Skip to main content
SpringerLink
Log in

Autism spectrum disorder: neuropathology and animal models

  • Review
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Abstract

Autism spectrum disorder (ASD) has a major impact on the development and social integration of affected individuals and is the most heritable of psychiatric disorders. An increase in the incidence of ASD cases has prompted a surge in research efforts on the underlying neuropathologic processes. We present an overview of current findings in neuropathology studies of ASD using two investigational approaches, postmortem human brains and ASD animal models, and discuss the overlap, limitations, and significance of each. Postmortem examination of ASD brains has revealed global changes including disorganized gray and white matter, increased number of neurons, decreased volume of neuronal soma, and increased neuropil, the last reflecting changes in densities of dendritic spines, cerebral vasculature and glia. Both cortical and non-cortical areas show region-specific abnormalities in neuronal morphology and cytoarchitectural organization, with consistent findings reported from the prefrontal cortex, fusiform gyrus, frontoinsular cortex, cingulate cortex, hippocampus, amygdala, cerebellum and brainstem. The paucity of postmortem human studies linking neuropathology to the underlying etiology has been partly addressed using animal models to explore the impact of genetic and non-genetic factors clinically relevant for the ASD phenotype. Genetically modified models include those based on well-studied monogenic ASD genes (NLGN3, NLGN4, NRXN1, CNTNAP2, SHANK3, MECP2, FMR1, TSC1/2), emerging risk genes (CHD8, SCN2A, SYNGAP1, ARID1B, GRIN2B, DSCAM, TBR1), and copy number variants (15q11-q13 deletion, 15q13.3 microdeletion, 15q11-13 duplication, 16p11.2 deletion and duplication, 22q11.2 deletion). Models of idiopathic ASD include inbred rodent strains that mimic ASD behaviors as well as models developed by environmental interventions such as prenatal exposure to sodium valproate, maternal autoantibodies, and maternal immune activation. In addition to replicating some of the neuropathologic features seen in postmortem studies, a common finding in several animal models of ASD is altered density of dendritic spines, with the direction of the change depending on the specific genetic modification, age and brain region. Overall, postmortem neuropathologic studies with larger sample sizes representative of the various ASD risk genes and diverse clinical phenotypes are warranted to clarify putative etiopathogenic pathways further and to promote the emergence of clinically relevant diagnostic and therapeutic tools. In addition, as genetic alterations may render certain individuals more vulnerable to developing the pathological changes at the synapse underlying the behavioral manifestations of ASD, neuropathologic investigation using genetically modified animal models will help to improve our understanding of the disease mechanisms and enhance the development of targeted treatments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

(Modified from [359])

Fig. 6

Similar content being viewed by others

Abbreviations

ASD:

Autism spectrum disorders

PFC:

Prefrontal cortex

FG:

Fusiform gyrus

CA1:

Cornu ammonis 1

GABA:

γ-Aminobutyric acid

VEN:

von Economo neuron

FI:

Frontoinsular

ACC:

Anterior cingulate cortex

aMCC:

Anterior midcingulate cortex

PCC:

Posterior cingulate cortex

PIOTG:

Postero-inferior occipitotemporal gyrus

CNVs:

Copy number variations

NLGN:

Neuroligins

MRI:

Magnetic resonance imaging

KO:

Knockout

KI:

Knock-in

PSD:

Postsynaptic density

AMPA:

α-Amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid

NMDA:

N-Methyl-d-aspartic acid

NRXN:

Neurexins

WT:

Wild type

CNTNAP2:

Contactin associated protein-like 2

SHANK:

SH3 and multiple ankyrin repeat domains protein

MECP2:

Methyl-CpG-binding protein 2

FMR1:

Fragile X mental retardation 1

FMRP:

Fragile X mental retardation protein

UBE3A:

E6AP-E3 ubiquitin protein ligase

TSC:

Tuberous sclerosis

mTOR:

Mammalian target of rapamycin

CHD8:

Chromodomain helicase DNA-binding protein 8

SCN2A:

Sodium channel, voltage-gated, type II alpha subunit

SYNGAP1:

Synaptic GTPase activating protein 1

ARID1B:

AT-rich interactive domain containing protein 1B

GRIN2B:

Glutamate receptor ionotropic, NMDA 2B

DSCAM:

Down syndrome cell adhesion molecule

TBR1:

T-brain-1

VPA:

Sodium valproate

MIA:

Maternal immune activation

References

  1. Abrahams BS, Geschwind DH (2008) Nat Rev Genet 9:341–355. doi:10.1038/nrg2346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Aceti M, Creson TK, Vaissiere T, Rojas C, Huang WC, Wang YX, Petralia RS, Page DT, Miller CA, Rumbaugh G (2015) Biol Psychiatry 77:805–815. doi:10.1016/j.biopsych.2014.08.001

    Article  CAS  PubMed  Google Scholar 

  3. Akashi K, Kakizaki T, Kamiya H, Fukaya M, Yamasaki M, Abe M, Natsume R, Watanabe M, Sakimura K (2009) J Neurosci 29:10869–10882. doi:10.1523/JNEUROSCI.5531-08.2009

    Article  CAS  PubMed  Google Scholar 

  4. Allman J, Hakeem A, Watson K (2002) Neuroscientist 8:335–346

    Article  PubMed  Google Scholar 

  5. Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Goubert V, Hof PR (2010) Brain Struct Funct 214:495–517

    Article  PubMed  Google Scholar 

  6. Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Trends Cogn Sci. 9:367–373

    Article  PubMed  Google Scholar 

  7. Altemeier WA, Altemeier LE (2009) Pediatr Ann 38(167–170):172

    Google Scholar 

  8. Diagnostic and statistical manual of mental disorders: Dsm-5tm (2013) American Psychiatric Publishing, Inc., Arlington

  9. Anderson GR, Galfin T, Xu W, Aoto J, Malenka RC, Südhof TC (2012) Proc Natl Acad Sci USA 109:18120–18125. doi:10.1073/pnas.1216398109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Antshel KM, Aneja A, Strunge L, Peebles J, Fremont WP, Stallone K, Abdulsabur N, Higgins AM, Shprintzen RJ, Kates WR (2007) J Autism Dev Disord 37:1776–1786. doi:10.1007/s10803-006-0308-6

    Article  PubMed  Google Scholar 

  11. Araki Y, Zeng M, Zhang M, Huganir RL (2015) Neuron 85:173–189. doi:10.1016/j.neuron.2014.12.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ariza J, Rogers H, Hashemi E, Noctor SC, Martínez-Cerdeño V (2016) Cereb Cortex. doi:10.1093/cercor/bhw349

    Google Scholar 

  13. Armstrong D, Dunn JK, Antalffy B, Trivedi R (1995) J Neuropathol Exp Neurol 54:195–201

    Article  CAS  PubMed  Google Scholar 

  14. Atladóttir HO, Thorsen P, Østergaard L, Schendel DE, Lemcke S, Abdallah M, Parner ET (2010) J Autism Dev Disord 40:1423–1430. doi:10.1007/s10803-010-1006-y

    Article  PubMed  Google Scholar 

  15. Azmitia EC, Saccomano ZT, Alzoobaee MF, Boldrini M, Whitaker-Azmitia PM (2016) J Autism Dev Disord 46:1307–1318. doi:10.1007/s10803-015-2672-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Azmitia EC, Singh JS, Hou XP, Wegiel J (2011) Anat Rec (Hoboken) 294:1653–1662. doi:10.1002/ar.21243

    Article  CAS  Google Scholar 

  17. Azmitia EC, Singh JS, Whitaker-Azmitia PM (2011) Neuropharmacology 60:1347–1354. doi:10.1016/j.neuropharm.2011.02.002

    Article  CAS  PubMed  Google Scholar 

  18. Bagni C, Tassone F, Neri G, Hagerman R (2012) J Clin Invest 122:4314–4322. doi:10.1172/JCI63141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, Rutter M, Lantos P (1998) Brain 121(Pt 5):889–905

    Article  PubMed  Google Scholar 

  20. Baker K, Chaddock CA, Baldeweg T, Skuse D (2011) Neuroimage 55:491–499. doi:10.1016/j.neuroimage.2010.12.041

    Article  PubMed  Google Scholar 

  21. Barnea-Goraly N, Kwon H, Menon V, Eliez S, Lotspeich L, Reiss AL (2004) Biol Psychiatry 55:323–326

    Article  PubMed  Google Scholar 

  22. Barnes SA, Wijetunge LS, Jackson AD, Katsanevaki D, Osterweil EK, Komiyama NH, Grant SG, Bear MF, Nagerl UV, Kind PC et al (2015) J Neurosci 35:15073–15081. doi:10.1523/JNEUROSCI.1087-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bauman M, Kemper TL (1985) Neurology 35:866–874

    Article  CAS  PubMed  Google Scholar 

  24. Bauman MD, Iosif AM, Ashwood P, Braunschweig D, Lee A, Schumann CM, Van de Water J, Amaral DG (2013) Transl Psychiatry 3:e278. doi:10.1038/tp.2013.47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bauman ML, Kemper TL, Arin DM (1995) Neurology 45:1581–1586

    Article  CAS  PubMed  Google Scholar 

  26. Beal JC (2014) J Child Neurol 29(NP186-18):8. doi:10.1177/0883073813510356

    Google Scholar 

  27. Bearden CE, van Erp TG, Dutton RA, Tran H, Zimmermann L, Sun D, Geaga JA, Simon TJ, Glahn DC, Cannon TD et al (2007) Cereb Cortex 17:1889–1898. doi:10.1093/cercor/bhl097

    Article  PubMed  Google Scholar 

  28. Bedogni F, Hodge RD, Elsen GE, Nelson BR, Daza RA, Beyer RP, Bammler TK, Rubenstein JL, Hevner RF (2010) Proc Natl Acad Sci USA 107:13129–13134. doi:10.1073/pnas.1002285107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Belichenko PV, Oldfors A, Hagberg B, Dahlstrom A (1994) NeuroReport 5:1509–1513

    Article  CAS  PubMed  Google Scholar 

  30. Belichenko PV, Wright EE, Belichenko NP, Masliah E, Li HH, Mobley WC, Francke U (2009) J Comp Neurol. 514:240–258. doi:10.1002/cne.22009

    Article  CAS  PubMed  Google Scholar 

  31. Bellone C, Nicoll RA (2007) Neuron 55:779–785. doi:10.1016/j.neuron.2007.07.035

    Article  CAS  PubMed  Google Scholar 

  32. Bernier R, Golzio C, Xiong B, Stessman HA, Coe BP, Penn O, Witherspoon K, Gerdts J, Baker C, Vulto-van Silfhout AT et al (2014) Cell 158:263–276. doi:10.1016/j.cell.2014.06.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Berryer MH, Chattopadhyaya B, Xing P, Riebe I, Bosoi C, Sanon N, Antoine-Bertrand J, Levesque M, Avoli M, Hamdan FF et al (2016) Nat Commun 7:13340. doi:10.1038/ncomms13340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Blackmon K, Ben-Avi E, Wang X, Pardoe HR, Di Martino A, Halgren E, Devinsky O, Thesen T, Kuzniecky R (2016) Neuroimage Clin 10:36–45. doi:10.1016/j.nicl.2015.10.017

    Article  PubMed  Google Scholar 

  35. Blatt GJ (2005) Int Rev Neurobiol 71:167–178

    Article  CAS  PubMed  Google Scholar 

  36. Boer K, Troost D, Jansen F, Nellist M, van den Ouweland AM, Geurts JJ, Spliet WG, Crino P, Aronica E (2008) Neuropathology 28:577–590. doi:10.1111/j.1440-1789.2008.00920.x

    PubMed  Google Scholar 

  37. Bolliger MF, Pei J, Maxeiner S, Boucard AA, Grishin NV, Südhof TC (2008) Proc Natl Acad Sci USA 105:6421–6426. doi:10.1073/pnas.0801383105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bolte S, Hubl D, Feineis-Matthews S, Prvulovic D, Dierks T, Poustka F (2006) Behav Neurosci 120:211–216. doi:10.1037/0735-7044.120.1.211

    Article  PubMed  Google Scholar 

  39. Bozdagi O, Sakurai T, Papapetrou D, Wang XB, Dickstein DL, Takahashi N, Kajiwara Y, Yang M, Katz AM, Scattoni ML et al (2010) Mol Autism. doi:10.1186/2040-2392-1-15

    PubMed  PubMed Central  Google Scholar 

  40. Braunschweig D, Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Croen LA, Pessah IN, Van de Water J (2008) Neurotoxicology 29:226–231. doi:10.1016/j.neuro.2007.10.010

    CAS  PubMed  Google Scholar 

  41. Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S, Seabold GK, Mathur P, Davis MI, Bock R, Gustin RM et al (2010) J Neurosci 30:4590–4600. doi:10.1523/JNEUROSCI.0640-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bringas ME, Carvajal-Flores FN, Lopez-Ramirez TA, Atzori M, Flores G (2013) Neuroscience 241:170–187. doi:10.1016/j.neuroscience.2013.03.030

    Article  CAS  PubMed  Google Scholar 

  43. Broca P (1861) Bull Mem Soc Anat Paris. 36:330–357

    Google Scholar 

  44. Bromley RL, Mawer G, Clayton-Smith J, Baker GA, Liverpool, Manchester Neurodevelopment G (2008) Neurology 71:1923–1924. doi:10.1212/01.wnl.0000339399.64213.1a

    Article  CAS  PubMed  Google Scholar 

  45. Brown WS, Paul LK, Symington M, Dietrich R (2005) Neuropsychologia 43:906–916. doi:10.1016/j.neuropsychologia.2004.09.008

    Article  PubMed  Google Scholar 

  46. Buxhoeveden DP, Semendeferi K, Buckwalter J, Schenker N, Switzer R, Courchesne E (2006) Neuropathol Appl Neurobiol 32:483–491. doi:10.1111/j.1365-2990.2006.00745.x

    Article  CAS  PubMed  Google Scholar 

  47. Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) Nature 377:295–296. doi:10.1038/377295a0

    Article  CAS  PubMed  Google Scholar 

  48. Camacho J, Ejaz E, Ariza J, Noctor SC, Martínez-Cerdeño V (2014) Neurosci Lett 579:163–167. doi:10.1016/j.neulet.2014.07.031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Campbell LE, Daly E, Toal F, Stevens A, Azuma R, Catani M, Ng V, van Amelsvoort T, Chitnis X, Cutter W et al (2006) Brain 129:1218–1228. doi:10.1093/brain/awl066

    Article  PubMed  Google Scholar 

  50. Canovas J, Berndt FA, Sepulveda H, Aguilar R, Veloso FA, Montecino M, Oliva C, Maass JC, Sierralta J, Kukuljan M (2015) J Neurosci 35:7552–7564. doi:10.1523/JNEUROSCI.0169-15.2015

    Article  CAS  PubMed  Google Scholar 

  51. Carlisle HJ, Manzerra P, Marcora E, Kennedy MB (2008) J Neurosci 28:13673–13683. doi:10.1523/JNEUROSCI.4695-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Carper RA, Courchesne E (2005) Biol Psychiatry 57:126–133. doi:10.1016/j.biopsych.2004.11.005

    Article  PubMed  Google Scholar 

  53. Carper RA, Moses P, Tigue ZD, Courchesne E (2002) Neuroimage 16:1038–1051

    Article  PubMed  Google Scholar 

  54. Casanova MF (2006) Neuroscientist 12:435–441. doi:10.1177/1073858406290375

    Article  PubMed  Google Scholar 

  55. Casanova MF, Buxhoeveden DP, Brown C (2002) J Child Neurol 17:692–695

    Article  PubMed  Google Scholar 

  56. Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) J Child Neurol 17:142–145

    Article  PubMed  Google Scholar 

  57. Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Neurology 58:428–432

    Article  PubMed  Google Scholar 

  58. Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) J Child Neurol 17:515–521

    Article  PubMed  Google Scholar 

  59. Casanova MF, El-Baz AS, Kamat SS, Dombroski BA, Khalifa F, Elnakib A, Soliman A, Allison-McNutt A, Switala AE (2013) Acta Neuropathol Commun 1:67. doi:10.1186/2051-5960-1-67

    Article  PubMed  PubMed Central  Google Scholar 

  60. Caspers J, Zilles K, Amunts K, Laird AR, Fox PT, Eickhoff SB (2014) Hum Brain Mapp 35:2754–2767. doi:10.1002/hbm.22364

    Article  PubMed  Google Scholar 

  61. Caspers J, Zilles K, Eickhoff SB, Schleicher A, Mohlberg H, Amunts K (2013) Brain Struct Funct 218:511–526. doi:10.1007/s00429-012-0411-8

    Article  PubMed  Google Scholar 

  62. Chanda S, Aoto J, Lee SJ, Wernig M, Südhof TC (2016) Mol Psychiatry 21:169–177. doi:10.1038/mp.2015.20

    Article  CAS  PubMed  Google Scholar 

  63. Chao HT, Zoghbi HY, Rosenmund C (2007) Neuron 56:58–65. doi:10.1016/j.neuron.2007.08.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chapleau CA, Boggio EM, Calfa G, Percy AK, Giustetto M, Pozzo-Miller L (2012) Neural Plast 2012:976164. doi:10.1155/2012/976164

    PubMed  PubMed Central  Google Scholar 

  65. Chapleau CA, Calfa GD, Lane MC, Albertson AJ, Larimore JL, Kudo S, Armstrong DL, Percy AK, Pozzo-Miller L (2009) Neurobiol Dis 35:219–233. doi:10.1016/j.nbd.2009.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Chen HJ, Rojas-Soto M, Oguni A, Kennedy MB (1998) Neuron 20:895–904

    Article  CAS  PubMed  Google Scholar 

  67. Chen RZ, Akbarian S, Tudor M, Jaenisch R (2001) Nat Genet 27:327–331. doi:10.1038/85906

    Article  CAS  PubMed  Google Scholar 

  68. Christensen DL, Baio J, Braun KV, Bilder D, Charles J, Constantino JN, Daniels J, Durkin MS, Fitzgerald RT, Kurzius-Spencer M et al (2016) MMWR Surveill Summ 65:1–23. doi:10.15585/mmwr.ss6503a1

    Article  PubMed  Google Scholar 

  69. Christensen J, Gronborg TK, Sorensen MJ, Schendel D, Parner ET, Pedersen LH, Vestergaard M (2013) JAMA 309:1696–1703. doi:10.1001/jama.2013.2270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Chu-Shore CJ, Frosch MP, Grant PE, Thiele EA (2009) Epilepsia 50:2648–2651. doi:10.1111/j.1528-1167.2009.02193.x

    Article  PubMed  Google Scholar 

  71. Chuang HC, Huang TN, Hsueh YP (2014) Front Cell Neurosci 8:280. doi:10.3389/fncel.2014.00280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Clement JP, Aceti M, Creson TK, Ozkan ED, Shi Y, Reish NJ, Almonte AG, Miller BH, Wiltgen BJ, Miller CA et al (2012) Cell 151:709–723. doi:10.1016/j.cell.2012.08.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Codagnone MG, Podesta MF, Uccelli NA, Reines A (2015) Dev Neurosci 37:215–231. doi:10.1159/000375489

    Article  CAS  PubMed  Google Scholar 

  74. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT (1997) Proc Natl Acad Sci USA 94:5401–5404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Committee on Children with Disabilities 2000–2001 (2000) Pediatrics 2001(108):192–196

    Google Scholar 

  76. Courchesne E, Campbell K, Solso S (2011) Brain Res 1380:138–145. doi:10.1016/j.brainres.2010.09.101

    Article  CAS  PubMed  Google Scholar 

  77. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, Barnes CC, Pierce K (2011) JAMA 306:2001–2010. doi:10.1001/jama.2011.1638

    Article  CAS  PubMed  Google Scholar 

  78. Cruz-Martín A, Crespo M, Portera-Cailliau C (2010) J Neurosci 30:7793–7803. doi:10.1523/JNEUROSCI.0577-10.2010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Cruz-Martín A, Crespo M, Portera-Cailliau C (2012) PLoS One 7:e32446. doi:10.1371/journal.pone.0032446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW et al (2011) Cell 146:247–261. doi:10.1016/j.cell.2011.06.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. De Rubeis S, Buxbaum JD (2015) Hum Mol Genet 24:R24–R31. doi:10.1093/hmg/ddv273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. De Rubeis S, Buxbaum JD (2015) Curr Neurol Neurosci Rep 15:36. doi:10.1007/s11910-015-0553-1

    Article  PubMed  CAS  Google Scholar 

  83. De Rubeis S, He X, Goldberg AP, Poultney CS, Samocha K, Cicek AE, Kou Y, Liu L, Fromer M, Walker S et al (2014) Nature 515:209–215. doi:10.1038/nature13772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Debbane M, Schaer M, Farhoumand R, Glaser B, Eliez S (2006) Neuropsychologia 44:2360–2365. doi:10.1016/j.neuropsychologia.2006.05.006

    Article  PubMed  Google Scholar 

  85. Deboer T, Wu Z, Lee A, Simon TJ (2007) Behav Brain Funct 3:54. doi:10.1186/1744-9081-3-54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Dindot SV, Antalffy BA, Bhattacharjee MB, Beaudet AL (2008) Hum Mol Genet 17:111–118. doi:10.1093/hmg/ddm288

    Article  CAS  PubMed  Google Scholar 

  87. Dodero L, Damiano M, Galbusera A, Bifone A, Tsaftsaris SA, Scattoni ML, Gozzi A (2013) PLoS One 8:e76655. doi:10.1371/journal.pone.0076655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Doyle CA, McDougle CJ (2012) Dialogues Clin Neurosci 14:263–279

    PubMed  PubMed Central  Google Scholar 

  89. Dudanova I, Tabuchi K, Rohlmann A, Südhof TC, Missler M (2007) J Comp Neurol 502:261–274. doi:10.1002/cne.21305

    Article  CAS  PubMed  Google Scholar 

  90. Duffney LJ, Zhong P, Wei J, Matas E, Cheng J, Qin L, Ma K, Dietz DM, Kajiwara Y, Buxbaum JD et al (2015) Cell Rep 11:1400–1413. doi:10.1016/j.celrep.2015.04.064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Durak O, Gao F, Kaeser-Woo YJ, Rueda R, Martorell AJ, Nott A, Liu CY, Watson LA, Tsai LH (2016) Nat Neurosci 19:1477–1488. doi:10.1038/nn.4400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Earls LR, Bayazitov IT, Fricke RG, Berry RB, Illingworth E, Mittleman G, Zakharenko SS (2010) J Neurosci 30:15843–15855. doi:10.1523/JNEUROSCI.1425-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Easton CR, Dickey CW, Moen SP, Neuzil KE, Barger Z, Anderson TM, Moody WJ, Hevner RF (2016) Dev Neurobiol 76:705–720. doi:10.1002/dneu.22354

    Article  CAS  PubMed  Google Scholar 

  94. Edalatmanesh MA, Nikfarjam H, Vafaee F, Moghadas M (2013) Brain Res 1526:15–25. doi:10.1016/j.brainres.2013.06.024

    Article  CAS  PubMed  Google Scholar 

  95. Eilam-Stock T, Xu P, Cao M, Gu X, Van Dam NT, Anagnostou E, Kolevzon A, Soorya L, Park Y, Siller M et al (2014) Brain 137:153–171. doi:10.1093/brain/awt294

    Article  PubMed  PubMed Central  Google Scholar 

  96. Ellegood J, Babineau BA, Henkelman RM, Lerch JP, Crawley JN (2013) Neuroimage 70:288–300. doi:10.1016/j.neuroimage.2012.12.029

    Article  PubMed  Google Scholar 

  97. Ellegood J, Lerch JP, Henkelman RM (2011) Autism Res 4:368–376. doi:10.1002/aur.215

    Article  PubMed  Google Scholar 

  98. Ellegood J, Nakai N, Nakatani J, Henkelman M, Takumi T, Lerch J (2015) Autism Res 8:545–555. doi:10.1002/aur.1469

    Article  PubMed  Google Scholar 

  99. Etherton M, Foldy C, Sharma M, Tabuchi K, Liu X, Shamloo M, Malenka RC, Südhof TC (2011) Proc Natl Acad Sci USA 108:13764–13769. doi:10.1073/pnas.1111093108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Etherton MR, Tabuchi K, Sharma M, Ko J, Südhof TC (2011) EMBO J 30:2908–2919. doi:10.1038/emboj.2011.182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Fairhall SL, Ishai A (2007) Cereb Cortex 17:2400–2406. doi:10.1093/cercor/bhl148

    Article  PubMed  Google Scholar 

  102. Fairless AH, Dow HC, Kreibich AS, Torre M, Kuruvilla M, Gordon E, Morton EA, Tan J, Berrettini WH, Li H et al (2012) Behav Brain Res 228:299–310. doi:10.1016/j.bbr.2011.12.001

    Article  PubMed  Google Scholar 

  103. Fairless AH, Dow HC, Toledo MM, Malkus KA, Edelmann M, Li H, Talbot K, Arnold SE, Abel T, Brodkin ES (2008) Brain Res 1230:211–217. doi:10.1016/j.brainres.2008.07.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Fajardo C, Escobar MI, Buritica E, Arteaga G, Umbarila J, Casanova MF, Pimienta H (2008) Neurosci Lett 435:215–218. doi:10.1016/j.neulet.2008.02.048

    Article  CAS  PubMed  Google Scholar 

  105. Fan J, Bernardi S, Van Dam NT, Anagnostou E, Gu X, Martin L, Park Y, Liu X, Kolevzon A, Soorya L et al (2012) Brain Behav 2:647–660. doi:10.1002/brb3.90

    Article  PubMed  PubMed Central  Google Scholar 

  106. Fan J, Gu X, Liu X, Guise KG, Park Y, Martin L, de Marchena A, Tang CY, Minzenberg MJ, Hof PR (2011) Neuroimage 54:2539–2546. doi:10.1016/j.neuroimage.2010.10.007

    Article  PubMed  Google Scholar 

  107. Fan J, Hof PR, Guise KG, Fossella JA, Posner MI (2008) Cereb Cortex 18:796–805. doi:10.1093/cercor/bhm125

    Article  PubMed  Google Scholar 

  108. Fatemi SH, Halt AR, Realmuto G, Earle J, Kist DA, Thuras P, Merz A (2002) Cell Mol Neurobiol 22:171–175

    Article  PubMed  Google Scholar 

  109. Feliciano DM, Quon JL, Su T, Taylor MM, Bordey A (2012) Hum Mol Genet 21:799–810. doi:10.1093/hmg/ddr511

    Article  CAS  PubMed  Google Scholar 

  110. Feliciano DM, Su T, Lopez J, Platel JC, Bordey A (2011) J Clin Invest 121:1596–1607. doi:10.1172/JCI44909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Fenelon K, Mukai J, Xu B, Hsu PK, Drew LJ, Karayiorgou M, Fischbach GD, Macdermott AB, Gogos JA (2011) Proc Natl Acad Sci USA 108:4447–4452. doi:10.1073/pnas.1101219108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Fenelon K, Xu B, Lai CS, Mukai J, Markx S, Stark KL, Hsu PK, Gan WB, Fischbach GD, MacDermott AB et al (2013) J Neurosci 33:14825–14839. doi:10.1523/JNEUROSCI.1611-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Fombonne E (2003) JAMA 289:87–89

    Article  PubMed  Google Scholar 

  114. Frazier TW, Hardan AY (2009) Biol Psychiatry 66:935–941. doi:10.1016/j.biopsych.2009.07.022

    Article  PubMed  PubMed Central  Google Scholar 

  115. Fukuda T, Itoh M, Ichikawa T, Washiyama K, Goto Y (2005) J Neuropathol Exp Neurol 64:537–544

    Article  CAS  PubMed  Google Scholar 

  116. Fuster JM (2001) Neuron 30:319–333

    Article  CAS  PubMed  Google Scholar 

  117. Galvez R, Gopal AR, Greenough WT (2003) Brain Res 971:83–89

    Article  CAS  PubMed  Google Scholar 

  118. Galvez R, Greenough WT (2005) Am J Med Genet A 135:155–160. doi:10.1002/ajmg.a.30709

    Article  PubMed  Google Scholar 

  119. Gaugler T, Klei L, Sanders SJ, Bodea CA, Goldberg AP, Lee AB, Mahajan M, Manaa D, Pawitan Y, Reichert J et al (2014) Nat Genet 46:881–885. doi:10.1038/ng.3039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Gazina EV, Leaw BT, Richards KL, Wimmer VC, Kim TH, Aumann TD, Featherby TJ, Churilov L, Hammond VE, Reid CA et al (2015) Hum Mol Genet 24:1457–1468. doi:10.1093/hmg/ddu562

    Article  CAS  PubMed  Google Scholar 

  121. Gazina EV, Richards KL, Mokhtar MB, Thomas EA, Reid CA, Petrou S (2010) Neuroscience 166:195–200. doi:10.1016/j.neuroscience.2009.12.011

    Article  CAS  PubMed  Google Scholar 

  122. Gdalyahu A, Lazaro M, Peñagarikano O, Golshani P, Trachtenberg JT, Geschwind DH (2015) PLoS One 10:e0125633. doi:10.1371/journal.pone.0125633

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. George J, Baden DG, Gerwick WH, Murray TF (2012) Proc Natl Acad Sci USA 109:19840–19845. doi:10.1073/pnas.1212584109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. George J, Dravid SM, Prakash A, Xie J, Peterson J, Jabba SV, Baden DG, Murray TF (2009) J Neurosci 29:3288–3301. doi:10.1523/JNEUROSCI.6104-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Gillberg C (1991) J Autism Dev Disord 21:61–77

    Article  CAS  PubMed  Google Scholar 

  126. Goffin D, Allen M, Zhang L, Amorim M, Wang IT, Reyes AR, Mercado-Berton A, Ong C, Cohen S, Hu L et al (2012) Nat Neurosci 15:274–283. doi:10.1038/nn.2997

    Article  CAS  Google Scholar 

  127. Gogolla N, Leblanc JJ, Quast KB, Südhof TC, Fagiolini M, Hensch TK (2009) J Neurodev Disord 1:172–181. doi:10.1007/s11689-009-9023-x

    Article  PubMed  PubMed Central  Google Scholar 

  128. Greco CM, Navarro CS, Hunsaker MR, Maezawa I, Shuler JF, Tassone F, Delany M, Au JW, Berman RF, Jin LW et al (2011) Mol Autism 2:2. doi:10.1186/2040-2392-2-2

    Article  PubMed  PubMed Central  Google Scholar 

  129. Grossman AW, Aldridge GM, Lee KJ, Zeman MK, Jun CS, Azam HS, Arii T, Imoto K, Greenough WT, Rhyu IJ (2010) Brain Res 1355:221–227. doi:10.1016/j.brainres.2010.07.090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Grossman AW, Elisseou NM, McKinney BC, Greenough WT (1084) Brain Res 2006:158–164. doi:10.1016/j.brainres.2006.02.044

    Google Scholar 

  131. Gu X, Eilam-Stock T, Zhou T, Anagnostou E, Kolevzon A, Soorya L, Hof PR, Friston KJ, Fan J (2015) Hum Brain Mapp 36:3323–3338. doi:10.1002/hbm.22840

    Article  PubMed  PubMed Central  Google Scholar 

  132. Gu X, Hof PR, Friston KJ, Fan J (2013) J Comp Neurol 521:3371–3388. doi:10.1002/cne.23368

    Article  PubMed  PubMed Central  Google Scholar 

  133. Gu X, Liu X, Van Dam NT, Hof PR, Fan J (2013) Cereb Cortex 23:20–27. doi:10.1093/cercor/bhr367

    Article  PubMed  Google Scholar 

  134. Guo YP, Commons KG (2017) Autism Res 10:66–77. doi:10.1002/aur.1665

    Article  PubMed  Google Scholar 

  135. Gutstein SE (2009) Ann Clin Psychiatry 21:174–182

    PubMed  Google Scholar 

  136. Haar S, Berman S, Behrmann M, Dinstein I (2016) Cereb Cortex 26:1440–1452. doi:10.1093/cercor/bhu242

    Article  PubMed  Google Scholar 

  137. Hadjikhani N, Joseph RM, Snyder J, Chabris CF, Clark J, Steele S, McGrath L, Vangel M, Aharon I, Feczko E et al (2004) Neuroimage 22:1141–1150. doi:10.1016/j.neuroimage.2004.03.025

    Article  PubMed  Google Scholar 

  138. Hagerman R, Hoem G, Hagerman P (2010) Mol Autism 1:12. doi:10.1186/2040-2392-1-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, Miller J, Fedele A, Collins J, Smith K et al (2011) Arch Gen Psychiatry 68:1095–1102. doi:10.1001/archgenpsychiatry.2011.76

    Article  PubMed  PubMed Central  Google Scholar 

  140. Hammer M, Krueger-Burg D, Tuffy LP, Cooper BH, Taschenberger H, Goswami SP, Ehrenreich H, Jonas P, Varoqueaux F, Rhee JS et al (2015) Cell Rep 13:516–523. doi:10.1016/j.celrep.2015.09.011

    Article  CAS  PubMed  Google Scholar 

  141. Han K, Holder JL Jr, Schaaf CP, Lu H, Chen H, Kang H, Tang J, Wu Z, Hao S, Cheung SW et al (2013) Nature 503:72–77. doi:10.1038/nature12630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Han W, Kwan KY, Shim S, Lam MM, Shin Y, Xu X, Zhu Y, Li M, Sestan N (2011) Proc Natl Acad Sci USA 108:3041–3046. doi:10.1073/pnas.1016723108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Hardan AY, Libove RA, Keshavan MS, Melhem NM, Minshew NJ (2009) Biol Psychiatry 66:320–326. doi:10.1016/j.biopsych.2009.04.024

    Article  PubMed  PubMed Central  Google Scholar 

  144. Harlow EG, Till SM, Russell TA, Wijetunge LS, Kind P, Contractor A (2010) Neuron 65:385–398. doi:10.1016/j.neuron.2010.01.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Harony-Nicolas H, De Rubeis S, Kolevzon A, Buxbaum JD (2015) J Child Neurol 30:1861–1870. doi:10.1177/0883073815600872

    Article  PubMed  PubMed Central  Google Scholar 

  146. Harting I, Seitz A, Rating D, Sartor K, Zschocke J, Janssen B, Ebinger F, Wolf NI (2009) Eur J Paediatr Neurol 13:271–276. doi:10.1016/j.ejpn.2008.04.005

    Article  PubMed  Google Scholar 

  147. Hashemi E, Ariza J, Lechpammer M, Noctor SC, Martínez-Cerdeño V (2016) J Med Case Rep 10:237. doi:10.1186/s13256-016-1020-6

    Article  PubMed  PubMed Central  Google Scholar 

  148. Hashemi E, Ariza J, Rogers H, Noctor SC, Martínez-Cerdeño V (2016) Cereb Cortex. doi:10.1093/cercor/bhw021

    PubMed  Google Scholar 

  149. Haxby JV, Hoffman EA, Gobbini MI (2000) Trends Cogn Sci 4:223–233

    Article  CAS  PubMed  Google Scholar 

  150. Hayashi M, Itoh M, Kabasawa Y, Hayashi H, Satoh J, Morimatsu Y (1992) Brain Dev 14:58–62

    Article  CAS  PubMed  Google Scholar 

  151. Hazlett HC, Gu H, Munsell BC, Kim SH, Styner M, Wolff JJ, Elison JT, Swanson MR, Zhu H, Botteron KN et al (2017) Nature 542:348–351. doi:10.1038/nature21369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Hazlett HC, Poe MD, Gerig G, Styner M, Chappell C, Smith RG, Vachet C, Piven J (2011) Arch Gen Psychiatry 68:467–476. doi:10.1001/archgenpsychiatry.2011.39

    Article  PubMed  PubMed Central  Google Scholar 

  153. Haznedar MM, Buchsbaum MS, Wei TC, Hof PR, Cartwright C, Bienstock CA, Hollander E (2000) Am J Psychiatry 157:1994–2001

    Article  CAS  PubMed  Google Scholar 

  154. He H, Kise Y, Izadifar A, Urwyler O, Ayaz D, Parthasarthy A, Yan B, Erfurth ML, Dascenco D, Schmucker D (2014) Science 344:1182–1186. doi:10.1126/science.1251852

    Article  CAS  PubMed  Google Scholar 

  155. Hering H, Sheng M (2001) Nat Rev Neurosci 2:880–888. doi:10.1038/35104061

    Article  CAS  PubMed  Google Scholar 

  156. Hevner RF, Miyashita-Lin E, Rubenstein JL (2002) J Comp Neurol 447:8–17. doi:10.1002/cne.10219

    Article  PubMed  Google Scholar 

  157. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Neuron 29:353–366

    Article  CAS  PubMed  Google Scholar 

  158. Hinton VJ, Brown WT, Wisniewski K, Rudelli RD (1991) Am J Med Genet 41:289–294. doi:10.1002/ajmg.1320410306

    Article  CAS  PubMed  Google Scholar 

  159. Horev G, Ellegood J, Lerch JP, Son YE, Muthuswamy L, Vogel H, Krieger AM, Buja A, Henkelman RM, Wigler M et al (2011) Proc Natl Acad Sci USA 108:17076–17081. doi:10.1073/pnas.1114042108

    Article  PubMed  PubMed Central  Google Scholar 

  160. Horsthemke B, Wagstaff J (2008) Am J Med Genet A 146A:2041–2052. doi:10.1002/ajmg.a.32364

    Article  CAS  PubMed  Google Scholar 

  161. Huang TN, Chuang HC, Chou WH, Chen CY, Wang HF, Chou SJ, Hsueh YP (2014) Nat Neurosci 17:240–247. doi:10.1038/nn.3626

    Article  CAS  PubMed  Google Scholar 

  162. Hutsler JJ, Zhang H (2010) Brain Res 1309:83–94. doi:10.1016/j.brainres.2009.09.120

    Article  CAS  PubMed  Google Scholar 

  163. Huttenlocher PR, Wollmann RL (1991) Ann N Y Acad Sci 615:140–148

    Article  CAS  PubMed  Google Scholar 

  164. Ingram JL, Peckham SM, Tisdale B, Rodier PM (2000) Neurotoxicol Teratol 22:319–324

    Article  CAS  PubMed  Google Scholar 

  165. Iossifov I, O’Roak BJ, Sanders SJ, Ronemus M, Krumm N, Levy D, Stessman HA, Witherspoon KT, Vives L, Patterson KE et al (2014) Nature 515:216–221. doi:10.1038/nature13908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Iossifov I, Ronemus M, Levy D, Wang Z, Hakker I, Rosenbaum J, Yamrom B, Lee YH, Narzisi G, Leotta A et al (2012) Neuron 74:285–299. doi:10.1016/j.neuron.2012.04.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Irwin SA, Galvez R, Greenough WT (2000) Cereb Cortex 10:1038–1044

    Article  CAS  PubMed  Google Scholar 

  168. Irwin SA, Idupulapati M, Gilbert ME, Harris JB, Chakravarti AB, Rogers EJ, Crisostomo RA, Larsen BP, Mehta A, Alcantara CJ et al (2002) Am J Med Genet 111:140–146. doi:10.1002/ajmg.10500

    Article  PubMed  Google Scholar 

  169. Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, Larsen BP, Kooy F, Willems PJ, Cras P, Kozlowski PB et al (2001) Am J Med Genet 98:161–167. doi:10.1002/1096-8628(20010115)98:2<161:AID-AJMG1025>3.0.CO;2-B

    Article  CAS  PubMed  Google Scholar 

  170. Ishai A, Int J (2007) Psychophysiol 63:181–185. doi:10.1016/j.ijpsycho.2006.03.010

    Article  Google Scholar 

  171. Ishai A, Haxby JV, Ungerleider LG (2002) Neuroimage 17:1729–1741

    Article  PubMed  Google Scholar 

  172. Isshiki M, Tanaka S, Kuriu T, Tabuchi K, Takumi T, Okabe S (2014) Nat Commun 5:4742. doi:10.1038/ncomms5742

    Article  CAS  PubMed  Google Scholar 

  173. Jacot-Descombes S, Uppal N, Wicinski B, Santos M, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR (2012) Acta Neuropathol 124:67–79. doi:10.1007/s00401-012-0976-6

    Article  CAS  PubMed  Google Scholar 

  174. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C et al (2003) Nat Genet 34:27–29. doi:10.1038/ng1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, Varoqueaux F, Ramanantsoa N, Gallego J, Ronnenberg A, Winter D et al (2008) Proc Natl Acad Sci USA 105:1710–1715. doi:10.1073/pnas.0711555105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Jay V, Becker LE, Chan FW, Perry TL Sr (1991) Neurology 41:416–422

    Article  CAS  PubMed  Google Scholar 

  177. Jellinger K, Seitelberger F (1986) Am J Med Genet Suppl 1:259–288

    Article  CAS  PubMed  Google Scholar 

  178. Jentarra GM, Olfers SL, Rice SG, Srivastava N, Homanics GE, Blue M, Naidu S, Narayanan V (2010) BMC Neurosci 11:19. doi:10.1186/1471-2202-11-19

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  179. Jiang H, Jiang W, Zou J, Wang B, Yu M, Pan Y, Lin Y, Mao Y, Wang Y (2015) Brain Res 1610:20–32. doi:10.1016/j.brainres.2015.03.031

    Article  CAS  PubMed  Google Scholar 

  180. Jiang M, Ash RT, Baker SA, Suter B, Ferguson A, Park J, Rudy J, Torsky SP, Chao HT, Zoghbi HY et al (2013) J Neurosci 33:19518–19533. doi:10.1523/JNEUROSCI.1745-13.2013

    Article  PubMed  PubMed Central  Google Scholar 

  181. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL (1998) Neuron 21:799–811

    Article  CAS  PubMed  Google Scholar 

  182. Jones EG (1986) Connectivity of the primate sensory-motor cortex. In: Jones EG, Peters A (eds) Cerebral cortex: sensory-motor areas and aspects of cortical connectivity. Plenum, New York, pp 113–183

    Chapter  Google Scholar 

  183. Ka M, Chopra DA, Dravid SM, Kim WY (2016) J Neurosci 36:2723–2742. doi:10.1523/JNEUROSCI.2321-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Kadam SD, French BM, Kim ST, Morris-Berry CM, Zimmerman AW, Blue ME, Singer HS (2013) J Exp Neurosci 7:93–99. doi:10.4137/JEN.S12979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Kanwisher N, Stanley D, Harris A (1999) NeuroReport 10:183–187

    Article  CAS  PubMed  Google Scholar 

  186. Kataoka S, Takuma K, Hara Y, Maeda Y, Ago Y, Matsuda T (2013) Int J Neuropsychopharmacol 16:91–103. doi:10.1017/S1461145711001714

    Article  CAS  PubMed  Google Scholar 

  187. Katayama Y, Nishiyama M, Shoji H, Ohkawa Y, Kawamura A, Sato T, Suyama M, Takumi T, Miyakawa T, Nakayama KI (2016) Nature 537:675–679. doi:10.1038/nature19357

    Article  CAS  PubMed  Google Scholar 

  188. Kaufman JA, Paul LK, Manaye KF, Granstedt AE, Hof PR, Hakeem AY, Allman JM (2008) Acta Neuropathol 116:479–489. doi:10.1007/s00401-008-0434-7

    Article  PubMed  Google Scholar 

  189. Kazlauskas N, Campolongo M, Lucchina L, Zappala C, Depino AM (2016) Psychoneuroendocrinology 72:11–21. doi:10.1016/j.psyneuen.2016.06.001

    Article  CAS  PubMed  Google Scholar 

  190. Kearney JA, Plummer NW, Smith MR, Kapur J, Cummins TR, Waxman SG, Goldin AL, Meisler MH (2001) Neuroscience 102:307–317

    Article  CAS  PubMed  Google Scholar 

  191. Kemper TL, Bauman ML (1993) Neurol Clin 11:175–187

    CAS  PubMed  Google Scholar 

  192. Kennedy DP, Semendeferi K, Courchesne E (2007) Brain Cogn 64:124–129

    Article  PubMed  Google Scholar 

  193. Kiehl TR, Chow EW, Mikulis DJ, George SR, Bassett AS (2009) Cereb Cortex 19:153–164. doi:10.1093/cercor/bhn066

    Article  CAS  PubMed  Google Scholar 

  194. Kim E, Camacho J, Combs Z, Ariza J, Lechpammer M, Noctor SC, Martínez-Cerdeño V (2015) Neurosci Lett 589:98–103. doi:10.1016/j.neulet.2015.01.021

    Article  CAS  PubMed  Google Scholar 

  195. Kim EJ, Sidhu M, Gaus SE, Huang EJ, Hof PR, Miller BL, DeArmond SJ, Seeley WW (2012) Cereb Cortex 22:251–259. doi:10.1093/cercor/bhr004

    Article  PubMed  Google Scholar 

  196. Kim H, Kunz PA, Mooney R, Philpot BD, Smith SL (2016) J Neurosci 36:4888–4894. doi:10.1523/JNEUROSCI.4204-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Kim JH, Liao D, Lau LF, Huganir RL (1998) Neuron 20:683–691

    Article  CAS  PubMed  Google Scholar 

  198. Kim KC, Choi CS, Kim JW, Han SH, Cheong JH, Ryu JH, Shin CY (2016) Mol Neurobiol 53:40–56. doi:10.1007/s12035-014-8987-z

    Article  CAS  PubMed  Google Scholar 

  199. Kim KC, Kim P, Go HS, Choi CS, Park JH, Kim HJ, Jeon SJ, Dela Pena IC, Han SH, Cheong JH et al (2013) J Neurochem 124:832–843. doi:10.1111/jnc.12147

    Article  CAS  PubMed  Google Scholar 

  200. Kishi N, Macklis JD (2004) Mol Cell Neurosci 27:306–321. doi:10.1016/j.mcn.2004.07.006

    Article  CAS  PubMed  Google Scholar 

  201. Klemmer P, Meredith RM, Holmgren CD, Klychnikov OI, Stahl-Zeng J, Loos M, van der Schors RC, Wortel J, de Wit H, Spijker S et al (2011) J Biol Chem 286:25495–25504. doi:10.1074/jbc.M110.210260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Kloth AD, Badura A, Li A, Cherskov A, Connolly SG, Giovannucci A, Bangash MA, Grasselli G, Peñagarikano O, Piochon C et al (2015) Elife 4:e06085. doi:10.7554/eLife.06085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  203. Koegel RL, Shirotova L, Koegel LK (2009) J Autism Dev Disord 39:1587–1592. doi:10.1007/s10803-009-0765-9

    Article  PubMed  PubMed Central  Google Scholar 

  204. Kogan JH, Gross AK, Featherstone RE, Shin R, Chen Q, Heusner CL, Adachi M, Lin A, Walton NM, Miyoshi S et al (2015) J Neurosci 35:16282–16294. doi:10.1523/JNEUROSCI.3967-14.2015

    Article  CAS  PubMed  Google Scholar 

  205. Kotagiri P, Chance SA, Szele FG, Esiri MM (2014) Dev Neurobiol 74:25–41. doi:10.1002/dneu.22127

    Article  CAS  PubMed  Google Scholar 

  206. Kouser M, Speed HE, Dewey CM, Reimers JM, Widman AJ, Gupta N, Liu S, Jaramillo TC, Bangash M, Xiao B et al (2013) J Neurosci 33:18448–18468. doi:10.1523/JNEUROSCI.3017-13.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Kulesza RJ, Mangunay K (2008) Brain Res 1200:132–137. doi:10.1016/j.brainres.2008.01.009

    Article  CAS  PubMed  Google Scholar 

  208. Kutsuwada T, Sakimura K, Manabe T, Takayama C, Katakura N, Kushiya E, Natsume R, Watanabe M, Inoue Y, Yagi T et al (1996) Neuron 16:333–344

    Article  CAS  PubMed  Google Scholar 

  209. Kyriakides T, Hallam LA, Hockey A, Silberstein P, Kakulas BA (1992) Acta Neuropathol 83:675–678

    Article  CAS  PubMed  Google Scholar 

  210. Lassi G, Priano L, Maggi S, Garcia-Garcia C, Balzani E, El-Assawy N, Pagani M, Tinarelli F, Giardino D, Mauro A et al (2016) Sleep 39:637–644. doi:10.5665/sleep.5542

    Article  PubMed  PubMed Central  Google Scholar 

  211. Lawrence YA, Kemper TL, Bauman ML, Blatt GJ (2010) Acta Neurol Scand 121:99–108. doi:10.1111/j.1600-0404.2009.01234.x

    Article  CAS  PubMed  Google Scholar 

  212. LeDoux J (2007) Curr Biol 17:R868–R874. doi:10.1016/j.cub.2007.08.005

    Article  CAS  PubMed  Google Scholar 

  213. Lee HJ, Dreyfus C, DiCicco-Bloom E (2016) Dev Neurobiol 76:780–798. doi:10.1002/dneu.22359

    Article  CAS  PubMed  Google Scholar 

  214. Levenga J, de Vrij FM, Buijsen RA, Li T, Nieuwenhuizen IM, Pop A, Oostra BA, Willemsen R (2011) Neurobiol Learn Mem 95:467–472. doi:10.1016/j.nlm.2011.02.009

    Article  CAS  PubMed  Google Scholar 

  215. Li H, Zhao P, Xu Q, Shan S, Hu C, Qiu Z, Xu X (2016) Sci Rep 6:29878. doi:10.1038/srep29878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Li S, Sukeena JM, Simmons AB, Hansen EJ, Nuhn RE, Samuels IS, Fuerst PG (2015) J Neurosci 35:5640–5654. doi:10.1523/JNEUROSCI.2202-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Li W, Xu X, Pozzo-Miller L (2016) Proc Natl Acad Sci USA. doi:10.1073/pnas.1517244113

    Google Scholar 

  218. Liakakis G, Nickel J, Seitz RJ (2011) Behav Brain Res 225:341–347. doi:10.1016/j.bbr.2011.06.022

    Article  CAS  PubMed  Google Scholar 

  219. Loutzenhiser L, Hadjistavropoulos H (2008) J Interprof Care 22:429–431. doi:10.1080/13561820801886487

    Article  PubMed  Google Scholar 

  220. Lui JH, Hansen DV, Kriegstein AR (2011) Cell 146:18–36. doi:10.1016/j.cell.2011.06.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Lukose R, Schmidt E, Wolski TP Jr, Murawski NJ, Kulesza RJ Jr (2011) Brain Res 1398:102–112. doi:10.1016/j.brainres.2011.05.013

    Article  CAS  PubMed  Google Scholar 

  222. Lukoshe A, White T, Schmidt MN, van der Lugt A, Hokken-Koelega AC (2013) J Neurodev Disord 5:31. doi:10.1186/1866-1955-5-31

    Article  PubMed  PubMed Central  Google Scholar 

  223. Maddock RJ (1999) Trends Neurosci 22:310–316

    Article  CAS  PubMed  Google Scholar 

  224. Maddock RJ, Garrett AS, Buonocore MH (2003) Hum Brain Mapp 18:30–41. doi:10.1002/hbm.10075

    Article  PubMed  Google Scholar 

  225. Maddock RJ, Garrett AS, Buonocore MH (2001) Neuroscience 104:667–676

    Article  CAS  PubMed  Google Scholar 

  226. Magri L, Cominelli M, Cambiaghi M, Cursi M, Leocani L, Minicucci F, Poliani PL, Galli R (2013) Dis Model Mech 6:1185–1197. doi:10.1242/dmm.012096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Maillard AM, Ruef A, Pizzagalli F, Migliavacca E, Hippolyte L, Adaszewski S, Dukart J, Ferrari C, Conus P, Mannik K et al (2015) Mol Psychiatry 20:140–147. doi:10.1038/mp.2014.145

    Article  CAS  PubMed  Google Scholar 

  228. Main SL, Kulesza RJ (2017) Neuroscience 340:34–47. doi:10.1016/j.neuroscience.2016.10.052

    Article  CAS  PubMed  Google Scholar 

  229. Martínez-Cerdeño V, Camacho J, Fox E, Miller E, Ariza J, Kienzle D, Plank K, Noctor SC, Van de Water J (2016) Cereb Cortex 26:374–383. doi:10.1093/cercor/bhu291

    Article  PubMed  Google Scholar 

  230. Maynard KR, Stein E (2012) J Neurosci 32:16637–16650. doi:10.1523/JNEUROSCI.2811-12.2012

    Article  CAS  PubMed  Google Scholar 

  231. Mazina V, Gerdts J, Trinh S, Ankenman K, Ward T, Dennis MY, Girirajan S, Eichler EE, Bernier R (2015) J Dev Behav Pediatr 36:61–67. doi:10.1097/DBP.0000000000000126

    Article  PubMed  PubMed Central  Google Scholar 

  232. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B (2011) J Neurosci 31:549–564. doi:10.1523/JNEUROSCI.4131-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. McKinney BC, Grossman AW, Elisseou NM, Greenough WT (2005) Am J Med Genet B Neuropsychiatr Genet 136B:98–102. doi:10.1002/ajmg.b.30183

    Article  PubMed  Google Scholar 

  234. Meechan DW, Tucker ES, Maynard TM, LaMantia AS (2009) Proc Natl Acad Sci USA 106:16434–16445. doi:10.1073/pnas.0905696106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. Mei Y, Monteiro P, Zhou Y, Kim JA, Gao X, Fu Z, Feng G (2016) Nature 530:481–484. doi:10.1038/nature16971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. Meikle L, Talos DM, Onda H, Pollizzi K, Rotenberg A, Sahin M, Jensen FE, Kwiatkowski DJ (2007) J Neurosci 27:5546–5558. doi:10.1523/JNEUROSCI.5540-06.2007

    Article  CAS  PubMed  Google Scholar 

  237. Mercer RE, Kwolek EM, Bischof JM, van Eede M, Henkelman RM, Wevrick R (2009) Am J Med Genet B Neuropsychiatr Genet 150B:1085–1099. doi:10.1002/ajmg.b.30934

    Article  CAS  PubMed  Google Scholar 

  238. Miller EK, Cohen JD (2001) Annu Rev Neurosci 24:167–202. doi:10.1146/annurev.neuro.24.1.167

    Article  CAS  PubMed  Google Scholar 

  239. Miller JL, Couch JA, Schmalfuss I, He G, Liu Y, Driscoll DJ (2007) Am J Med Genet A 143A:476–483. doi:10.1002/ajmg.a.31508

    Article  PubMed  Google Scholar 

  240. Miller VM, Gupta D, Neu N, Cotroneo A, Boulay CB, Seegal RF (2013) Brain Res 1513:26–33. doi:10.1016/j.brainres.2013.04.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Minshew NJ, Keller TA (2010) Curr Opin Neurol 23:124–130. doi:10.1097/WCO.0b013e32833782d4

    Article  PubMed  PubMed Central  Google Scholar 

  242. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, Südhof TC (2003) Nature 423:939–948. doi:10.1038/nature01755

    Article  CAS  PubMed  Google Scholar 

  243. Mizuguchi M, Takashima S (2001) Brain Dev 23:508–515

    Article  CAS  PubMed  Google Scholar 

  244. Morgan JT, Barger N, Amaral DG, Schumann CM (2014) PLoS One 9:e110356. doi:10.1371/journal.pone.0110356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  245. Morgan JT, Chana G, Abramson I, Semendeferi K, Courchesne E, Everall IP (2012) Brain Res 1456:72–81. doi:10.1016/j.brainres.2012.03.036

    Article  CAS  PubMed  Google Scholar 

  246. Mountcastle VB (1997) Brain 120(Pt 4):701–722

    Article  PubMed  Google Scholar 

  247. Mowery TM, Wilson SM, Kostylev PV, Dina B, Buchholz JB, Prieto AL, Garraghty PE (2015) Int J Dev Neurosci 40:15–23. doi:10.1016/j.ijdevneu.2014.10.003

    Article  CAS  PubMed  Google Scholar 

  248. Mukaetova-Ladinska EB, Arnold H, Jaros E, Perry R, Perry E (2004) Neuropathol Appl Neurobiol 30:615–623. doi:10.1111/j.1365-2990.2004.00574.x

    Article  CAS  PubMed  Google Scholar 

  249. Mukai J, Dhilla A, Drew LJ, Stark KL, Cao L, MacDermott AB, Karayiorgou M, Gogos JA (2008) Nat Neurosci 11:1302–1310. doi:10.1038/nn.2204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Mychasiuk R, Richards S, Nakahashi A, Kolb B, Gibb R (2012) Dev Neurosci 34:268–276. doi:10.1159/000341786

    Article  CAS  PubMed  Google Scholar 

  251. Nagaoka A, Takehara H, Hayashi-Takagi A, Noguchi J, Ishii K, Shirai F, Yagishita S, Akagi T, Ichiki T, Kasai H (2016) Sci Rep 6:26651. doi:10.1038/srep26651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, Weinberg RJ, Worley PF, Sheng M (1999) Neuron 23:569–582

    Article  CAS  PubMed  Google Scholar 

  253. Nakatani J, Tamada K, Hatanaka F, Ise S, Ohta H, Inoue K, Tomonaga S, Watanabe Y, Chung YJ, Banerjee R et al (2009) Cell 137:1235–1246. doi:10.1016/j.cell.2009.04.024

    Article  PubMed  PubMed Central  Google Scholar 

  254. Neale BM, Kou Y, Liu L, Ma’ayan A, Samocha KE, Sabo A, Lin CF, Stevens C, Wang LS, Makarov V et al (2012) Nature. 485:242–245. doi:10.1038/nature11011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  255. Neuhofer D, Henstridge CM, Dudok B, Sepers M, Lassalle O, Katona I, Manzoni OJ (2015) Front Cell Neurosci 9:100. doi:10.3389/fncel.2015.00100

    Article  PubMed  PubMed Central  Google Scholar 

  256. Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR (1999) Proc Natl Acad Sci USA 96:5268–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Nimchinsky EA, Oberlander AM, Svoboda K (2001) J Neurosci 21:5139–5146

    CAS  PubMed  Google Scholar 

  258. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) J Comp Neurol 355:27–37

    Article  CAS  PubMed  Google Scholar 

  259. Nordahl CW, Braunschweig D, Iosif AM, Lee A, Rogers S, Ashwood P, Amaral DG, Van de Water J (2013) Brain Behav Immun 30:61–65. doi:10.1016/j.bbi.2013.01.084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  260. Nuber U, Schwarz SE, Scheffner M (1998) Eur J Biochem 254:643–649

    Article  CAS  PubMed  Google Scholar 

  261. O’Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, Coe BP, Levy R, Ko A, Lee C, Smith JD et al (2012) Nature 485:246–250. doi:10.1038/nature10989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  262. Oblak AL, Rosene DL, Kemper TL, Bauman ML, Blatt GJ (2011) Autism Res. doi:10.1002/aur.188

    PubMed  PubMed Central  Google Scholar 

  263. Ohnishi T, Matsuda H, Hashimoto T, Kunihiro T, Nishikawa M, Uema T, Sasaki M (2000) Brain 123(Pt 9):1838–1844

    Article  PubMed  Google Scholar 

  264. Ohno T, Maeda H, Murabe N, Kamiyama T, Yoshioka N, Mishina M, Sakurai M (2010) Proc Natl Acad Sci USA 107:15252–15257. doi:10.1073/pnas.0906551107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  265. Olde Loohuis NF, Kole K, Glennon JC, Karel P, Van der Borg G, Van Gemert Y, Van den Bosch D, Meinhardt J, Kos A, Shahabipour F et al (2015) Neurobiol Dis 80:42–53. doi:10.1016/j.nbd.2015.05.006

    Article  CAS  PubMed  Google Scholar 

  266. Olmos-Serrano JL, Paluszkiewicz SM, Martin BS, Kaufmann WE, Corbin JG, Huntsman MM (2010) J Neurosci 30:9929–9938. doi:10.1523/JNEUROSCI.1714-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  267. Osorio N, Alcaraz G, Padilla F, Couraud F, Delmas P, Crest M (2005) J Physiol 569:801–816. doi:10.1113/jphysiol.2005.097022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Ospina MB, Krebs Seida J, Clark B, Karkhaneh M, Hartling L, Tjosvold L, Vandermeer B, Smith V (2008) PLoS One 3:e3755. doi:10.1371/journal.pone.0003755

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  269. Ozkan ED, Creson TK, Kramar EA, Rojas C, Seese RR, Babyan AH, Shi Y, Lucero R, Xu X, Noebels JL et al (2014) Neuron 82:1317–1333. doi:10.1016/j.neuron.2014.05.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  270. Pagani M, Damiano M, Galbusera A, Tsaftaris SA, Gozzi A (2016) J Neurosci Methods 267:62–73. doi:10.1016/j.jneumeth.2016.04.007

    Article  PubMed  Google Scholar 

  271. Pagliardini S, Ren J, Wevrick R, Greer JJ (2005) Am J Pathol 167:175–191. doi:10.1016/S0002-9440(10)62964-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Pagnamenta AT, Wing K, Sadighi Akha E, Knight SJ, Bolte S, Schmotzer G, Duketis E, Poustka F, Klauck SM, Poustka A et al (2009) Eur J Hum Genet 17:687–692. doi:10.1038/ejhg.2008.228

    Article  CAS  PubMed  Google Scholar 

  273. Pan F, Aldridge GM, Greenough WT, Gan WB (2010) Proc Natl Acad Sci USA 107:17768–17773. doi:10.1073/pnas.1012496107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  274. Paronett EM, Meechan DW, Karpinski BA, LaMantia AS, Maynard TM (2015) Cereb Cortex 25:3977–3993. doi:10.1093/cercor/bhu285

    Article  PubMed  Google Scholar 

  275. Pasciuto E, Bagni C (2014) Cell 158(1446–1446):e1441. doi:10.1016/j.cell.2014.08.035

    Google Scholar 

  276. Paul LK, Van Lancker-Sidtis D, Schieffer B, Dietrich R, Brown WS (2003) Brain Lang 85:313–324

    Article  PubMed  Google Scholar 

  277. Peça J, Feliciano C, Ting JT, Wang WT, Wells MF, Venkatraman TN, Lascola CD, Fu ZY, Feng GP (2011) Nature 472:437–442. doi:10.1038/nature09965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  278. Peñagarikano O, Abrahams BS, Herman EI, Winden KD, Gdalyahu A, Dong H, Sonnenblick LI, Gruver R, Almajano J, Bragin A et al (2011) Cell 147:235–246. doi:10.1016/j.cell.2011.08.040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  279. Peñagarikano O, Lazaro MT, Lu XH, Gordon A, Dong H, Lam HA, Peles E, Maidment NT, Murphy NP, Yang XW et al (2015) Sci Transl Med 7(271r):a278. doi:10.1126/scitranslmed.3010257

    Google Scholar 

  280. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, Woolfrey KM (2011) Nat Neurosci 14:285–293. doi:10.1038/nn.2741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Peters SU, Kaufmann WE, Bacino CA, Anderson AW, Adapa P, Chu Z, Yallampalli R, Traipe E, Hunter JV, Wilde EA (2011) Dev Med Child Neurol 53:361–367. doi:10.1111/j.1469-8749.2010.03838.x

    Article  PubMed  Google Scholar 

  282. Phelps EA, LeDoux JE (2005) Neuron 48:175–187. doi:10.1016/j.neuron.2005.09.025

    Article  CAS  PubMed  Google Scholar 

  283. Pierce K, Haist F, Sedaghat F, Courchesne E (2004) Brain 127:2703–2716. doi:10.1093/brain/awh289

    Article  PubMed  Google Scholar 

  284. Pierce K, Muller RA, Ambrose J, Allen G, Courchesne E (2001) Brain 124:2059–2073

    Article  CAS  PubMed  Google Scholar 

  285. Piggot J, Kwon H, Mobbs D, Blasey C, Lotspeich L, Menon V, Bookheimer S, Reiss AL (2004) J Am Acad Child Adolesc Psychiatry 43:473–480. doi:10.1097/00004583-200404000-00014

    Article  PubMed  Google Scholar 

  286. Pinto D, Delaby E, Merico D, Barbosa M, Merikangas A, Klei L, Thiruvahindrapuram B, Xu X, Ziman R, Wang Z et al (2014) Am J Hum Genet 94:677–694. doi:10.1016/j.ajhg.2014.03.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. Platt RJ, Zhou Y, Slaymaker IM, Shetty AS, Weisbach NR, Kim JA, Sharma J, Desai M, Sood S, Kempton HR et al (2017) Cell Rep 19:335–350. doi:10.1016/j.celrep.2017.03.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  288. Pop AS, Levenga J, de Esch CE, Buijsen RA, Nieuwenhuizen IM, Li T, Isaacs A, Gasparini F, Oostra BA, Willemsen R (2014) Psychopharmacology 231:1227–1235. doi:10.1007/s00213-012-2947-y

    Article  CAS  PubMed  Google Scholar 

  289. Portmann T, Yang M, Mao R, Panagiotakos G, Ellegood J, Dolen G, Bader PL, Grueter BA, Goold C, Fisher E et al (2014) Cell Rep 7:1077–1092. doi:10.1016/j.celrep.2014.03.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  290. Puce A, Allison T, Bentin S, Gore JC, McCarthy G (1998) J Neurosci 18:2188–2199

    CAS  PubMed  Google Scholar 

  291. Pucilowska J, Vithayathil J, Tavares EJ, Kelly C, Karlo JC, Landreth GE (2015) J Neurosci 35:3190–3200. doi:10.1523/JNEUROSCI.4864-13.2015

    Article  CAS  PubMed  Google Scholar 

  292. Qureshi AY, Mueller S, Snyder AZ, Mukherjee P, Berman JI, Roberts TP, Nagarajan SS, Spiro JE, Chung WK, Sherr EH et al (2014) J Neurosci 34:11199–11211. doi:10.1523/JNEUROSCI.1366-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  293. Radyushkin K, Hammerschmidt K, Boretius S, Varoqueaux F, El-Kordi A, Ronnenberg A, Winter D, Frahm J, Fischer J, Brose N et al (2009) Genes Brain Behav 8:416–425. doi:10.1111/j.1601-183X.2009.00487.x

    Article  CAS  PubMed  Google Scholar 

  294. Ramocki MB, Peters SU, Tavyev YJ, Zhang F, Carvalho CM, Schaaf CP, Richman R, Fang P, Glaze DG, Lupski JR et al (2009) Ann Neurol 66:771–782. doi:10.1002/ana.21715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  295. Rausch A, Zhang W, Haak KV, Mennes M, Hermans EJ, van Oort E, van Wingen G, Beckmann CF, Buitelaar JK, Groen WB (2016) Mol Autism 7:13. doi:10.1186/s13229-015-0060-x

    Article  PubMed  PubMed Central  Google Scholar 

  296. Raymond GV, Bauman ML, Kemper TL (1996) Acta Neuropathol 91:117–119

    Article  CAS  PubMed  Google Scholar 

  297. Raza S, Harker A, Richards S, Kolb B, Gibb R (2015) Behav Brain Res 282:25–36. doi:10.1016/j.bbr.2014.12.055

    Article  CAS  PubMed  Google Scholar 

  298. Reith RM, McKenna J, Wu H, Hashmi SS, Cho SH, Dash PK, Gambello MJ (2013) Neurobiol Dis 51:93–103. doi:10.1016/j.nbd.2012.10.014

    Article  CAS  PubMed  Google Scholar 

  299. Richards C, Jones C, Groves L, Moss J, Oliver C (2015) Lancet Psychiatry 2:909–916. doi:10.1016/S2215-0366(15)00376-4

    Article  PubMed  Google Scholar 

  300. Rietveld L, Stuss DP, McPhee D, Delaney KR (2015) Front Cell Neurosci 9:145. doi:10.3389/fncel.2015.00145

    Article  PubMed  PubMed Central  Google Scholar 

  301. Rinaldi T, Silberberg G, Markram H (2008) Cereb Cortex 18:763–770. doi:10.1093/cercor/bhm117

    Article  PubMed  Google Scholar 

  302. Robinson L, Guy J, McKay L, Brockett E, Spike RC, Selfridge J, De Sousa D, Merusi C, Riedel G, Bird A et al (2012) Brain 135:2699–2710. doi:10.1093/brain/aws096

    Article  PubMed  PubMed Central  Google Scholar 

  303. Rodier PM, Ingram JL, Tisdale B, Nelson S, Romano J (1996) J Comp Neurol 370:247–261. doi:10.1002/(SICI)1096-9861(19960624)370:2<247:AID-CNE8>3.0.CO;2-2

    Article  CAS  PubMed  Google Scholar 

  304. Ronald A, Hoekstra RA (2011) Am J Med Genet B Neuropsychiatr Genet 156B:255–274. doi:10.1002/ajmg.b.31159

    Article  PubMed  Google Scholar 

  305. Rudelli RD, Brown WT, Wisniewski K, Jenkins EC, Laure-Kamionowska M, Connell F, Wisniewski HM (1985) Acta Neuropathol 67:289–295

    Article  CAS  PubMed  Google Scholar 

  306. Rumbaugh G, Adams JP, Kim JH, Huganir RL (2006) Proc Natl Acad Sci USA 103:4344–4351. doi:10.1073/pnas.0600084103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  307. Sabers A, Bertelsen FC, Scheel-Kruger J, Nyengaard JR, Moller A (2014) Neurosci Lett 580:12–16. doi:10.1016/j.neulet.2014.07.036

    Article  CAS  PubMed  Google Scholar 

  308. Sacco R, Gabriele S, Persico AM (2015) Psychiatry Res 234:239–251. doi:10.1016/j.pscychresns.2015.08.016

    Article  PubMed  Google Scholar 

  309. Sanders SJ, Murtha MT, Gupta AR, Murdoch JD, Raubeson MJ, Willsey AJ, Ercan-Sencicek AG, DiLullo NM, Parikshak NN, Stein JL et al (2012) Nature 485:237–241. doi:10.1038/nature10945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  310. Sandin S, Lichtenstein P, Kuja-Halkola R, Larsson H, Hultman CM, Reichenberg A (2014) JAMA 311:1770–1777. doi:10.1001/jama.2014.4144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  311. Santos M, Uppal N, Butti C, Wicinski B, Schmeidler J, Giannakopoulos P, Heinsen H, Schmitz C, Hof PR (2011) Brain Res 1380:206–217. doi:10.1016/j.brainres.2010.08.067

    Article  CAS  PubMed  Google Scholar 

  312. Sato M, Stryker MP (2010) Proc Natl Acad Sci USA 107:5611–5616. doi:10.1073/pnas.1001281107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  313. Sceniak MP, Lang M, Enomoto AC, Howell CJ, Hermes DJ, Katz DM (2016) Cereb Cortex 26:1938–1956. doi:10.1093/cercor/bhv002

    Article  PubMed  Google Scholar 

  314. Schaer M, Schmitt JE, Glaser B, Lazeyras F, Delavelle J, Eliez S (2006) Psychiatry Res 146:1–11. doi:10.1016/j.pscychresns.2005.10.002

    Article  PubMed  Google Scholar 

  315. Schmahmann JD, Weilburg JB, Sherman JC (2007) Cerebellum 6:254–267. doi:10.1080/14734220701490995

    Article  PubMed  Google Scholar 

  316. Schmitt JE, Vandekar S, Yi J, Calkins ME, Ruparel K, Roalf DR, Whinna D, Souders MC, Satterwaite TD, Prabhakaran K et al (2015) Biol Psychiatry 78:135–143. doi:10.1016/j.biopsych.2014.10.025

    Article  CAS  PubMed  Google Scholar 

  317. Schultz RT, Grelotti DJ, Klin A, Kleinman J, Van der Gaag C, Marois R, Skudlarski P (2003) Philos Trans R Soc Lond B Biol Sci 358:415–427. doi:10.1098/rstb.2002.1208

    Article  PubMed  PubMed Central  Google Scholar 

  318. Schumann CM, Amaral DG (2006) J Neurosci 26:7674–7679. doi:10.1523/JNEUROSCI.1285-06.2006

    Article  CAS  PubMed  Google Scholar 

  319. Schumann CM, Bloss CS, Barnes CC, Wideman GM, Carper RA, Akshoomoff N, Pierce K, Hagler D, Schork N, Lord C et al (2010) J Neurosci 30:4419–4427. doi:10.1523/JNEUROSCI.5714-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  320. Schumann CM, Nordahl CW (2011) Brain Res 1380:175–186. doi:10.1016/j.brainres.2010.09.061

    Article  CAS  PubMed  Google Scholar 

  321. Seeley WW (2010) Brain Struct Funct 214:465–475. doi:10.1007/s00429-010-0263-z

    Article  PubMed  PubMed Central  Google Scholar 

  322. Seeley WW, Allman JM, Carlin DA, Crawford RK, Macedo MN, Greicius MD, Dearmond SJ, Miller BL (2007) Alzheimer Dis Assoc Disord 21:S50–S57

    Article  PubMed  Google Scholar 

  323. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, Dearmond SJ (2006) Ann Neurol 60:660–667

    Article  PubMed  Google Scholar 

  324. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Nature 368:144–147. doi:10.1038/368144a0

    Article  CAS  PubMed  Google Scholar 

  325. Shi L, Smith SE, Malkova N, Tse D, Su Y, Patterson PH (2009) Brain Behav Immun 23:116–123. doi:10.1016/j.bbi.2008.07.012

    Article  PubMed  CAS  Google Scholar 

  326. Shinawi M, Liu P, Kang SH, Shen J, Belmont JW, Scott DA, Probst FJ, Craigen WJ, Graham BH, Pursley A et al (2010) J Med Genet 47:332–341. doi:10.1136/jmg.2009.073015

    Article  CAS  PubMed  Google Scholar 

  327. Simms ML, Kemper TL, Timbie CM, Bauman ML, Blatt GJ (2009) Acta Neuropathol 118:673–684. doi:10.1007/s00401-009-0568-2

    Article  PubMed  Google Scholar 

  328. Singer HS, Morris CM, Gause CD, Gillin PK, Crawford S, Zimmerman AW (2008) J Neuroimmunol 194:165–172. doi:10.1016/j.jneuroim.2007.11.004

    Article  CAS  PubMed  Google Scholar 

  329. Skefos J, Cummings C, Enzer K, Holiday J, Weed K, Levy E, Yuce T, Kemper T, Bauman M (2014) PLoS One 9:e81255. doi:10.1371/journal.pone.0081255

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  330. Smrt RD, Eaves-Egenes J, Barkho BZ, Santistevan NJ, Zhao C, Aimone JB, Gage FH, Zhao X (2007) Neurobiol Dis 27:77–89. doi:10.1016/j.nbd.2007.04.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  331. Snow WM, Hartle K, Ivanco TL (2008) Dev Psychobiol 50:633–639

    Article  PubMed  Google Scholar 

  332. Sosa-Diaz N, Bringas ME, Atzori M, Flores G (2014) Synapse 68:468–473. doi:10.1002/syn.21759

    Article  CAS  PubMed  Google Scholar 

  333. Soumiya H, Fukumitsu H, Furukawa S (2011) J Neurosci Res 89:1575–1585. doi:10.1002/jnr.22704

    Article  CAS  PubMed  Google Scholar 

  334. Sparks BF, Friedman SD, Shaw DW, Aylward EH, Echelard D, Artru AA, Maravilla KR, Giedd JN, Munson J, Dawson G et al (2002) Neurology 59:184–192

    Article  CAS  PubMed  Google Scholar 

  335. Srinivasan K, Leone DP, Bateson RK, Dobreva G, Kohwi Y, Kohwi-Shigematsu T, Grosschedl R, McConnell SK (2012) Proc Natl Acad Sci USA 109:19071–19078. doi:10.1073/pnas.1216793109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  336. Stark KL, Xu B, Bagchi A, Lai WS, Liu H, Hsu R, Wan X, Pavlidis P, Mills AA, Karayiorgou M et al (2008) Nat Genet 40:751–760. doi:10.1038/ng.138

    Article  CAS  PubMed  Google Scholar 

  337. Steinman KJ, Spence SJ, Ramocki MB, Proud MB, Kessler SK, Marco EJ, Green Snyder L, D’Angelo D, Chen Q, Chung WK et al (2016) Am J Med Genet A 170:2943–2955. doi:10.1002/ajmg.a.37820

    Article  CAS  PubMed  Google Scholar 

  338. Stephenson DT, O’Neill SM, Narayan S, Tiwari A, Arnold E, Samaroo HD, Du F, Ring RH, Campbell B, Pletcher M et al (2011) Mol Autism 2:7. doi:10.1186/2040-2392-2-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  339. Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E (2014) N Engl J Med 370:1209–1219. doi:10.1056/NEJMoa1307491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  340. Strauss KA, Puffenberger EG, Huentelman MJ, Gottlieb S, Dobrin SE, Parod JM, Stephan DA, Morton DH (2006) N Engl J Med 354:1370–1377. doi:10.1056/NEJMoa052773

    Article  CAS  PubMed  Google Scholar 

  341. Stuss DP, Boyd JD, Levin DB, Delaney KR (2012) PLoS One 7:e31896. doi:10.1371/journal.pone.0031896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  342. Su H, Fan W, Coskun PE, Vesa J, Gold JA, Jiang YH, Potluri P, Procaccio V, Acab A, Weiss JH et al (2011) Neurosci Lett 487:129–133. doi:10.1016/j.neulet.2009.06.079

    Article  CAS  PubMed  Google Scholar 

  343. Sugathan A, Biagioli M, Golzio C, Erdin S, Blumenthal I, Manavalan P, Ragavendran A, Brand H, Lucente D, Miles J et al (2014) Proc Natl Acad Sci USA 111:E4468–E4477. doi:10.1073/pnas.1405266111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  344. Sykes NH, Lamb JA (2007) Expert Rev Mol Med 9:1–15. doi:10.1017/S1462399407000452

    Article  PubMed  Google Scholar 

  345. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM, Südhof TC (2007) Science 318:71–76. doi:10.1126/science.1146221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  346. Takuma K, Hara Y, Kataoka S, Kawanai T, Maeda Y, Watanabe R, Takano E, Hayata-Takano A, Hashimoto H, Ago Y et al (2014) Pharmacol Biochem Behav 126:43–49. doi:10.1016/j.pbb.2014.08.013

    Article  CAS  PubMed  Google Scholar 

  347. Talkowski ME, Rosenfeld JA, Blumenthal I, Pillalamarri V, Chiang C, Heilbut A, Ernst C, Hanscom C, Rossin E, Lindgren AM et al (2012) Cell 149:525–537. doi:10.1016/j.cell.2012.03.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  348. Taneja P, Ogier M, Brooks-Harris G, Schmid DA, Katz DM, Nelson SB (2009) J Neurosci 29:12187–12195. doi:10.1523/JNEUROSCI.3156-09.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  349. Tang G, Gudsnuk K, Kuo SH, Cotrina ML, Rosoklija G, Sosunov A, Sonders MS, Kanter E, Castagna C, Yamamoto A et al (2014) Neuron 83:1131–1143. doi:10.1016/j.neuron.2014.07.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  350. Tang G, Gutierrez Rios P, Kuo SH, Akman HO, Rosoklija G, Tanji K, Dwork A, Schon EA, Dimauro S, Goldman J et al (2013) Neurobiol Dis 54:349–361. doi:10.1016/j.nbd.2013.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  351. Tavazoie SF, Alvarez VA, Ridenour DA, Kwiatkowski DJ, Sabatini BL (2005) Nat Neurosci 8:1727–1734. doi:10.1038/nn1566

    Article  CAS  PubMed  Google Scholar 

  352. Tetreault NA, Hakeem AY, Jiang S, Williams BA, Allman E, Wold BJ, Allman JM (2012) J Autism Dev Disord 42:2569–2584. doi:10.1007/s10803-012-1513-0

    Article  PubMed  Google Scholar 

  353. Till SM, Wijetunge LS, Seidel VG, Harlow E, Wright AK, Bagni C, Contractor A, Gillingwater TH, Kind PC (2012) Hum Mol Genet 21:2143–2156. doi:10.1093/hmg/dds030

    Article  CAS  PubMed  Google Scholar 

  354. Tiwari VN, Jeong JW, Wilson BJ, Behen ME, Chugani HT, Sundaram SK (2012) Neuroimage 59:349–355. doi:10.1016/j.neuroimage.2011.07.067

    Article  PubMed  Google Scholar 

  355. Tottenham N, Hare TA, Casey BJ (2009) A developmental perspective on human amygdala function. In: Whalen PJ, Phelps EA (eds) The human amygdala. The Guilford Press, New York, p 107

    Google Scholar 

  356. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M (2012) Nature 488:647–651. doi:10.1038/nature11310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  357. Turk AA, Brown WS, Symington M, Paul LK (2010) Neuropsychologia 48:43–50. doi:10.1016/j.neuropsychologia.2009.08.009

    Article  PubMed  Google Scholar 

  358. Uppal N, Gianatiempo I, Wicinski B, Schmeidler J, Heinsen H, Schmitz C, Buxbaum JD, Hof PR (2014) Mol Autism 5:17. doi:10.1186/2040-2392-5-17

    Article  PubMed  PubMed Central  Google Scholar 

  359. Uppal N, Puri R, Yuk F, Janssen WG, Bozdagi-Gunal O, Harony-Nicolas H, Dickstein DL, Buxbaum JD, Hof PR (2015) Mol Autism 6:41. doi:10.1186/s13229-015-0036-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  360. Uppal N, Wicinski B, Buxbaum JD, Heinsen H, Schmitz C, Hof PR (2014) J Neuropathol Exp Neurol 73:891–902. doi:10.1097/NEN.0000000000000108

    Article  PubMed  Google Scholar 

  361. van Amelsvoort T, Daly E, Henry J, Robertson D, Ng V, Owen M, Murphy KC, Murphy DG (2004) Arch Gen Psychiatry 61:1085–1096. doi:10.1001/archpsyc.61.11.1085

    Article  PubMed  Google Scholar 

  362. van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, Hof PR, van Engeland H, Schmitz C (2008) Brain 131:987–999. doi:10.1093/brain/awn033

    Article  PubMed  Google Scholar 

  363. Varea O, Martin-de-Saavedra MD, Kopeikina KJ, Schurmann B, Fleming HJ, Fawcett-Patel JM, Bach A, Jang S, Peles E, Kim E et al (2015) Proc Natl Acad Sci USA 112:6176–6181. doi:10.1073/pnas.1423205112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  364. Vismara LA, Colombi C, Rogers SJ (2009) Autism. 13:93–115. doi:10.1177/1362361307098516

    Article  PubMed  Google Scholar 

  365. Vogt BA, Berger GR, Derbyshire SW (2003) Eur J Neurosci 18:3134–3144. doi:10.1111/j.1460-9568.2003.03034.x

    Article  PubMed  PubMed Central  Google Scholar 

  366. von Economo C. Zschr ges Neurol Psychiatr. 1926:706-712

  367. Wahlsten D, Metten P, Crabbe JC (2003) Brain Res 971:47–54

    Article  CAS  PubMed  Google Scholar 

  368. Wallace ML, Burette AC, Weinberg RJ, Philpot BD (2012) Neuron 74:793–800. doi:10.1016/j.neuron.2012.03.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  369. Wang CC, Held RG, Chang SC, Yang L, Delpire E, Ghosh A, Hall BJ (2011) Neuron 72:789–805. doi:10.1016/j.neuron.2011.09.023

    Article  CAS  PubMed  Google Scholar 

  370. Wang IT, Reyes AR, Zhou Z (2013) Neurobiol Dis 58:3–12. doi:10.1016/j.nbd.2013.04.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  371. Wang X, Bey AL, Katz BM, Badea A, Kim N, David LK, Duffney LJ, Kumar S, Mague SD, Hulbert SW et al (2016) Nat Commun 7:11459. doi:10.1038/ncomms11459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  372. Wang X, McCoy PA, Rodriguiz RM, Pan Y, Je HS, Roberts AC, Kim CJ, Berrios J, Colvin JS, Bousquet-Moore D et al (2011) Hum Mol Genet 20:3093–3108. doi:10.1093/hmg/ddr212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  373. Wang X, Xu Q, Bey AL, Lee Y, Jiang YH (2014) Mol Autism 5:30. doi:10.1186/2040-2392-5-30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  374. Watanabe Y, Murakami T, Kawashima M, Hasegawa-Baba Y, Mizukami S, Imatanaka N, Akahori Y, Yoshida T, Shibutani M (2017) Neurotox Res 31:46–62. doi:10.1007/s12640-016-9660-2

    Article  CAS  PubMed  Google Scholar 

  375. Watson KK, Jones TK, Allman JM (2006) Neuroscience 141:1107–1112

    Article  CAS  PubMed  Google Scholar 

  376. Wegiel J, Flory M, Kuchna I, Nowicki K, Ma SY, Imaki H, Cohen IL, London E, Brown WT, Wisniewski T (2014) Acta Neuropathol Commun 2:28. doi:10.1186/2051-5960-2-28

    Article  PubMed  PubMed Central  Google Scholar 

  377. Wegiel J, Flory M, Kuchna I, Nowicki K, Ma SY, Imaki H, Frackowiak J, Kolecka BM, Wierzba-Bobrowicz T, London E et al (2015) Acta Neuropathol Commun 3:2. doi:10.1186/s40478-015-0183-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  378. Wegiel J, Flory M, Schanen NC, Cook EH, Nowicki K, Kuchna I, Imaki H, Ma SY, London E, Casanova MF et al (2015) Acta Neuropathol Commun 3:63. doi:10.1186/s40478-015-0241-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  379. Wegiel J, Kuchna I, Nowicki K, Imaki H, Marchi E, Ma SY, Chauhan A, Chauhan V, Bobrowicz TW, de Leon M et al (2010) Acta Neuropathol 119:755–770. doi:10.1007/s00401-010-0655-4

    Article  PubMed  PubMed Central  Google Scholar 

  380. Wegiel J, Kuchna I, Nowicki K, Imaki H, Wegiel J, Ma SY, Azmitia EC, Banerjee P, Flory M, Cohen IL et al (2013) Brain Res 1512:106–122. doi:10.1016/j.brainres.2013.03.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  381. Wei H, Ma Y, Ding C, Jin G, Liu J, Chang Q, Hu F, Yu L (2016) Neurochem Res 41:3129–3137. doi:10.1007/s11064-016-2035-5

    Article  CAS  PubMed  Google Scholar 

  382. Weidenheim KM, Goodman L, Dickson DW, Gillberg C, Rastam M, Rapin I (2001) J Child Neurol 16:809–819

    Article  CAS  PubMed  Google Scholar 

  383. Weir RK, Forghany R, Smith SE, Patterson PH, McAllister AK, Schumann CM, Bauman MD (2015) Brain Behav Immun 48:139–146. doi:10.1016/j.bbi.2015.03.009

    Article  CAS  PubMed  Google Scholar 

  384. Welchew DE, Ashwin C, Berkouk K, Salvador R, Suckling J, Baron-Cohen S, Bullmore E (2005) Biol Psychiatry 57:991–998. doi:10.1016/j.biopsych.2005.01.028

    Article  PubMed  Google Scholar 

  385. Whitney ER, Kemper TL, Rosene DL, Bauman ML, Blatt GJ (2008) J Neurosci Methods 168:42–47. doi:10.1016/j.jneumeth.2007.09.009

    Article  CAS  PubMed  Google Scholar 

  386. Whitney ER, Kemper TL, Rosene DL, Bauman ML, Blatt GJ (2009) J Neurosci Res 87:2245–2254. doi:10.1002/jnr.22056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  387. Williams RS, Hauser SL, Purpura DP, DeLong GR, Swisher CN (1980) Arch Neurol 37:749–753

    Article  CAS  PubMed  Google Scholar 

  388. Wilson BJ, Sundaram SK, Huq AH, Jeong JW, Halverson SR, Behen ME, Bui DQ, Chugani HT (2011) Pediatr Neurol 44:350–356. doi:10.1016/j.pediatrneurol.2010.12.002

    Article  PubMed  PubMed Central  Google Scholar 

  389. Wisniewski KE, Segan SM, Miezejeski CM, Sersen EA, Rudelli RD (1991) Am J Med Genet 38:476–480

    Article  CAS  PubMed  Google Scholar 

  390. Wu P, Teot L, Murdoch G, Monaghan-Nichols AP, McFadden K (2014) Pediatr Dev Pathol 17:386–392. doi:10.2350/13-11-1399-CR.1

    Article  PubMed  Google Scholar 

  391. Xu B, Hsu PK, Stark KL, Karayiorgou M, Gogos JA (2013) Cell 152:262–275. doi:10.1016/j.cell.2012.11.052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  392. Xu Y, Ye H, Shen Y, Xu Q, Zhu L, Liu J, Wu JY (2011) Protein Cell 2:647–655. doi:10.1007/s13238-011-1072-8

    Article  PubMed  PubMed Central  Google Scholar 

  393. Yan J, Oliveira G, Coutinho A, Yang C, Feng J, Katz C, Sram J, Bockholt A, Jones IR, Craddock N et al (2005) Mol Psychiatry 10:329–332. doi:10.1038/sj.mp.4001629

    Article  CAS  PubMed  Google Scholar 

  394. Yashiro K, Riday TT, Condon KH, Roberts AC, Bernardo DR, Prakash R, Weinberg RJ, Ehlers MD, Philpot BD (2009) Nat Neurosci 12:777–783. doi:10.1038/nn.2327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  395. Yasuda S, Sugiura H, Katsurabayashi S, Shimada T, Tanaka H, Takasaki K, Iwasaki K, Kobayashi T, Hino O, Yamagata K (2014) Sci Rep 4:5155. doi:10.1038/srep05155

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  396. Yi JJ, Berrios J, Newbern JM, Snider WD, Philpot BD, Hahn KM, Zylka MJ (2015) Cell 162:795–807. doi:10.1016/j.cell.2015.06.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  397. Zerbo O, Iosif AM, Walker C, Ozonoff S, Hansen RL, Hertz-Picciotto I (2013) J Autism Dev Disord 43:25–33. doi:10.1007/s10803-012-1540-x

    Article  PubMed  PubMed Central  Google Scholar 

  398. Zhou Y, Kaiser T, Monteiro P, Zhang X, Van der Goes MS, Wang D, Barak B, Zeng M, Li C, Lu C et al (2016) Neuron 89:147–162. doi:10.1016/j.neuron.2015.11.023

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are indebted to all of the families for generously donating postmortem brain specimens. Our work on autism is supported by the Seaver Foundation (to JDB and PRH), the Simons Foundation (Grant FA #345922 from Foundation Associates, LLC, to PRH), Autism Speaks (the Autism Celloidin Library Project to PRH), the Foundation for Prader–Willi Research (to PRH and MV) and the National Institutes of Health (Grants MH093725 and MH101584 to JDB and PRH). SDR is a Seaver fellow.

Author information

Author notes

  1. Merina Varghese and Neha Keshav contributed equally.

Authors and Affiliations

  1. Fishberg Department of Neuroscience, Icahn School of Medicine at Mount Sinai, Box 1639, One Gustave L. Levy Place, New York, NY, 10029, USA

    Merina Varghese, Neha Keshav, Sarah Jacot-Descombes, Tahia Warda, Bridget Wicinski, Dara L. Dickstein, Joseph D. Buxbaum & Patrick R. Hof

  2. Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Merina Varghese, Neha Keshav, Sarah Jacot-Descombes, Tahia Warda, Bridget Wicinski, Dara L. Dickstein, Joseph D. Buxbaum & Patrick R. Hof

  3. Seaver Autism Center for Research and Treatment, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Neha Keshav, Hala Harony-Nicolas, Silvia De Rubeis, Elodie Drapeau, Joseph D. Buxbaum & Patrick R. Hof

  4. Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Hala Harony-Nicolas, Silvia De Rubeis, Elodie Drapeau & Joseph D. Buxbaum

  5. Unit of Psychiatry, Department of Children and Teenagers, University Hospitals and School of Medicine, Geneva, CH-1205, Switzerland

    Sarah Jacot-Descombes

  6. Department of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, 20814, USA

    Dara L. Dickstein

Authors
  1. Merina Varghese
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neha Keshav
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah Jacot-Descombes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tahia Warda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bridget Wicinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dara L. Dickstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hala Harony-Nicolas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Silvia De Rubeis
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Elodie Drapeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Joseph D. Buxbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Patrick R. Hof
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MV and NK wrote the manuscript; SJ-D, HH-N, TW, BW, DLD, SDR, ED, JDB, and PRH provided content and revised the manuscript; all authors read and approved the final version.

Corresponding author

Correspondence to Patrick R. Hof.

Ethics declarations

Funding

This study was supported by the Seaver Foundation (JDB, PRH), the Simons Foundation Grant FA #345922 (PRH), Autism Speaks and the Autism Celloidin Library Project (PRH), the Foundation for Prader–Willi Research (to PRH and MV), and the National Institutes of Health Grants R01 MH093725 (JDB, PRH) and R01 MH101584 (JDB, PRH). SDR is a Seaver Fellow.

Conflict of interest

The authors declare that they have no conflict of interest.

Disclaimer

The opinions expressed herein are those of the authors and are not necessarily representative of those of the Uniformed Services University of the Health Sciences, the Department of Defense; or, the United States Army, Navy, or Air Force (DLD).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 532 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varghese, M., Keshav, N., Jacot-Descombes, S. et al. Autism spectrum disorder: neuropathology and animal models. Acta Neuropathol 134, 537–566 (2017). https://doi.org/10.1007/s00401-017-1736-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00401-017-1736-4

Keywords

Search

Navigation