. Conversion of xenopus ectoderm into neurons by neurod, a basic helix-loop-helix protein. Science 1995, 268:836-844.
121. Lee J.E., Bigler E.D., Alexander A.L., Lazar M., DuBray M.B., Chung M.K., et al. Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett 2007, 424:127-132.
122. Leng J., Jiang L., Chen H., Zhang X. Brain-derived neurotrophic factor and electrophysiological properties of voltage-gated ion channels during neuronal stem cell development. Brain Res 2009, 1272:14-24.
123. Lewis J.D., Elman J.L. Growth-related neural reorganization and the autism phenotype: a test of the hypothesis that altered brain growth leads to altered connectivity. Dev Sci 2008, 11:135-155.
124. Lewis M., Kim S.J. The pathophysiology of restricted repetitive behavior. J Neurodev Disord 2009, 1:114-132.
125. Lewis M.H., Tanimura Y., Lee L.W., Bodfish J.W. Animal models of restricted repetitive behavior in autism. Behav Brain Res 2007, 176:66-74.
126. Liu Z., Richmond B.J., Murray E.A., Saunders R.C., Steenrod S., Stubblefield B.K., et al. DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward. Proc Natl Acad Sci U S A 2004, 101:12336-12341.
127. Llinas R.R., Leznik E., Urbano F.J. Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci U S A 2002, 99:449-454.
128. Luna B., Garver K.E., Urban T.A., Lazar N.A., Sweeney J.A. Maturation of cognitive processes from late childhood to adulthood. Child Dev 2004, 75:1357-1372.
129. Lund J.S. Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). J Comp Neurol 1973, 147:455-496.
130. Maes J.H., Eling P.A., Wezenberg E., Vissers C.T., Kan C.C. Attentional set shifting in autism spectrum disorder: differentiating between the role of perseveration, learned irrelevance, and novelty processing. J Clin Exp Neuropsychol 2011, 33:210-217.
131. Maisonpierre P.C., Belluscio L., Friedman B., Alderson R.F., Wiegand S.J., Furth M.E., et al. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 1990, 5:501-509.
132. Makkonen I., Riikonen R., Kokki H., Airaksinen M.M., Kuikka J.T. Serotonin and dopamine transporter binding in children with autism determined by SPECT. Dev Med Child Neurol 2008, 50:593-597.
133. Markram H., Rinaldi T., Markram K. The intense world syndrome - an alternative hypothesis for autism. Front Neurosci 2007, 1:77-96.
134. Markram K., Rinaldi T., La Mendola D., Sandi C., Markram H. Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 2008, 33:901-912.
135. McAllister A.K., Lo D.C., Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 1995, 15:791-803.
136. McBride P.A., Anderson G.M., Hertzig M.E., Snow M.E., Thompson S.M., Khait V.D., et al. Effects of diagnosis, race, and puberty on platelet serotonin levels in autism and mental retardation. J Am Acad Child Adolesc Psychiatry 1998, 37:767-776.
137. McCormick D.A., Prince D.A. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol 1987, 393:743-762.
138. McDougle C.J., Kresch L.E., Posey D.J. Repetitive thoughts and behavior in pervasive developmental disorders: treatment with serotonin reuptake inhibitors. J Autism Dev Disord 2000, 30:427-435.
139. Meis S., Munsch T., Sosulina L., Pape H.C. Postsynaptic mechanisms underlying responsiveness of amygdaloid neurons to cholecystokinin are mediated by a transient receptor potential-like current. Mol Cell Neurosci 2007, 35:356-367.
140. Minshew N.J., Williams D.L. The new neurobiology of autism: cortex, connectivity, and neuronal organization. Arch Neurol 2007, 64:945-950.
141. Miyazaki K., Narita N., Sakuta R., Miyahara T., Naruse H., Okado N., et al. Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Brain Dev 2004, 26:292-295.
142. Miyazaki K., Narita N., Narita M. Maternal administration of thalidomide or valproic acid causes abnormal serotonergic neurons in the offspring: implication for pathogenesis of autism. Int J Dev Neurosci 2005, 23:287-297.
143. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 2007, 8:427-437.
144. Monti B., Polazzi E., Contestabile A. Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection. Curr Mol Pharmacol 2009, 2:95-109.
145. Moore S.J., Turnpenny P., Quinn A., Glover S., Lloyd D.J., Montgomery T., et al. A clinical study of 57 children with fetal anticonvulsant syndromes. J Med Genet 2000, 37:489-497.
146. Mountcastle V.B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 1957, 20:408-434.
147. Murphy D.G., Daly E., Schmitz N., Toal F., Murphy K., Curran S., et al. Cortical serotonin 5-HT2A receptor binding and social communication in adults with Asperger's syndrome: an in vivo SPECT study. Am J Psychiatry 2006, 163:934-936.
148. Nagae L.M., Zarnow D.M., Blaskey L., Dell J., Khan S.Y., Qasmieh S., et al. Elevated mean diffusivity in the left hemisphere superior longitudinal fasciculus in autism spectrum disorders increases with more profound language impairment. AJNR Am J Neuroradiol 2012.
149. Nakamura K., Sekine Y., Ouchi Y., Tsujii M., Yoshikawa E., Futatsubashi M., et al. Brain serotonin and dopamine transporter bindings in adults with high-functioning autism. Arch Gen Psychiatry 2010, 67:59-68.
150. Narayan M., Srinath S., Anderson G.M., Meundi D.B. Cerebrospinal fluid levels of homovanillic acid and 5-hydroxyindoleacetic acid in autism. Biol Psychiatry 1993, 33:630-635.
151. Narita N., Kato M., Tazoe M., Miyazaki K., Narita M., Okado N. Increased monoamine concentration in the brain and blood of fetal thalidomide- and valproic acid-exposed rat: putative animal models for autism. Pediatr Res 2002, 52:576-579.
152. Nelson K.B., Grether J.K., Croen L.A., Dambrosia J.M., Dickens B.F., Jelliffe L.L., et al. Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Ann Neurol 2001, 49:597-606.
153. Nesaratnam N., Dunham J.S., Gabbott P.L., Mason S., Schmitz C., Rezaie P. A quantitative analysis of synaptophysin immunoreactivity within the cerebral cortex in autism. Neuropathol Appl Neurobiol 2011, 37(Suppl. 1):22-23.
154. Nieuwenhuys R. The neocortex: an overview of its evolutionary development, structural organization and synaptology. Anat Embryol 1994, 190:307-337.
155. Notle J. The human brain: an introduction to its functional anatomy 2002, Mosby, St. Louis. 5th ed.
156. Oblak A.L., Rosene D.L., Kemper T.L., Bauman M.L., Blatt G.J. Altered posterior cingulate cortical cyctoarchitecture, but normal density of neurons and interneurons in the posterior cingulate cortex and fusiform gyrus in autism. Autism Res 2011, 4:200-211.
157. Ogawa H., Kuwagata M., Shioda S. The search for a fetal origin for autism: evidence of aberrant brain development in a rat model of autism produced by prenatal exposure to valproate. Transmitters and modulators in disease: new frontiers in neuroscience 2009, 83-88. Springer, Tokyo. S. Shioda, I. Homma, N. Kato (Eds.).
158. O'Hearn E., Molliver M.E. Organization of raphe-cortical projections in rat: a quantitative retrograde study. Brain Res Bull 1984, 13:709-726.
159. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat Rev Neurosci 2002, 3:715-727.
160. Oz M. Receptor-independent actions of cannabinoids on cell membranes: focus on endocannabinoids. Pharmacol Ther 2006, 111:114-144.
161. Parnas D., Linial M. Acceleration of neuronal maturation of P19 cells by increasing culture density. Brain Res Dev Brain Res 1997, 101:115-124.
162. Parnavelas J.G. The origin and migration of cortical neurones: new vistas. Trends Neurosci 2000, 23:126-131.
163. Parnavelas J.G., Lieberman A.R., Webster K.E. Organization of neurons in the visual cortex, area 17, of the rat. J Anat 1977, 124:305-322.
164. Paus T., Toro R. Could sex differences in white matter be explained by g ratio?. Front Neuroanat 2009, 3:14.
165. Pellegri G., Magistretti P.J., Martin J.L. VIP and PACAP potentiate the action of glutamate on BDNF expression in mouse cortical neurones. Eur J Neurosci 1998, 10:272-280.
166. Phiel C.J., Zhang F., Huang E.Y., Guenther M.G., Lazar M.A., Klein P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 2001, 276:36734-36741.
167. Picken Bahrey H.L., Moody W.J. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol 2003, 89:1761-1773.
168. Poljac E., Simon S., Ringlever L., Kalcik D., Groen W.B., Buitelaar J.K., et al. Impaired task switching performance in children with dyslexia but not in children with autism. Q J Exp Psychol (Hove) 2010, 63:401-416.
169. Posey D.J., Stigler K.A., Erickson C.A., McDougle C.J. Antipsychotics in the treatment of autism. J Clin Invest 2008, 118:6-14.
170. Previc F.H. Prenatal influences on brain dopamine and their relevance to the rising incidence of autism. Med Hypotheses 2007, 68:46-60.
171. Quartz S.R. The constructivist brain. Trends Cogn Sci 1999, 3:48-57.
172. Quartz S.R., Sejnowski T.J. The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 1997, 20:537-556. [discussion 556-96].
173. Rakic P. Neuroscience. No more cortical neurons for you. Science 2006, 313:928-929.
174. Rasalam A.D., Hailey H., Williams J.H., Moore S.J., Turnpenny P.D., Lloyd D.J., et al. Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev Med Child Neurol 2005, 47:551-555.
175. Reinoso B.S., Undie A.S., Levitt P. Dopamine receptors mediate differential morphological effects on cerebral cortical neurons in vitro. J Neurosci Res 1996, 43:439-453.
176. Represa A., Ben-Ari Y. Trophic actions of GABA on neuronal development. Trends Neurosci 2005, 28:278-283.
177. Reynolds S., Millette A., Devine D.P. Sensory and motor characterization in the postnatal valproate rat model of autism. Dev Neurosci 2012, 34:258-267. [Epub].
178. Riccio O., Jacobshagen M., Golding B., Vutskits L., Jabaudon D., Hornung P., et al. Excess of serotonin affects neocortical pyramidal neuron migration. Transl Psychiatry 2011, 1:e47.
179. Rinaldi T., Kulangara K., Antoniello K., Markram H. Elevated nmda receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc Natl Acad Sci U S A 2007, 104:13501-13506.
180. Rinaldi T., Perrodin C., Markram H. Hyper-connectivity and hyper-plasticity in the medial prefrontal cortex in the valproic acid animal model of autism. Front Neural Circuits 2008, 2:4.
181. Ringstedt T., Linnarsson S., Wagner J., Lendahl U., Kokaia Z., Arenas E., et al. Bdnf regulates reelin expression and cajal-retzius cell development in the cerebral cortex. Neuron 1998, 21:305-315.
182. Ritvo E.R., Yuwiler A., Geller E., Ornitz E.M., Saeger K., Plotkin S. Increased blood serotonin and platelets in early infantile autism. Arch Gen Psychiatry 1970, 23:566-572.
183. Rockel A.J., Hiorns R.W., Powell T.P. The basic uniformity in structure of the neocortex. Brain 1980, 103:221-244.
184. Roullet F.I., Wollaston L., Decatanzaro D., Foster J.A. Behavioral and molecular changes in the mouse in response to prenatal exposure to the anti-epileptic drug valproic acid. Neuroscience 2010, 170:514-522.
185. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2003, 2:255-267.
186. Satoh J., Suzuki K. Tyrosine hydroxylase-immunoreactive neurons in the mouse cerebral cortex during the postnatal period. Brain Res Dev Brain Res 1990, 53:1-5.
187. Schain R.J., Freedman D.X. Studies on 5-hydroxyindole metabolism in autistic and other mentally retarded children. J Pediatr 1961, 58:315-320.
188. Scherf K.S., Behrmann M., Humphreys K., Luna B. Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Dev Sci 2007, 10:F15-F30.
189. Schneider T., Przewlocki R. Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 2005, 30:80-89.
190. Schneider T., Turczak J., Przewlocki R. Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 2006, 31:36-46.
191. Schneider T., Roman A., Basta-Kaim A., Kubera M., Budziszewska B., Schneider K., et al. Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid. Psychoneuroendocrinology 2008, 33:728-740.
192. Schumann C.M., Bloss C.S., Barnes C.C., Wideman G.M., Carper R.A., Akshoomoff N., et al. Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J Neurosci 2010, 30:4419-4427.
193. Schwab M.H., Druffel-Augustin S., Gass P., Jung M., Klugmann M., Bartholomae A., et al. Neuronal basic helix-loop-helix proteins (NEX, neuroD, NDRF): spatiotemporal expression and targeted disruption of the NEX gene in transgenic mice. J Neurosci 1998, 18:1408-1418.
194. Schwab M.H., Bartholomae A., Heimrich B., Feldmeyer D., Druffel-Augustin S., Goebbels S., et al. Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J Neurosci 2000, 20:3714-3724.
195. Seeman P., Weinshenker D., Quirion R., Srivastava L.K., Bhardwaj S.K., Grandy D.K., et al. Dopamine supersensitivity correlates with D2High states, implying many paths to psychosis. Proc Natl Acad Sci U S A 2005, 102:3513-3518.
196. Shaw P., Eckstrand K., Sharp W., Blumenthal J., Lerch J.P., Greenstein D., et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A 2007, 104:19649-19654.
197. Shukla D.K., Keehn B., Muller R.A. Tract-specific analyses of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. J Child Psychol Psychiatry 2011, 52:286-295.
198. Shukla D.K., Keehn B., Smylie D.M., Muller R.A. Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia 2011, 49:1378-1382.
199. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010, 11:490-502.
200. Simms M.L., Kemper T.L., Timbie C.M., Bauman M.L., Blatt G.J. The anterior cingulate cortex in autism: heterogeneity of qualitative and quantitative cytoarchitectonic features suggests possible subgroups. Acta Neuropathol 2009, 118:673-684.
201. Smiley J.F., Williams S.M., Szigeti K., Goldman-Rakic P.S. Light and electron microscopic characterization of dopamine-immunoreactive axons in human cerebral cortex. J Comp Neurol 1992, 321:325-335.
202. Spitzer N.C. Electrical activity in early neuronal development. Nature 2006, 444:707-712.
203. Takahashi S., Kanai H., Miyamoto Y. Reassessment of elevated serotonin levels in blood platelets in early infantile autism. J Autism Child Schizophr 1976, 6:317-326.
204. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 2003, 467:60-79.
205. Todd R.D. Neural development is regulated by classical neurotransmitters: dopamine D2 receptor stimulation enhances neurite outgrowth. Biol Psychiatry 1992, 31:794-807.
206. Tsai S.J. Is autism caused by early hyperactivity of brain-derived neurotrophic factor?. Med Hypotheses 2005, 65:79-82.
207. Tsujino N., Nakatani Y., Seki Y., Nakasato A., Nakamura M., Sugawara M., et al. Abnormality of circadian rhythm accompanied by an increase in frontal cortex serotonin in animal model of autism. Neurosci Res 2007, 57:289-295.
208. Tuchman R., Rapin I. Epilepsy in autism. Lancet Neurol 2002, 1:352-358.
209. Van Essen D.C. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997, 385:313-318.
210. van Kooten I.A., Palmen S.J., von Cappeln P., Steinbusch H.W., Korr H., Heinsen H., et al. Neurons in the fusiform gyrus are fewer and smaller in autism. Brain 2008, 131:987-999.
211. Veenstra-VanderWeele J., Muller C.L., Iwamoto H., Sauer J.E., Owens W.A., Shah C.R., et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci U S A 2012, 109:5469-5474.
212. Vitalis T., Cases O., Passemard S., Callebert J., Parnavelas J.G. Embryonic depletion of serotonin affects cortical development. Eur J Neurosci 2007, 26:331-344.
213. Vorhees C.V. Behavioral teratogenicity of valproic acid: selective effects on behavior after prenatal exposure to rats. Psychopharmacology (Berl) 1987, 92:173-179.
214. Vorhees C.V. Teratogenicity and developmental toxicity of valproic acid in rats. Teratology 1987, 35:195-202.
215. Wagner G.C., Reuhl K.R., Cheh M., McRae P., Halladay A.K. A new neurobehavioral model of autism in mice: pre- and postnatal exposure to sodium valproate. J Autism Dev Disord 2006, 36:779-793.
216. Waltereit R., Japs B., Schneider M., de Vries P.J., Bartsch D. Epilepsy and Tsc2 haploinsufficiency lead to autistic-like social deficit behaviors in rats. Behav Genet 2011, 41:364-372.
217. Wegiel J., Kuchna I., Nowicki K., Imaki H., Marchi E., Ma S.Y., et al. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol 2010, 119:755-770.
218. Whitaker-Azmitia P.M. Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism?. Int J Dev Neurosci 2005, 23:75-83.
219. White T., Su S., Schmidt M., Kao C.Y., Sapiro G. The development of gyrification in childhood and adolescence. Brain Cogn 2010, 72:36-45.
220. Williams P.G., Hersh J.H. A male with fetal valproate syndrome and autism. Dev Med Child Neurol 1997, 39:632-634.
221. Williams G., King J., Cunningham M., Stephan M., Kerr B., Hersh J.H. Fetal valproate syndrome and autism: additional evidence of an association. Dev Med Child Neurol 2001, 43:202-206.
222. Wing L. The history of ideas on autism: legends, myths and reality. Autism 1997, 1:13-23.
223. Wolff J.J., Gu H., Gerig G., Elison J.T., Styner M., Gouttard S., et al. Differences in white matter fiber tract development present from 6 to 24months in infants with autism. Am J Psychiatry 2012, 169:589-600.
224. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat Rev Neurosci 2006, 7:687-696.
225. Yasuda S., Liang M.H., Marinova Z., Yahyavi A., Chuang D.M. The mood stabilizers lithium and valproate selectively activate the promoter IV of brain-derived neurotrophic factor in neurons. Mol Psychiatry 2009, 14:51-59.
226. Yochum C.L., Dowling P., Reuhl K.R., Wagner G.C., Ming X. VPA-induced apoptosis and behavioral deficits in neonatal mice. Brain Res 2008, 1203:126-132.
227. Yochum C.L., Bhattacharya P., Patti L., Mirochnitchenko O., Wagner G.C. Animal model of autism using GSTM1 knockout mice and early post-natal sodium valproate treatment. Behav Brain Res 2010, 210:202-210.
228. Yuste R. Origin and classification of neocortical interneurons. Neuron 2005, 48:524-527.
229. Zhang Z.W. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol 2004, 91:1171-1182.
230. Zikopoulos B., Barbas H. Changes in prefrontal axons may disrupt the network in autism. J Neurosci 2010, 30:14595-14609.
231. Zwaigenbaum L., Bryson S., Rogers T., Roberts W., Brian J., Szatmari P. Behavioral manifestations of autism in the first year of life. Int J Dev Neurosci 2005, 23:143-152.