Studying autism in rodent models: Reconciling endophenotypes with comorbidities

Frontiers in Human Neuroscience

Volumn , Issue JUL, 2013, Pages

  Argyropoulos, Andrew ^a   Gilby, Krista ^a   Hill Yardin, Elisa Llewellyn ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aggression; Anxiety; Autism; Epilepsy; Gastrointestinal function; Motor deficits; Sensory; Sleep

Indexed keywords

MEMBRANE PROTEIN; NEUROLIGIN; PROPIONIC ACID; SH3 AND MULTIPLE AMKYRIN REPEAT DOMAIN PROTEIN; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL BEHAVIOR; ANXIETY; AUTISM; BEHAVIOR CHANGE; BEHAVIOR CONTROL; CLINICAL FEATURE; COMORBIDITY; CONTACTIN ASSOCIATED PROTEIN LIKE 2 GENE; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; ENDOPHENOTYPE; ENVIRONMENTAL FACTOR; EXPERIMENTAL MODEL; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; HEREDITY; HUMAN; MOLECULAR PATHOLOGY; MOTOR DYSFUNCTION; NONHUMAN; PHENOTYPE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; RISK ASSESSMENT; RISK FACTOR; SEIZURE;

EID: 84933678850     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00417     Document Type: Review

References (124)

1. Allik, H., Larsson, J.O., and Smedje, H. (2006). Sleep patterns of school-age children with Asperger syndrome or high-functioning autism. J. Autism Dev. Disord. 36, 585-595.
2. Amiet, C., Gourfinkel-An, I., Bouzamondo, A., Tordjman, S., Baulac, M., Lechat, P., Mottron, L., and Cohen, D. (2008). Epilepsy in autism is associated with intellectual disability and gender: evidence from a meta-analysis. Biol. Psychiatry 64, 577-582.
3. Anderson, J.S., Druzgal, T.J., Froehlich, A., Dubray, M.B., Lange, N., Alexander, A.L., Abildskov, T., Nielsen, J.A., Cariello, A.N., Cooperrider, J.R., Bigler, E.D., and Lainhart, J.E. (2011). Decreased interhemispheric functional connectivity in autism. Cereb. Cortex 21, 1134-1146.
4. Anisman, H., Kelly, O., Hayley, S., Borowski, T., Merali, Z., and Mcintyre, D.C. (2000). Acoustic startle and fear-potentiated startle in rats selectively bred for fast and slow kindling rates: relation to monoamine activity. Eur. J. Neurosc. 12, 4405-4416.
5. Anisman, H., and Mcintyre, D.C. (2002). Conceptual, spatial, and cue learning in the Morris water maze in fast or slow kindling rats: attention deficit comorbidity. J. Neurosci. 22, 7809-7817.
6. Arons, M.H., Thynne, C.J., Grabrucker, A.M., Li, D., Schoen, M., Cheyne, J.E., Boeckers, T.M., Montgomery, J.M., and Garner, C.C. (2012). Autism-associated mutations in ProSAP2/Shank3 impair synaptic transmission and neurexin-neuroligin-mediated transsynaptic signaling. J. Neurosci. 32, 14966-14978.
7. Azarbar, A., Mcintyre, D.C., and Gilby, K.L. (2010). Caloric restriction alters seizure disposition and behavioral profiles in seizure-prone (fast) versus seizure-resistant (slow) rats. Behav. Neurosci. 124, 106-114.
8. Banko, M.L., Allen, K.M., Dolina, S., Neumann, P.E., and Seyfried, T.N. (1997). Genomic imprinting and audiogenic seizures in mice. Behav. Genet. 27, 465-475.
9. Baron, M.K., Boeckers, T.M., Vaida, B., Faham, S., Gingery, M., Sawaya, M.R., Salyer, D., Gundelfinger, E.D., and Bowie, J.U. (2006). An architectural framework that may lie at the core of the postsynaptic density. Science 311, 531-535.
10. Bennetto, L., Kuschner, E.S., and Hyman, S.L. (2007). Olfaction and taste processing in autism. Biol. Psychiatry 62, 1015-1021.
11. Berkel, S., Marshall, C.R., Weiss, B., Howe, J., Roeth, R., Moog, U., Endris, V., Roberts, W., Szatmari, P., Pinto, D., Bonin, M., Riess, A., Engels, H., Sprengel, R., Scherer, S.W., and Rappold, G.A. (2010). Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat. Genet. 42, 489-491.
12. Betancur, C. (2011). Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting. Brain Res. 1380, 42-77.
13. Betancur, C., Sakurai, T., and Buxbaum, J.D. (2009). The emerging role of synaptic cell512 adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci. 32, 402-412.
14. Blakemore, S.J., Tavassoli, T., Calo, S., Thomas, R.M., Catmur, C., Frith, U., and Haggard, P. (2006). Tactile sensitivity in Asperger syndrome. Brain Cogn. 61, 5-13.
15. Bonaglia, M.C., Giorda, R., Mani, E., Aceti, G., Anderlid, B.M., Baroncini, A., Pramparo, T., and Zuffardi, O. (2006). Identification of a recurrent breakpoint within the SHANK3 gene in the 22q13.3 deletion syndrome. J. Med. Genet. 43, 822-828.
16. Bourgeron, T. (2009). A synaptic trek to autism. Curr. Opin. Neurobiol. 19, 231-234.
17. Bozdagi, O., Sakurai, T., Papapetrou, D., Wang, X., Dickstein, D.L., Takahashi, N., Kajiwara, Y., Yang, M., Katz, A.M., Scattoni, M.L., Harris, M.J., Saxena, R., Silverman, J.L., Crawley, J.N., Zhou, Q., Hof, P.R., and Buxbaum, J.D. (2010). Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol. Autism 1, 15-15.
18. Brodkin, E.S. (2007). BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav. Brain Res. 176, 53-65.
19. Bromley, R.L., Mawer, G., Clayton-Smith, J., and Baker, G.A. (2008). Autism spectrum disorders following in utero exposure to antiepileptic drugs. Neurology 71, 1923-1924.
20. Buie, T., Fuchs, G.J., 3rd, Furuta, G.T., Kooros, K., Levy, J., Lewis, J.D., Wershil, B.K., and Winter, H. (2010). Recommendations for evaluation and treatment of common gastrointestinal problems in children with ASDs. Pediatrics 125 Suppl 1, S19-29.
21. Cascio, C., Mcglone, F., Folger, S., Tannan, V., Baranek, G., Pelphrey, K.A., and Essick, G. (2008). Tactile perception in adults with autism: a multidimensional psychophysical study. J. Autism Dev. Disord. 38, 127-137.
22. Chadman, K.K., Gong, S., Scattoni, M.L., Boltuck, S.E., Gandhy, S.U., Heintz, N., and Crawley, J.N. (2008). Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 1, 147-158.
23. Chakrabarti, B., Dudbridge, F., Kent, L., Wheelwright, S., Hill-Cawthorne, G., Allison, C., Banerjee-Basu, S., and Baron-Cohen, S. (2009). Genes related to sex steroids, neural growth, and social-emotional behavior are associated with autistic traits, empathy, and Asperger syndrome. Autism Res. 2, 157-177.
24. Chapman, A., Keane, P.E., Meldrum, B.S., Simiand, J., and Vernieres, J.C. (1982). Mechanism of anticonvulsant action of valproate. Prog. Neurobiol 19, 315-359.
25. Crawley, J.N. (2007). Mouse Behavioral Assays Relevant to the Symptoms of Autism. Brain Pathol. 17, 448-459.
26. Dakin, S., and Frith, U. (2005). Vagaries of visual perception in autism. Neuron 48, 497-507.
27. Dudova, I., Vodicka, J., Havlovicova, M., Sedlacek, Z., Urbanek, T., and Hrdlicka, M. (2011). Odor detection threshold, but not odor identification, is impaired in children with autism. Eur. Child Adolesc. Psychiatry 20, 333-340.
28. Durand, C.M., Betancur, C., Boeckers, T.M., Bockmann, J., Chaste, P., Fauchereau, F., Nygren, G., Rastam, M., Gillberg, I.C., Anckarsater, H., Sponheim, E., Goubran-Botros, H., Delorme, R., Chabane, N., Mouren-Simeoni, M.C., De Mas, P., Bieth, E., Roge, B., Heron, D., Burglen, L., Gillberg, C., Leboyer, M., and Bourgeron, T. (2007). Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 39, 25-27.
29. Ebert, D. H, and Greenberg M.E. (2013). Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493, 327-337.
30. Ekinci, O., Arman, A.R., Isik, U., Bez, Y., and Berkem, M. (2010). EEG abnormalities and epilepsy in autistic spectrum disorders: clinical and familial correlates. Epilepsy Behav. 17, 178-182.
31. Etherton, M., Foldy, C., Sharma, M., Tabuchi, K., Liu, X., Shamloo, M., Malenka, R.C., and Sudhof, T.C. (2011). Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proc. Natl. Acad. Sci. U S A.
32. Etherton, M.R., Blaiss, C.A., Powell, C.M., and Sudhof, T.C. (2009). Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. U S A 106, 17998-18003.
33. Frye, R.E., Melnyk, S., and Macfabe, D.F. (2013). Unique acyl-carnitine profiles are potential biomarkers for acquired mitochondrial disease in autism spectrum disorder. Transl. Psychiatry 3, e220.
34. Gandal, M.J., Edgar, J.C., Ehrlichman, R.S., Mehta, M., Roberts, T.P., and Siegel, S.J. (2010). Validating gamma oscillations and delayed auditory responses as translational biomarkers of autism. Biol. Psychiatry 68, 1100-1106.
35. Gershon, M.D., and Ratcliffe, E.M. (2004). Developmental biology of the enteric nervous system: pathogenesis of Hirschsprung's disease and other congenital dysmotilities. Semin. Pediatr. Surg. 13, 224-235.
36. Geschwind, D.H. (2009). Advances in autism. Annu. Rev. Med. 60, 367-380.
37. Geschwind, D.H. (2011). Genetics of autism spectrum disorders. Trends Cogn. Sci. 15, 409-416
38. Gilby, K.L. (2008). A new rat model for vulnerability to epilepsy and autism spectrum disorders. Epilepsia 49 Suppl 8, 108-110.
39. Gilby, K.L., Da Silva, A.G., and Mcintyre, D.C. (2005). Differential GABA(A) subunit expression following status epilepticus in seizure-prone and seizure-resistant rats: a putative mechanism for refractory drug response. Epilepsia 46 Suppl 5, 3-9.
40. Gilby, K.L., and O'brien, T.J. (2013). Epilepsy, autism, and neurodevelopment: Kindling a shared vulnerability? Epilepsy Behav. 26, 370-374.
41. Gilby, K.L., Thorne, V., Patey, A., and Mcintyre, D.C. (2007). Ruling out postnatal origins to attention-deficit/hyperactivity disorder (ADHD)-like behaviors in a seizure-prone rat strain. Behav. Neurosci. 121, 370-379.
42. Goldberg, E.M., and Coulter, D.A. (2013). Mechanisms of epileptogenesis: a convergence on neural circuit dysfunction. Nat Rev Neurosci.14, 337-349.
43. Gomot, M., Bernard, F.A., Davis, M.H., Belmonte, M.K., Ashwin, C., Bullmore, E.T., and Baron-Cohen, S. (2006). Change detection in children with autism: an auditory event594 related fMRI study. Neuroimage 29, 475-484.
44. Grabrucker, A. M, Schmeisser, M.J., Schoen, M., and Boeckers, T.M. (2011). Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol. 21, 594-603.
45. Hara, H. (2007). Autism and epilepsy: a retrospective follow-up study. Brain Dev. 29, 486-490
46. Hayashi, M.K., Tang, C., Verpelli, C., Narayanan, R., Stearns, M.H., Xu, R.M., Li, H., Sala, C., and Hayashi, Y. (2009). The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137, 159-171.
47. Herbert, M.R. (2011). SHANK3, the synapse, and autism. N. Engl. J. Med. 365, 173-175.
48. Helbig, I., Scheffer, I.E., Mulley, J.C., and Berkovic, S.F. (2008). Navigating the channels and beyond: unravelling the genetics of the epilepsies. Lancet Neurol. 7, 231-245.
49. Huett, A., Leong, J.M., Podolsky, D.K., and Xavier, R.J. (2009). The cytoskeletal scaffold Shank3 is recruited to pathogen-induced actin rearrangements. Exp. Cell Res. 315, 2001-2011.
50. Ibrahim, S.H., Voigt, R.G., Katusic, S.K., Weaver, A.L., and Barbaresi, W.J. (2009). Incidence of gastrointestinal symptoms in children with autism: a population-based study. Pediatrics 124, 680-686.
51. Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T.W., and Sudhof, T.C. (1997). Binding of neuroligins to PSD-95. Science 277, 1511-1515.
52. Jamain, S., Quach, H., Betancur, C., Rastam, M., Colineaux, C., Gillberg, I.C., Soderstrom, H., Giros, B., Leboyer, M., Gillberg, C., and Bourgeron, T. (2003). Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34, 27-29.
53. Jeste, S.S. (2011). The neurology of autism spectrum disorders. Curr. Opin. Neurol. 24, 132-139
54. Kanne, S.M., and Mazurek, M.O. (2011). Aggression in Children and Adolescents with ASD: Prevalence and Risk Factors. J. Autism Dev. Disord. 41, 926-937.
55. Karaki, S., Mitsui, R., Hayashi, H., Kato, I., Sugiya, H., Iwanaga, T., Furness, J.B., and Kuwahara, A. (2006). Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res. 324, 353-360.
56. Kim, K.C., Kim, P., Go, H.S., Choi, C.S., Yang, S.I., Cheong, J.H., Shin, C.Y., and Ko, K.H. (2011). The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol. Lett. 201, 137-142.
57. Krakowiak, P., Goodlin-Jones, B., Hertz-Picciotto, I., Croen, L.A., and Hansen, R.L. (2008). Sleep problems in children with autism spectrum disorders, developmental delays, and typical development: a population-based study. J. Sleep Res. 17, 197-206.
58. Krueger, D.D., Tuffy, L.P., Papadopoulos, T., and Brose, N. (2012). The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr. Opin. Neurobiol. 22, 412-422.
59. Kumar, R.A. (2010). SHANK2 redemption: another synaptic protein for mental retardation and autism. Clin. Genet. 78, 519-521.
60. Kwakye, L.D., Foss-Feig, J.H., Cascio, C.J., Stone, W.L., and Wallace, M.T. (2011). Altered auditory and multisensory temporal processing in autism spectrum disorders. Front. Integr. Neurosci. 4, 129.
61. Latham, K., Chung, S.T., Allen, P.M., Tavassoli, T., and Baron-Cohen, S. (2013). Spatial localisation in autism: evidence for differences in early cortical visual processing. Mol. Autism 4, 4.
62. Leekam, S.R., Nieto, C., Libby, S.J., Wing, L., and Gould, J. (2007). Describing the sensory abnormalities of children and adults with autism. J. Autism Dev. Disord. 37, 894-910.
63. Lim, C.E., Turner, L.H., and Heinrichs, S.C. (2007). Short-term social recognition memory deficit and atypical social and physiological stressor reactivity in seizure-susceptible El mice. Seizure 16, 59-68.
64. Macfabe, D.F., Cain, D.P., Rodriguez-Capote, K., Franklin, A.E., Hoffman, J.E., Boon, F., Taylor, A.R., Kavaliers, M., and Ossenkopp, K.P. (2007). Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav. Brain Res. 176, 149-169.
65. Macfabe, D.F., Cain, N.E., Boon, F., Ossenkopp, K.P., and Cain, D.P. (2011). Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder. Behav. Brain Res. 217, 47-54.
66. Malow, B.A., Marzec, M.L., Mcgrew, S.G., Wang, L., Henderson, L.M., and Stone, W.L. (2006). Characterizing sleep in children with autism spectrum disorders: a multidimensional approach. Sleep 29, 1563-1571.
67. Markram, K., Rinaldi, T., La Mendola, D., Sandi, C., and Markram, H. (2008). Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 33, 901-912.
68. Mcfadyen-Leussis, M.P., and Heinrichs, S.C. (2005). Seizure-prone EL/Suz mice exhibit physical and motor delays and heightened locomotor activity in response to novelty during development. Epilepsy and Behavior 6, 312-319.
69. Mcfarlane, H.G., Kusek, G.K., Yang, M., Phoenix, J.L., Bolivar, V.J., and Crawley, J.N. (2008). Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 7, 152-163.
70. Mcintyre, D.C., Kelly, M.E., a nd Dufresne, C. (1999). FAST and SLOW amygdala kindling rat strains: comparison of amygdala, hippocampal, piriform and perirhinal cortex kindling. Epilepsy Res. 35, 197-209.
71. Meador, K.J., Baker, G.A., Finnell, R.H., Kalayjian, L.A., Liporace, J.D., Loring, D.W., Mawer, G., Pennell, P.B., Smith, J.C., Wolff, M.C., and Group, N.S. (2006). In utero antiepileptic drug exposure: fetal death and malformations. Neurology 67, 407-412.
72. Meidenbauer, J.J., Mantis, J.G., and Seyfried, T.N. (2011). The EL mouse: a natural model of autism and epilepsy. Epilepsia 52, 347-357.
73. Meyer, G., Varoqueaux, F., Neeb, A., Oschlies, M., and Brose, N. (2004). The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology 47, 724-733.
74. Morin, C.L., Dolina, S., Robertson, R.T., and Ribak, C.E. (1994). An inbred epilepsy-prone substrain of BALB/c mice shows absence of the corpus callosum, an abnormal projection to the basal forebrain, and bilateral projections to the thalamus. Cereb. Cortex (New York, N.Y.: 1991) 4, 119-128.
75. Moy, S.S., Nadler, J.J., Poe, M.D., Nonneman, R.J., Young, N.B., Koller, B.H., Crawley, J.N., Duncan, G.E., and Bodfish, J.W. (2008). Development of a mouse test for repetitive, restricted behaviors: relevance to autism. Behav. Brain Res. 188, 178-194.
76. Mulle, J.G., Sharp, W.G., and Cubells, J.F. (2013). The gut microbiome: a new frontier in autism research. Curr. Psychiatry Rep. 15, 337.
77. Neal, K.B., Parry, L.J., and Bornstein, J.C. (2009). Strain-specific genetics, anatomy and function of enteric neural serotonergic pathways in inbred mice. J. Physiol. 587, 567-586
78. Nesslinger, N.J., Gorski, J.L., Kurczynski, T.W., Shapira, S.K., Siegel-Bartelt, J., Dumanski, J.P., Cullen, R.F., Jr., French, B.N., and Mcdermid, H.E. (1994). Clinical, cytogenetic, and molecular characterization of seven patients with deletions of chromosome 22q13.3. Am. J. Hum. Genet. 54, 464-472.
79. Nutt, D.J., and Lister, R.G. (1988). Strain differences in response to a benzodiazepine receptor inverse agonist (FG 7142) in mice. Psychopharmacology 94, 335-336.
80. Parmeggiani, A., Barcia, G., Posar, A., Raimondi, E., Santucci, M., and Scaduto, M.C. (2010). Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders. Brain Dev 32, 783-789.
81. Parracho, H.M., Bingham, M.O., Gibson, G.R., and Mccartney, A.L. (2005). Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. J. Med. Microbiol. 54, 987-991.
82. Pearson, B.L., Pobbe, R.L., Defensor, E.B., Oasay, L., Bolivar, V.J., Blanchard, D.C., and Blanchard, R.J. (2011). Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism. Genes. Brain Behav. 10, 228-235.
83. Peca, J., Feliciano, C., Ting, J.T., Wang, W., Wells, M.F., Venkatraman, T.N., Lascola, C.D., Fu, Z., and Feng, G. (2011). Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472, 437-442.
84. Penagarikano, O., Abrahams, B.S., Herman, E.I., Winden, K.D., Gdalyahu, A., Dong, H., Sonnenblick, L.I., Gruver, R., Almajano, J., Bragin, A., Golshani, P., Trachtenberg, J.T., Peles, E., and Geschwind, D.H. (2011). Absence of CNTNAP2 Leads to Epilepsy, Neuronal Migration Abnormalities, and Core Autism-Related Deficits. Cell 147, 235-246.
85. Pobbe, R.L., Defensor, E.B., Pearson, B.L., Bolivar, V.J., Blanchard, D.C., and Blanchard, R.J. (2011). General and social anxiety in the BTBR T+ tf/J mouse strain. Behav. Brain Res. 216, 446-451.
86. Pouw, L. B., Rieffe, C., Oosterveld, P., Huskens, B., and Stockmann, L. (2013). Reactive/proactive aggression and affective/cognitive empathy in children with ASD. Res. Dev. Disabil. 34, 1256-1266.
87. Raab, M., Boeckers, T.M., and Neuhuber, W.L. (2010). Proline-rich synapse-associated protein-1 and 2 (ProSAP1/Shank2 and ProSAP2/Shank3)-scaffolding proteins are also present in postsynaptic specializations of the peripheral nervous system. Neuroscience.171, 421-33.
88. Racine, R.J., Steingart, M., and Mcintyre, D.C. (1999). Development of kindling-prone and kindling-resistant rats: selective breeding and electrophysiological studies. Epilepsy Res. 35, 183-195.
89. Rasalam, A.D., Hailey, H., Williams, J.H., Moore, S.J., Turnpenny, P.D., Lloyd, D.J., and Dean, J.C. (2005). Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev. Med. Child Neurol. 47, 551-555.
90. Reinhart, C.J., Mcintyre, D.C., Metz, G.A., and Pellis, S.M. (2006). Play fighting between kindling-prone (FAST) and kindling-resistant (SLOW) rats. J. Comp. Psychol. 120, 19-30.
91. Reinhart, C.J., Pellis, S.M., and Mcintyre, D.C. (2004). Development of play fighting in kindling-prone (FAST) and kindling-resistant (SLOW) rats: how does the retention of phenotypic juvenility affect the complexity of play? Dev. Psychobiol. 45, 83-92.
92. Rinehart, N.J., Tonge, B.J., Iansek, R., Mcginley, J., Brereton, A.V., Enticott, P.G., and Bradshaw, J.L. (2006). Gait function in newly diagnosed children with autism: Cerebellar and basal ganglia related motor disorder. Dev. Med. Child Neurol. 48, 819-824
93. Roberts, R.R., Murphy, J.F., Young, H.M., and Bornstein, J.C. (2007). Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G930-938.
94. Robertson, C., Kravitz, D., Freyberg, J., Baron-Cohen, S., and Baker, C. (2013). Tunnel Vision: Sharper Gradient of Spatial Attention in Autism. J. Neurosci. 33, 6676-6681.
95. Rogawski, M.A., and Loscher, W. (2004). The neurobiology of antiepileptic drugs. Nat. Rev. Neurosci. 5, 553-564.
96. Roullet, F.I., Wollaston, L., Decatanzaro, D., and Foster, J.A. (2010). Behavioral and molecular changes in the mouse in response to prenatal exposure to the anti-epileptic drug valproic acid. Neuroscience 170, 514-522.
97. Ryan, B.C., Young, N.B., Crawley, J.N., Bodfish, J.W., and Moy, S.S. (2010). Social deficits, stereotypy and early emergence of repetitive behavior in the C58/J inbred mouse strain. Behav. Brain Res. 208, 178-188.
98. Sansa, G., Carlson, C., Doyle, W., Weiner, H.L., Bluvstein, J., Barr, W., and Devinsky, O. (2011). Medically refractory epilepsy in autism. Epilepsia 52, 1071-1075.
99. Schmeisser, M.J., Ey, E., Wegener, S., Bockmann, J., Stempel, A.V., Kuebler, A., Janssen, A.L., Udvardi, P.T., Shiban, E., Spilker, C., Balschun, D., Skryabin, B.V., Dieck, S., Smalla, K.H., Montag, D., Leblond, C.S., Faure, P., Torquet, N., Le Sourd, A.M., Toro, R., Grabrucker, A.M., Shoichet, S.A., Schmitz, D., Kreutz, M.R., Bourgeron, T., Gundelfinger, E.D., and Boeckers, T.M. (2012). Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 486, 256-260.
100. Schneider, T., and Przewlocki, R. (2005). Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30, 80-89.
101. Shoji, H., and Kato, K. (2009). Maternal care affects the development of maternal behavior in inbred mice. Dev. Psychobiol. 51, 345-357.
102. Shultz, S.R., Macfabe, D.F., Martin, S., Jackson, J., Taylor, R., Boon, F., Ossenkopp, K.P., and Cain, D.P. (2009). Intracerebroventricular injections of the enteric bacterial metabolic product propionic a cid impair cognition and sensorimotor ability in the Long-Evans rat: further development of a rodent model of autism. Behav. Brain. Res. 200, 33-41.
103. Shultz, S.R., Macfabe, D.F., Ossenkopp, K.P., Scratch, S., Whelan, J., Taylor, R., and Cain, D.P. (2008). Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 54, 901-911.
104. Silverman, J.L., Yang, M., Lord, C., and Crawley, J.N. (2010a). Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 11, 490-502.
105. Silverman, J.L., Yang, M., Turner, S.M., Katz, A.M., Bell, D.B., Koenig, J.I., and Crawley, J.N. (2010b). Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism. Neuroscience 171, 1197-1208.
106. Sobrian, S.K., and Nandedkar, A.K. (1986). Prenatal antiepileptic drug exposure alters seizure susceptibility in rats. Pharmacol. Biochem. Behav. 24, 1383-1391.
107. Strauss, K.A., Puffenberger, E.G., Huentelman, M.J., Gottlieb, S., Dobrin, S.E., Parod, J.M., Stephan, D.A., and Morton, D.H. (2006). Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2. N. Engl. J. Med. 354, 1370-1377.
108. Sudhof, T.C. (2008). Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911.
109. Tabuchi, K., Blundell, J., Etherton, M.R., Hammer, R.E., Liu, X., Powell, C.M., and Südhof, T.C. (2007). A Neuroligin-3 Mutation Implicated in Autism Increases Inhibitory Synaptic Transmission in Mice. Science 318, 71-76.
110. Thomas, R.H., Foley, K.A., Mepham, J.R., Tichenoff, L.J., Possmayer, F., and Macfabe, D.F. (2010). Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J. Neurochem. 113, 515-529.
111. Todorova, M.T., Burwell, T.J., and Seyfried, T.N. (1999). Environmental risk factors for multifactorial epilepsy in EL mice. Epilepsia 40, 1697-1707.
112. Tsujino, N., Nakatani, Y., Seki, Y., Nakasato, A., Nakamura, M., Sugawara, M., and Arita, H. (2007). Abnormality of circadian rhythm accompanied by an increase in frontal cortex serotonin in animal model of autism. Neurosci Res 57, 289-295.
113. Turner, L.H., Lim, C.E., and Heinrichs, S.C. (2007). Antisocial and seizure susceptibility phenotypes in an animal model of epilepsy are normalized by impairment of brain corticotropin-releasing factor. Epilepsy Behav. 10, 8-15.
114. Valicenti-Mcdermott, M., Mcvicar, K., Rapin, I., Wershil, B.K., Cohen, H., and Shinnar, S. (2006). Frequency of gastrointestinal symptoms in children with autistic spectrum disorders and association with family history of autoimmune disease. J. Dev. Behav. Pediatr. 27, S128-136.
115. Van Steensel, F.J., Bogels, S.M., and Perrin, S. (2011). Anxiety disorders in children and adolescents with autistic spectrum disorders: a meta-analysis. Clin. Child Fam. Psychol. Rev. 14, 302-317.
116. Velez, L., Sokoloff, G., Miczek, K.A., Palmer, A.A., and Dulawa, S.C. (2010). Differences in aggressive behavior and DNA copy number variants between BALB/cJ and BALB/cByJ substrains. Behav. Genet. 40, 201-210.
117. Verpelli, C., and Sala, C. (2012). Molecular and synaptic defects in intellectual disability syndromes. Curr. Opin. Neurobiol. 22, 530-536.
118. Wagner, G.C., Reuhl, K.R., Cheh, M., Mcrae, P., and Halladay, A.K. (2006). A new neurobehavioral model of autism in mice: pre-and postnatal exposure to sodium valproate. J. Autism Dev. Dis. 36, 779-793.
119. Wang, L.W., Tancredi, D.J., and Thomas, D.W. (2011a). The prevalence of gastrointestinal problems in children across the United States with autism spectrum disorders from families with multiple affected members. J. Dev. Behav. Pediatr. 32, 351-360.
120. Wang, X., Mccoy, P.A., Rodriguiz, R.M., Pan, Y., Je, H.S., Roberts, A.C., Kim, C.J., Berrios, J., Colvin, J.S., Bousquet-Moore, D., Lorenzo, I., Wu, G., Weinberg, R.J., Ehlers, M.D., Philpot, B.D., Beaudet, A.L., Wetsel, W.C., and Jiang, Y.H. (2011b). Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 20, 3093-3108.
121. Won, H., Lee, H.R., Gee, H.Y., Mah, W., Kim, J.I., Lee, J., Ha, S., Chung, C., Jung, E.S., Cho, Y.S., Park, S.G., Lee, J.S., Lee, K., Kim, D., Bae, Y.C., Kaang, B.K., Lee, M.G., and Kim, E. (2012). Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 486, 261-265.
122. Woolfenden, S., Sarkozy, V., Ridley, G., Coory, M., and Williams, K. (2012). A systematic review of two outcomes in autism spectrum disorder-epilepsy and mortality. Dev. Med. Child Neurol. 54, 306-312.
123. Xu, B., Mcintyre, D.C., Fahnestock, M., and Racine, R.J. (2004). Strain differences affect the induction of status epilepticus and seizure-induced morphological changes. Eur. J. Neurosci. 20, 403-418.
124. Zhang, Q., Wang, J., Li, A., Liu, H., Zhang, W., Cui, X., and Wang, K. (2013). Expression of neurexin and neuroligin in the enteric nervous system and their down-regulated expression levels in Hirschsprung disease. Mol Biol Rep. 40, 2969-2975.