Advertisement

Rodent Models of Autism, Epigenetics, and the Inescapable Problem of Animal Constraint

  • Garet P. Lahvis
Part of the Advances in Behavior Genetics book series (AIBG)

Abstract

Autism spectrum disorder (ASD) is characterized by deficits in social interaction, delays and impairments in communication, and restricted interests and repetitive behaviors. ASD is highly heritable, indicating genetic causal factors, but its rising prevalence also suggests environmental changes, such as expanding numbers of chemical pollutants. Putative risk factors for ASD include various environmental factors and mutations in any one of over 19,000 human genes.

To identify risk factors, scientists apply statistical approaches to identify factors associated with ASD, then employ laboratory animals, commonly rodents, to ascertain whether the association indicates a causal relationship. If a mouse strain with a targeted mutation or chemical exposure expresses autistic-like phenotypes, it can be used as a “mouse model of autism” to elucidate causal mechanisms and develop drug treatments. Such approaches were successfully employed to understand Retts and Fragile-X syndromes, disabilities sharing features with autism. This review describes the social features of ASD and their behavioral analogues in laboratory rodents. It also describes the genetic and chemical risk factors associated with ASD and the underlying epigenetic processes mediating their influence on brain development and social behavior.

Epigenetic processes are powerfully affected by life experience. Natural environments offer rodents a complex array of choices, contingencies, rewards, and punishments. By contrast, standard laboratory cages and so-called “enriched” cages offer rodents sparse spatial and temporal variation, precluding variety of affective experience or opportunity to exercise their naturally evolved capacities for decision-making. Paucity of life experience can irreversibly obstruct development and run at cross-purposes with efforts to identify risk factors and treatments for ASD. Alternatives to standard laboratory animal caging will be explored.

Keywords

Autism Spectrum Disorder Autism Spectrum Disorder Autism Diagnostic Observation Schedule Aryl Hydrocarbon Receptor BTBR Mouse 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abrahams, B. S., & Geschwind, D. H. (2008). Advances in autism genetics: On the threshold of a new neurobiology. Nature Reviews Genetics, 9(5), 341–355.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alberti, A., Pirrone, P., Elia, M., Waring, R. H., & Romano, C. (1999). Sulphation deficit in “low-functioning” autistic children: A pilot study. Biological Psychiatry, 46(3), 420–424.PubMedCrossRefGoogle Scholar
  3. Allan, A. M., Liang, X., Luo, Y., Pak, C., Li, X., Szulwach, K. E., et al. (2008). The loss of methyl-CpG binding protein 1 leads to autism-like behavioral deficits. Human Molecular Genetics, 17(13), 2047–2057.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Andres, C. (2002). Molecular genetics and animal models in autistic disorder. Brain Research Bulletin, 57(1), 109–119.PubMedCrossRefGoogle Scholar
  5. Ashwin, C., Baron-Cohen, S., Wheelwright, S., O’Riordan, M., & Bullmore, E. T. (2007). Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome. Neuropsychologia, 45(1), 2–14.PubMedCrossRefGoogle Scholar
  6. Ashwood, P., Schauer, J., Isaac, N., Pessah, I. N., & Van de Water, J. (2009). Preliminary evidence of the in vitro effects of BDE-47 on innate immune responses in children with autism spectrum disorders. Journal of Neuroimmunology, 208, 130–135.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., et al. (2011). Experience modulates vicarious freezing in rats: A model for empathy. Stress and Cognition, 6, 17.Google Scholar
  8. Auger, A. P., Jessen, H. M., & Edelmann, M. N. (2011). Epigenetic organization of brain sex differences and juvenile social play behavior. Hormones and Behavior, 59(3), 358–363.PubMedCrossRefGoogle Scholar
  9. Auger, A. P., & Olesen, K. M. (2009). Brain sex differences and the organisation of juvenile social play behaviour. Journal of Neuroendocrinology, 21(6), 519–525.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Autism Genome Project Consortium, Szatmari, P., Paterson, A. D., Zwaigenbaum, L., Roberts, W., Brian, J., et al. (2007). Mapping autism risk loci using genetic linkage and chromosomal rearrangements. .[erratum appears in Nat Genet. 2007 Oct;39(10):1285 Note: Meyer, Kacie J [added]; Koop, Frederike [corrected to Koop, Frederieke]; Langemeijer, Marjolijn [corrected to Langemeijer, Marjolein]; Hijimans, Channa [corrected to Hijmans, Channa]]. Nature Genetics, 39(3), 319–328.CrossRefGoogle Scholar
  11. Baccarelli, A., & Bollati, V. (2009). Epigenetics and environmental chemicals. Current Opinion in Pediatrics, 21(2), 243.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bacon, A., Fein, D., Morris, R., Waterhouse, L., & Allen, D. (1998). The responses of autistic children to the distress of others. Journal of Autism and Developmental Disorders, 28(2), 129–142.PubMedCrossRefGoogle Scholar
  13. Bailey, A., Le Couteur, A., Gottesman, I., Bolton, P., Simonoff, E., Yuzda, E., et al. (1995). Autism as a strongly genetic disorder: Evidence from a British twin study. Psychological Medicine, 25(01), 63–77.PubMedCrossRefGoogle Scholar
  14. Baio, J. (2012). Prevalence of Autism Spectrum Disorders—Autism and Developmental Disabilities Monitoring Network, 14 Sites, United States, 2008. MMWR Surveillance Summaries, 61(3), 1–19.Google Scholar
  15. Bardo, M., Klebaur, J., Valone, J., & Deaton, C. (2001). Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology, 155(3), 278–284.PubMedCrossRefGoogle Scholar
  16. Baron-Cohen, S., Campbell, R., Karmiloff-Smith, A., Grant, J., & Walker, J. (1995). Are children with autism blind to the mentalistic significance of the eyes? British Journal of Developmental Psychology, 13(4), 379–398. doi: 10.1111/j.2044-835X.1995.tb00687.x.CrossRefGoogle Scholar
  17. Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient: An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34(2), 163–175. doi: 10.1023/b:jadd.0000022607.19833.00.PubMedCrossRefGoogle Scholar
  18. Barrett, S., Beck, J. C., Bernier, R., Bisson, E., Braun, T. A., Casavant, T. L., et al. (1999). An autosomal genomic screen for autism. Collaborative linkage study of autism. American Journal of Medical Genetics, 88(6), 609–615.PubMedCrossRefGoogle Scholar
  19. Bartal, I. B.-A., Decety, J., & Mason, P. (2011). Empathy and pro-social behavior in rats. Science, 334(6061), 1427–1430.PubMedCentralCrossRefGoogle Scholar
  20. Bartal, I. B.-A., Rodgers, D. A., Sarria, M. S. B., Decety, J., & Mason, P. (2014). Pro-social behavior in rats is modulated by social experience. Elife, 3, e01385.Google Scholar
  21. Basu, N., Scheuhammer, A. M., Bursian, S. J., Elliott, J., Rouvinen-Watt, K., & Chan, H. M. (2007). Mink as a sentinel species in environmental health. Environmental Research, 103(1), 130–144.PubMedCrossRefGoogle Scholar
  22. Bellini, E., Pavesi, G., Barbiero, I., Bergo, A., Chandola, C., Nawaz, M. S., et al. (2014). MeCP2 post-translational modifications: A mechanism to control its involvement in synaptic plasticity and homeostasis? Frontiers in Cellular Neuroscience, 8, 236.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Belmonte, M. K., Allen, G., Beckel-Mitchener, A., Boulanger, L. M., Carper, R. A., & Webb, S. J. (2004). Autism and abnormal development of brain connectivity. Journal of Neuroscience, 24(42), 9228–9231.PubMedCrossRefGoogle Scholar
  24. Bennett, E. L., Rosenzweig, M. R., & Diamond, M. C. (1969). Rat brain: Effects of environmental enrichment on wet and dry weights. Science, 163(3869), 825–826.PubMedCrossRefGoogle Scholar
  25. Benson, A. D., Burket, J. A., & Deutsch, S. I. (2013). Balb/c mice treated with d-cycloserine arouse increased social interest in conspecifics. Brain Research Bulletin, 99, 95–99.PubMedCrossRefGoogle Scholar
  26. Berg, J. M., & Geschwind, D. H. (2012). Autism genetics: Searching for specificity and convergence. Genome Biology, 13(7), 247. doi: 10.1186/gb-2012-1113-1187-1247.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bertrand, J., Mars, A., Boyle, C., Bove, F., Yeargin-Allsopp, M., & Decoufle, P. (2001). Prevalence of autism in a United States population: The Brick Township, New Jersey, investigation. Pediatrics, 108(5), 1155–1161.PubMedCrossRefGoogle Scholar
  28. Beura, L. K., Hamilton, S. E., Bi, K., Schenkel, J. M., Odumade, O. A., Casey, K. A., et al. (2016). Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature, 532, 512–516.PubMedCrossRefGoogle Scholar
  29. Bishop, S. L., & Lahvis, G. P. (2011). The autism diagnosis in translation: Shared affect in children and mouse models of ASD. Autism Research, 4(5), 317–335.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Bjeldanes, L. F., Kim, J. Y., Grose, K. R., Bartholomew, J. C., & Bradfield, C. A. (1991). Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: Comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proceedings of the National Academy of Sciences, 88(21), 9543–9547.CrossRefGoogle Scholar
  31. Black, J. E., Sirevaag, A. M., & Greenough, W. T. (1987). Complex experience promotes capillary formation in young rat visual cortex. Neuroscience Letters, 83(3), 351–355.PubMedCrossRefGoogle Scholar
  32. Blanchard, R. J., Dulloog, L., Markham, C., Nishimura, O., Compton, J. N., Jun, A., et al. (2001). Sexual and aggressive interactions in a visible burrow system with provisioned burrows. Physiology & Behavior, 72(1), 245–254.CrossRefGoogle Scholar
  33. Bohacek, J., Gapp, K., Saab, B. J., & Mansuy, I. M. (2013). Transgenerational epigenetic effects on brain functions. Biological Psychiatry, 73(4), 313–320.PubMedCrossRefGoogle Scholar
  34. Bollati, V., Baccarelli, A., Hou, L., Bonzini, M., Fustinoni, S., Cavallo, D., et al. (2007). Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Research, 67(3), 876–880.PubMedCrossRefGoogle Scholar
  35. Bourgeron, T. (2009). A synaptic trek to autism. Current Opinion in Neurobiology, 19(2), 231–234. doi: 10.1016/j.conb.2009.06.003.PubMedCrossRefGoogle Scholar
  36. Bourgeron, T. (2012). Genetics and epigenetics of autism spectrum disorders. In C. Paolo Sassone & C. Yves (Eds.), Epigenetics, brain and behavior (pp. 105–132). Berlin: Springer.CrossRefGoogle Scholar
  37. Branchi, I. (2009). The mouse communal nest: Investigating the epigenetic influences of the early social environment on brain and behavior development. Neuroscience & Biobehavioral Reviews, 33(4), 551–559. doi: 10.1016/j.neubiorev.2008.03.011.CrossRefGoogle Scholar
  38. Branchi, I., & Alleva, E. (2006). Communal nesting, an early social enrichment, increases the adult anxiety-like response and shapes the role of social context in modulating the emotional behavior. Behavioural Brain Research, 172(2), 299–306.PubMedCrossRefGoogle Scholar
  39. Branchi, I., D’Andrea, I., Fiore, M., Di Fausto, V., Aloe, L., & Alleva, E. (2006). Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biological Psychiatry, 60(7), 690–696. doi: 10.1016/j.biopsych.2006.01.005.PubMedCrossRefGoogle Scholar
  40. Branchi, I., Santucci, D., Vitale, A., & Alleva, E. (1998). Ultrasonic vocalizations by infant laboratory mice: A preliminary spectrographic characterization under different conditions. Developmental Psychobiology, 33(3), 249–256.PubMedCrossRefGoogle Scholar
  41. Brechbühl, J., Moine, F., Klaey, M., Nenniger-Tosato, M., Hurni, N., Sporkert, F., et al. (2013). Mouse alarm pheromone shares structural similarity with predator scents. Proceedings of the National Academy of Sciences, 110(12), 4762–4767.CrossRefGoogle Scholar
  42. Bredy, T., Humpartzoomian, R., Cain, D., & Meaney, M. (2003). Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience, 118(2), 571–576.PubMedCrossRefGoogle Scholar
  43. Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J. (2004). Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. European Journal of Neuroscience, 20(5), 1355–1362.PubMedCrossRefGoogle Scholar
  44. Brodkin, E. S. (2008). Social behavior phenotypes in fragile X syndrome, autism, and the Fmr1 knockout mouse: Theoretical comment on McNaughton et al. (2008). Behavioral Neuroscience, 122(2), 483–489.PubMedCrossRefGoogle Scholar
  45. Brokken, L. J. S., Lundberg-Giwercman, Y., Rajpert-De Meyts, E., Eberhard, J., Stahl, O., Cohn-Cedermark, G., et al. (2013). Association between polymorphisms in the aryl hydrocarbon receptor repressor gene and disseminated testicular germ cell cancer. Frontiers in Endocrinology, 4, 4.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Budimirovic, D. B., & Kaufmann, W. E. (2011). What can we learn about autism from studying fragile X syndrome? Developmental Neuroscience, 33(5), 379.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Burbach, K. M., Poland, A., & Bradfield, C. A. (1992). Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proceedings of the National Academy of Sciences, 89(17), 8185–8189.CrossRefGoogle Scholar
  48. Burgdorf, J., Panksepp, J., Brudzynski, S. M., Kroes, R., & Moskal, J. R. (2005). Breeding for 50-kHz positive affective vocalization in rats. Behavior Genetics, 35(1), 67–72.PubMedCrossRefGoogle Scholar
  49. Bussey, C., de Leeuw, A., Cook, R., Ashley, Z., Schofield, J., & Lamberts, R. (2014). Dual implantation of a radio-telemeter and vascular access port allows repeated hemodynamic and pharmacological measures in conscious lean and obese rats. Laboratory Animals, 48(3), 250–260.PubMedCrossRefGoogle Scholar
  50. Buxbaum, J., Silverman, J., Smith, C., Greenberg, D., Kilifarski, M., Reichert, J., et al. (2002). Association between a GABRB3 polymorphism and autism. Molecular Psychiatry, 7(3), 311–316.PubMedCrossRefGoogle Scholar
  51. Carden, S. E., Bortot, A. T., & Hofer, M. A. (1993). Ultrasonic vocalizations are elicited from rat pups in the home cage by pentylenetetrazol and U50,488, but not naltrexone. Behavioral Neuroscience, 107(5), 851–859.PubMedCrossRefGoogle Scholar
  52. Carlier, P., & Jamon, M. (2006). Observational learning in C57BL/6j mice. Behavioural Brain Research, 174(1), 125–131.PubMedCrossRefGoogle Scholar
  53. Carney, R. M., Wolpert, C. M., Ravan, S. A., Shahbazian, M., Ashley-Koch, A., Cuccaro, M. L., et al. (2003). Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatric Neurology, 28(3), 205–211.PubMedCrossRefGoogle Scholar
  54. Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T., Qin, J., et al. (2008). MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320(5880), 1224–1229.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Champagne, F. A., Weaver, I. C., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology, 147(6), 2909–2915.PubMedCrossRefGoogle Scholar
  56. Chang, H., Wan, Y., Wu, S., Fan, Z., & Hu, J. (2011). Occurrence of androgens and progestogens in wastewater treatment plants and receiving river waters. Comparison to Estrogens, 45(2), 732–740.Google Scholar
  57. Chao, H.-T., & Zoghbi, H. Y. (2012). MeCP2: Only 100 % will do. Nature Neuroscience, 15(2), 176–177.PubMedCrossRefGoogle Scholar
  58. Cheadle, J. P., Gill, H., Fleming, N., Maynard, J., Kerr, A., Leonard, H., et al. (2000). Long-read sequence analysis of the MECP2 gene in Rett syndrome patients: Correlation of disease severity with mutation type and location. Human Molecular Genetics, 9(7), 1119–1129.PubMedCrossRefGoogle Scholar
  59. Chen, Q., Panksepp, J. B., & Lahvis, G. P. (2009). Empathy is moderated by genetic background in mice. PLoS One [Electronic Resource], 4(2), e4387.CrossRefGoogle Scholar
  60. Cheslack-Postava, K., Rantakokko, P. V., Hinkka-Yli-Salomäki, S., Surcel, H.-M., McKeague, I. W., Kiviranta, H. A., et al. (2013). Maternal serum persistent organic pollutants in the Finnish Prenatal Study of Autism: A pilot study. Neurotoxicology and Teratology, 38, 1–5.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16(4), 231–239.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Chien, W.-H., Gau, S. S.-F., Chen, C.-H., Tsai, W.-C., Wu, Y.-Y., Chen, P.-H., et al. (2013). Increased gene expression of FOXP1 in patients with autism spectrum disorders. Molecular Autism, 4(1), 23.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Chi-Tai, Y., & Gow-Chin, Y. (2003). Effects of phenolic acids on human phenolsulfotransferases in relation to their antioxidant activity. Journal of Agricultural and Food Chemistry, 26(51), 1474–1479.Google Scholar
  64. Choi, K. D., Lee, J. S., Lee, J. O., Oh, K. S., & Shin, I. S. (2009). Investigation of domoic acid in shellfish collected from Korean fish retail outlets. Food Science and Biotechnology, 18(4), 842–848.Google Scholar
  65. Chourbaji, S., Hörtnagl, H., Molteni, R., Riva, M., Gass, P., & Hellweg, R. (2012). The impact of environmental enrichment on sex-specific neurochemical circuitries–effects on brain-derived neurotrophic factor and the serotonergic system. Neuroscience, 220, 267–276.PubMedCrossRefGoogle Scholar
  66. Chun-Hua, L., Chien-Chang, C., Chih-Ming, C., Chen-Yu, W., Chia-Chi, H., Julia, Y. C., et al. (2009). Knockdown of the aryl hydrocarbon receptor attenuates excitotoxicity and enhances NMDA-induced BDNF expression in cortical neurons. Journal of Neurochemistry, 111(3), 777–789.CrossRefGoogle Scholar
  67. Clark, T. F., Winkielman, P., & McIntosh, D. N. (2008). Autism and the extraction of emotion from briefly presented facial expressions: Stumbling at the first step of empathy. Emotion, 8(6), 803–809.PubMedCrossRefGoogle Scholar
  68. Colle, L., Baron-Cohen, S., Wheelwright, S., & Lely, H. J. (2008). Narrative discourse in adults with high-functioning autism or Asperger syndrome. Journal of Autism and Developmental Disorders, 38(1), 28–40. doi: 10.1007/s10803-007-0357-5.PubMedCrossRefGoogle Scholar
  69. Collins, R. L. (1988). Observational learning of a left-right behavioral asymmetry in mice (Mus musculus). Journal of Comparative Psychology, 102(3), 222–224.PubMedCrossRefGoogle Scholar
  70. Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., et al. (1997). Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits. Proceedings of the National Academy of Sciences of the United States of America, 94(10), 5401–5404.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Cook, E. H., Jr., Lindgren, V., Leventhal, B. L., Courchesne, R., Lincoln, A., Shulman, C., et al. (1997). Autism or atypical autism in maternally but not paternally derived proximal 15q duplication. American Journal of Human Genetics, 60(4), 928.PubMedPubMedCentralGoogle Scholar
  72. Courchesne, E., & Pierce, K. (2005). Why the frontal cortex in autism might be talking only to itself: Local over-connectivity but long-distance disconnection. Current Opinion in Neurobiology, 15(2), 225–230. doi: 10.1016/j.conb.2005.03.001.PubMedCrossRefGoogle Scholar
  73. Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999). Genetics of mouse behavior: Interactions with laboratory environment. Science, 284(5420), 1670–1672. doi: 10.1126/science.284.5420.1670.PubMedCrossRefGoogle Scholar
  74. Crawley, J. N. (2012). Translational animal models of autism and neurodevelopmental disorders. Dialogues in Clinical Neuroscience, 14(3), 293.PubMedPubMedCentralGoogle Scholar
  75. Cromwell, H. C., Johnson, A., McKnight, L., Horinek, M., Asbrock, C., Burt, S., et al. (2007). Effects of polychlorinated biphenyls on maternal odor conditioning in rat pups. Physiology & Behavior, 91(5), 658–666.CrossRefGoogle Scholar
  76. Crowcroft, P. (1966). Mice all over. London: Foulis.Google Scholar
  77. Crowcroft, P., & Rowe, F. P. (1963). Social organization and territorial behaviour in the wild house mouse (Mus musculus L.). Proceedings of the Zoological Society of London, 140, 517–531.CrossRefGoogle Scholar
  78. Curley, J. P., Davidson, S., Bateson, P., & Champagne, F. A. (2009). Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Frontiers in Behavioral Neuroscience, 3, 25. doi: 10.3389/neuro.08.025.2009.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Curran, S., Powell, J., Neale, B., Dworzynski, K., Li, T., Murphy, D., et al. (2006). An association analysis of candidate genes on chromosome 15 q11-13 and autism spectrum disorder. Molecular Psychiatry, 11(8), 709–713.PubMedCrossRefGoogle Scholar
  80. D’Amato, F. R., Scalera, E., Sarli, C., & Moles, A. (2005). Pups call, mothers rush: Does maternal responsiveness affect the amount of ultrasonic vocalizations in mouse pups? Behavior Genetics, 35(1), 103–112.PubMedCrossRefGoogle Scholar
  81. D’Andrea, I., Alleva, E., & Branchi, I. (2007). Communal nesting, an early social enrichment, affects social competences but not learning and memory abilities at adulthood. Behavioural Brain Research, 183(1), 60–66.PubMedCrossRefGoogle Scholar
  82. Dastur, F. N., McGregor, I. S., & Brown, R. E. (1999). Dopaminergic modulation of rat pup ultrasonic vocalizations. European Journal of Pharmacology, 382(2), 53–67.PubMedCrossRefGoogle Scholar
  83. Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., et al. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–283.PubMedCrossRefGoogle Scholar
  84. Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27(3), 403–424.PubMedCrossRefGoogle Scholar
  85. de Marchena, A., & Eigsti, I.-M. (2010). Conversational gestures in autism spectrum disorders: Asynchrony but not decreased frequency. Autism Research, 3(6), 311–322. doi: 10.1002/aur.159.PubMedCrossRefGoogle Scholar
  86. De Waard, W. J., Aarts, J. M. M. J. G., Peijnenburg, A. C. M., De Kok, T. M. C. M., Van Schooten, F.-J., & Hoogenboom, L. A. P. (2008). Ah receptor agonist activity in frequently consumed food items. Food Additives & Contaminants: Part A: Chemistry, Analysis, Control, Exposure & Risk Assessment, 25(6), 779–787.CrossRefGoogle Scholar
  87. Del Arco, A., Segovia, G., Garrido, P., de Blas, M., & Mora, F. (2007). Stress, prefrontal cortex and environmental enrichment: Studies on dopamine and acetylcholine release and working memory performance in rats. Behavioural Brain Research, 176(2), 267–273.PubMedCrossRefGoogle Scholar
  88. Diehl, J. (2008). Prosody comprehension in high-functioning autism. Dissertation Abstracts International: Section B: The Sciences and Engineering.Google Scholar
  89. Diehl, J., Bennetto, L., & Young, E. C. (2006). Story recall and narrative coherence of high-functioning children with autism spectrum disorders. Journal of Abnormal Child Psychology, 34(1), 83–98. doi: 10.1007/s10802-005-9003-x.CrossRefGoogle Scholar
  90. Dolen, G., Darvishzadeh, A., Huang, K. W., & Malenka, R. C. (2013). Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature, 501(7466), 179–184.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Donaldson, Z. R., & Young, L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science, 322(5903), 900–904.PubMedCrossRefGoogle Scholar
  92. Dudley, K. J., Li, X., Kobor, M. S., Kippin, T. E., & Bredy, T. W. (2011). Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders. Neuroscience & Biobehavioral Reviews, 35(7), 1544–1551. doi: 10.1016/j.neubiorev.2010.12.016.CrossRefGoogle Scholar
  93. Duffy, S. N., Craddock, K. J., Abel, T., & Nguyen, P. V. (2001). Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learning and Memory, 8(1), 26–34.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Durkin, M. S., Maenner, M. J., Newschaffer, C. J., Lee, L.-C., Cunniff, C. M., Daniels, J. L., et al. (2008). Advanced parental age and the risk of autism spectrum disorder. American Journal of Epidemiology, 168(11), 1268–1276.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ehret, G., & Bernecker, C. (1986). Low-frequency sound communication by mouse pups (Mus musculus): Wriggling calls release maternal behavior. Animal Behaviour, 34(3), 821–830.CrossRefGoogle Scholar
  96. El Rawas, R., Thiriet, N., Lardeux, V., Jaber, M., & Solinas, M. (2009). Environmental enrichment decreases the rewarding but not the activating effects of heroin. Psychopharmacology, 203(3), 561–570.PubMedCrossRefGoogle Scholar
  97. Enstrom, A. M., Lit, L., Onore, C. E., Gregg, J. P., Hansen, R. L., Pessah, I. N., et al. (2009). Altered gene expression and function of peripheral blood natural killer cells in children with autism. Brain, Behavior, and Immunity, 23(1), 124–133.PubMedCrossRefGoogle Scholar
  98. Escorihuela, R. M., Tobeña, A., & Fernández-Teruel, A. (1994). Environmental enrichment reverses the detrimental action of early inconsistent stimulation and increases the beneficial effects of postnatal handling on shuttlebox learning in adult rats. Behavioural Brain Research, 61(2), 169–173.PubMedCrossRefGoogle Scholar
  99. Faherty, C. J., Shepherd, K. R., Herasimtschuk, A., & Smeyne, R. J. (2005). Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Molecular Brain Research, 134(1), 170–179.PubMedCrossRefGoogle Scholar
  100. Fatemi, S. H., Stary, J. M., Halt, A. R., & Realmuto, G. R. (2001). Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. Journal of Autism and Developmental Disorders, 31(6), 529–535.PubMedCrossRefGoogle Scholar
  101. Forbes-Lorman, R. M., Rautio, J. J., Kurian, J. R., Auger, A. P., & Auger, C. J. (2012). Neonatal MeCP2 is important for the organization of sex differences in vasopressin expression. Epigenetics, 7(3), 230–238.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Forgays, D. G., & Forgays, J. W. (1952). The nature of the effect of free-environmental experience in the rat. Journal of Comparative and Physiological Psychology, 45(4), 322.PubMedCrossRefGoogle Scholar
  103. Fox, G. A. (2001). Wildlife as sentinels of human health effects in the Great Lakes—St. Lawrence basin. Environmental Health Perspectives, 109(Suppl. 6), 853.PubMedPubMedCentralGoogle Scholar
  104. Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002). Environmental enrichment reverses the effects of maternal separation on stress reactivity. The Journal of Neuroscience, 22(18), 7840–7843.PubMedGoogle Scholar
  105. Fukuchi, M., Nii, T., Ishimaru, N., Minamino, A., Hara, D., Takasaki, I., et al. (2009). Valproic acid induces up-or down-regulation of gene expression responsible for the neuronal excitation and inhibition in rat cortical neurons through its epigenetic actions. Neuroscience Research, 65(1), 35–43.PubMedCrossRefGoogle Scholar
  106. Fyffe, S. L., Neul, J. L., Samaco, R. C., Chao, H.-T., Ben-Shachar, S., Moretti, P., et al. (2008). Deletion of Mecp2 in Sim1-expressing neurons reveals a critical role for MeCP2 in feeding behavior, aggression, and the response to stress. Neuron, 59(6), 947–958.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Gascon, M., Vrijheid, M., Martinez, D., Forns, J., Grimalt, J. O., Torrent, M., et al. (2011). Effects of pre and postnatal exposure to low levels of polybromodiphenyl ethers on neurodevelopment and thyroid hormone levels at 4 years of age. Environment International, 37(3), 605–611. doi: 10.1016/j.envint.2010.12.005.PubMedCrossRefGoogle Scholar
  108. Galef, B. G. (2013). Imitation and local enhancement: Detrimental effects of consensus definitions on analyses of social learning in animals. Behavioural Processes, 100, 123–130.PubMedCrossRefGoogle Scholar
  109. Geier, D. A., Kern, J. K., Garver, C. R., Adams, J. B., Audhya, T., Nataf, R., et al. (2009a). Biomarkers of environmental toxicity and susceptibility in autism. Journal of the Neurological Sciences, 280(1–2), 101–108.PubMedCrossRefGoogle Scholar
  110. Geier, D. A., Kern, J. K., Garver, C. R., Adams, J. B., Audhya, T., & Geier, M. R. (2009b). A prospective study of transsulfuration biomarkers in autistic disorders. [Erratum appears in Neurochem Res 2009 Feb;34(2):394]. Neurochemical Research, 34(2), 386–393.PubMedCrossRefGoogle Scholar
  111. Gernsbacher, M. A., Stevenson, J. L., Khandakar, S., & Goldsmith, H. H. (2008). Why does joint attention look atypical in autism? Child Development Perspectives, 2(1), 38–45. doi: 10.1111/j.1750-8606.2008.00039.x.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Geschwind, D. H., & Levitt, P. (2007). Autism spectrum disorders: Developmental disconnection syndromes. Current Opinion in Neurobiology, 17(1), 103–111.PubMedCrossRefGoogle Scholar
  113. Gipson, C., Beckmann, J., El-Maraghi, S., Marusich, J., & Bardo, M. (2011). Effect of environmental enrichment on escalation of cocaine self-administration in rats. Psychopharmacology, 214(2), 557–566. doi: 10.1007/s00213-010-2060-z.PubMedCrossRefGoogle Scholar
  114. Glickman, G. (2010). Circadian rhythms and sleep in children with autism. Neuroscience & Biobehavioral Reviews, 34(5), 755–768.CrossRefGoogle Scholar
  115. Globus, A., Rosenzweig, M. R., Bennett, E. L., & Diamond, M. C. (1973). Effects of differential experience on dendritic spine counts in rat cerebral cortex. Journal of Comparative and Physiological Psychology, 82(2), 175.PubMedCrossRefGoogle Scholar
  116. Goldberg, N. R., Fields, V., Pflibsen, L., Salvatore, M. F., & Meshul, C. K. (2012). Social enrichment attenuates nigrostriatal lesioning and reverses motor impairment in a progressive 1-methyl-2-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) mouse model of Parkinson’s disease. Neurobiology of Disease, 45(3), 1051–1067.PubMedCrossRefGoogle Scholar
  117. Goldberg, N., Haack, A., & Meshul, C. (2011). Enriched environment promotes similar neuronal and behavioral recovery in a young and aged mouse model of Parkinson’s disease. Neuroscience, 172, 443–452.PubMedCrossRefGoogle Scholar
  118. Grabrucker, A. M. (2012). Environmental factors in autism. Frontiers in Psychiatry, 3, 118.PubMedGoogle Scholar
  119. Gracceva, G., Venerosi, A., Santucci, D., Calamandrei, G., & Ricceri, L. (2009). Early social enrichment affects responsiveness to different social cues in female mice. Behavioural Brain Research, 196(2), 304–309.PubMedCrossRefGoogle Scholar
  120. Grafodatskaya, D., Chung, B., Szatmari, P., & Weksberg, R. (2010). Autism spectrum disorders and epigenetics. Journal of the American Academy of Child and Adolescent Psychiatry, 49(8), 794–809.PubMedCrossRefGoogle Scholar
  121. Grandjean, P., & Landrigan, P. J. (2006). Developmental neurotoxicity of industrial chemicals. The Lancet, 368(9553), 2167–2178.CrossRefGoogle Scholar
  122. Green, T. A., Alibhai, I. N., Roybal, C. N., Winstanley, C. A., Theobald, D. E., Birnbaum, S. G., et al. (2010). Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biological Psychiatry, 67(1), 28–35.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Greenough, W. T., Hwang, H., & Gorman, C. (1985). Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proceedings of the National Academy of Sciences, 82(13), 4549–4552.CrossRefGoogle Scholar
  124. Greenough, W. T., Volkmar, F. R., & Juraska, J. M. (1973). Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Experimental Neurology, 41(2), 371–378.PubMedCrossRefGoogle Scholar
  125. Gregg, J. P., Lit, L., Baron, C. A., Hertz-Picciotto, I., Walker, W., Davis, R. A., et al. (2008). Gene expression changes in children with autism. Genomics, 91(1), 22–29.PubMedCrossRefGoogle Scholar
  126. Gregory, S. G., Connelly, J. J., Towers, A. J., Johnson, J., Biscocho, D., Markunas, C. A., et al. (2009). Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Medicine, 7(1), 62.PubMedPubMedCentralCrossRefGoogle Scholar
  127. Guilarte, T. R., Toscano, C. D., McGlothan, J. L., & Weaver, S. A. (2003). Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Annals of Neurology, 53(1), 50–56.PubMedCrossRefGoogle Scholar
  128. Guy, J., Cheval, H., Selfridge, J., & Bird, A. (2011). The role of MeCP2 in the brain. Annual Review of Cell and Developmental Biology, 27, 631–652.PubMedCrossRefGoogle Scholar
  129. Guzman, Y. F., Tronson, N. C., Guedea, A., Huh, K. H., Gao, C., & Radulovic, J. (2009). Social modeling of conditioned fear in mice by non-fearful conspecifics. Behavioural Brain Research, 201(1), 173–178.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Hackam, D. G., & Redelmeier, D. A. (2006). Translation of research evidence from animals to humans. JAMA, 296(14), 1727–1732. doi: 10.1001/jama.296.14.1731.CrossRefGoogle Scholar
  131. Hadjikhani, N., Joseph, R. M., Manoach, D. S., Naik, P., Snyder, J., Dominick, K., et al. (2009). Body expressions of emotion do not trigger fear contagion in autism spectrum disorder. Social Cognitive and Affective Neuroscience, 4(1), 70–78.PubMedPubMedCentralCrossRefGoogle Scholar
  132. Hagerman, R. J., Berry-Kravis, E., Kaufmann, W. E., Ono, M. Y., Tartaglia, N., Lachiewicz, A., et al. (2009). Advances in the treatment of fragile X syndrome. Pediatrics, 123(1), 378–390.PubMedPubMedCentralCrossRefGoogle Scholar
  133. Hagerman, R. J., Jackson, A. W., 3rd, Levitas, A., Rimland, B., & Braden, M. (1986). An analysis of autism in fifty males with the fragile X syndrome. American Journal of Medical Genetics, 23(1–2), 359–374.PubMedCrossRefGoogle Scholar
  134. Hall, L., & Kelley, E. (2013). The contribution of epigenetics to understanding genetic factors in autism. Autism, 18(8), 872–881.PubMedCrossRefGoogle Scholar
  135. Halladay, A. K., Amaral, D., Aschner, M., Bolivar, V. J., Bowman, A., DiCicco-Bloom, E., et al. (2009). Animal models of autism spectrum disorders: Information for neurotoxicologists. Neurotoxicology, 30(5), 811–821.PubMedPubMedCentralCrossRefGoogle Scholar
  136. Hallmayer, J., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., et al. (2011). Genetic heritability and shared environmental factors among twin pairs with autism. Archives of General Psychiatry, 68(11), 1095–1102.PubMedPubMedCentralCrossRefGoogle Scholar
  137. Hamilton, S. M., Spencer, C. M., Harrison, W. R., Yuva-Paylor, L. A., Graham, D. F., Daza, R. A. M., et al. (2011). Multiple autism-like behaviors in a novel transgenic mouse model. Behavioural Brain Research, 218(1), 29–41. doi: 10.1016/j.bbr.2010.11.026.PubMedCrossRefGoogle Scholar
  138. Harmon, K. M., Cromwell, H. C., Burgdorf, J., Moskal, J. R., Brudzynski, S. M., Kroes, R. A., et al. (2008). Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation. Developmental Psychobiology, 50(4), 322–331.PubMedCrossRefGoogle Scholar
  139. Harper, P. A., Wong, J. M. Y., Lam, M. S. M., & Okey, A. B. (2002). Polymorphisms in the human AH receptor. Chemico-Biological Interactions, 141(1–2), 161–187. doi: 10.1016/S0009-2797(02)00071-6.PubMedCrossRefGoogle Scholar
  140. Harris, S. W., Hessl, D., Goodlin-Jones, B., Ferranti, J., Bacalman, S., Barbato, I., et al. (2008). Autism profiles of males with fragile X syndrome. American Journal on Mental Retardation, 113(6), 427–438.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Hertz-Picciotto, I., Park, H. Y., Dostal, M., Kocan, A., Trnovec, T., & Sram, R. (2008). Prenatal exposures to persistent and non-persistent organic compounds and effects on immune system development. Basic & Clinical Pharmacology & Toxicology, 102(2), 146–154.CrossRefGoogle Scholar
  142. Hoffman, M. L. (1975). Developmental synthesis of affect and cognition and its interplay for altruistic motivation. Developmental Psychology, 11, 607–622.CrossRefGoogle Scholar
  143. Hogart, A., Nagarajan, R. P., Patzel, K. A., Yasui, D. H., & LaSalle, J. M. (2007). 15q11-13 GABAA receptor genes are normally biallelically expressed in brain yet are subject to epigenetic dysregulation in autism-spectrum disorders. Human Molecular Genetics, 16(6), 691–703.PubMedPubMedCentralCrossRefGoogle Scholar
  144. Hooper, K., She, J., Sharp, M., Chow, J., Jewell, N., Gephart, R., et al. (2007). Depuration of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in breast milk from California first-time mothers (Primiparae). Environmental Health Perspectives, 115(9), 1271–1275.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Hu, V. W., Frank, B. C., Heine, S., Lee, N. H., & Quackenbush, J. (2006). Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics, 7(1), 118.PubMedPubMedCentralCrossRefGoogle Scholar
  146. Hu, Q., Franklin, J. N., Bryan, I., Morris, E., Wood, A., & DeWitt, J. C. (2012). Does developmental exposure to perflurooctanoic acid (PFOA) induce immunopathologies commonly observed in neurodevelopmental disorders? Neurotoxicology, 33(6), 1491–1498. doi: 10.1016/j.neuro.2012.10.016.PubMedCrossRefGoogle Scholar
  147. Hu, V. W., Sarachana, T., Kim, K. S., Nguyen, A., Kulkarni, S., Steinberg, M. E., et al. (2009). Gene expression profiling differentiates autism case–controls and phenotypic variants of autism spectrum disorders: Evidence for circadian rhythm dysfunction in severe autism. Autism Research, 2(2), 78–97.PubMedPubMedCentralCrossRefGoogle Scholar
  148. Hubert, B., Wicker, B., Moore, D., Monfardini, E., Duverger, H., Da Fonseca, D., et al. (2007a). Brief report: Recognition of emotional and non-emotional biological motion in individuals with autistic spectrum disorders. Journal of Autism and Developmental Disorders, 37(7), 1386–1392.PubMedCrossRefGoogle Scholar
  149. Hubert, B., Wicker, B., Moore, D., Monfardini, E., Duverger, H., Da Fonseca, D., et al. (2007b). “Brief report: Recognition of emotional and non-emotional biological motion in individuals with autistic spectrum disorders”: Erratum. Journal of Autism and Developmental Disorders, 37(7), 1393.CrossRefGoogle Scholar
  150. Humphreys, K., Minshew, N., Leonard, G. L., & Behrmanna, M. (2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45(4), 685–695.PubMedCrossRefGoogle Scholar
  151. Hung, W.-T., Lambert, G. H., Huang, P.-W., Patterson, D. G., Jr., & Guo, Y. L. (2013). Genetic susceptibility to dioxin-like chemicals’ induction of cytochrome P4501A2 in the human adult linked to specific AhRR polymorphism. Chemosphere, 90(9), 2358–2364. doi: 10.1016/j.chemosphere.2012.10.026.PubMedCrossRefGoogle Scholar
  152. Hurst, J. L. (1990). Urine marking in populations of wild house mice Mus domesticus Rutty. I. Communication between males. Animal Behaviour, 40(2), 209–222.CrossRefGoogle Scholar
  153. Ingelido, A. M., Ballard, T., Dellatte, E., di Domenico, A., Ferri, F., Fulgenzi, A. R., et al. (2007). Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in milk from Italian women living in Rome and Venice. Chemosphere, 67(9), S301–S306. Epub 2007 Jan 2025.PubMedCrossRefGoogle Scholar
  154. Inoue, K., Okada, F., Ito, R., Kato, S., Sasaki, S., Nakajima, S., et al. (2004). Perfluorooctane sulfonate (PFOS) and related perfluorinated compounds in human maternal and cord blood samples: Assessment of PFOS exposure in a susceptible population during pregnancy. Environmental Health Perspectives, 112(11), 1204–1207.PubMedPubMedCentralCrossRefGoogle Scholar
  155. James, S. J., Melnyk, S., Fuchs, G., Reid, T., Jernigan, S., Pavliv, O., et al. (2009). Efficacy of methylcobalamin and folinic acid treatment on glutathione redox status in children with autism. American Journal of Clinical Nutrition, 89(1), 425–430.PubMedCrossRefGoogle Scholar
  156. James, S., Shpyleva, S., Melnyk, S., Pavliv, O., & Pogribny, I. (2013). Complex epigenetic regulation of Engrailed-2 (EN-2) homeobox gene in the autism cerebellum. Translational Psychiatry, 3(2), e232.PubMedPubMedCentralCrossRefGoogle Scholar
  157. Jankowsky, J. L., Melnikova, T., Fadale, D. J., Xu, G. M., Slunt, H. H., Gonzales, V., et al. (2005). Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer’s disease. The Journal of Neuroscience, 25(21), 5217–5224.PubMedPubMedCentralCrossRefGoogle Scholar
  158. Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., et al. (2010). Observational fear learning involves affective pain system and Cav1. 2 Ca2+ channels in ACC. Nature Neuroscience, 13(4), 482–488.PubMedPubMedCentralCrossRefGoogle Scholar
  159. Jeon, D., & Shin, H. S. (2011). A mouse model for observational fear learning and the empathetic response. Current Protocols in Neuroscience, 8, Unit 8.27.PubMedGoogle Scholar
  160. Jiang, Y., Chen, J., Tong, J., & Chen, T. (2014). Trichloroethylene-induced gene expression and DNA methylation changes in B6C3F1 mouse liver. PLoS One, 9(12), e116–179.CrossRefGoogle Scholar
  161. Josh Huang, Z., & Zeng, H. (2013). Genetic approaches to neural circuits in the mouse. Annual Review of Neuroscience, 36, 183–215.PubMedCrossRefGoogle Scholar
  162. Jurado-Parras, M. T., Gruart, A., & Delgado-García, J. M. (2012). Observational learning in mice can be prevented by medial prefrontal cortex stimulation and enhanced by nucleus accumbens stimulation. Learning & Memory, 19(3), 99–106.CrossRefGoogle Scholar
  163. Juraska, J. M., Greenough, W. T., Elliott, C., Mack, K. J., & Berkowitz, R. (1980). Plasticity in adult rat visual cortex: An examination of several cell populations after differential rearing. Behavioral and Neural Biology, 29(2), 157–167.PubMedCrossRefGoogle Scholar
  164. Juraska, J. M., Greenough, W. T., & Conlee, J. W. (1983). Differential rearing affects responsiveness of rats to depressant and convulsant drugs. Physiology & Behavior, 31(5), 711–715.CrossRefGoogle Scholar
  165. Kane, M. J., Angoa-Peréz, M., Briggs, D. I., Sykes, C. E., Francescutti, D. M., Rosenberg, D. R., et al. (2012). Mice genetically depleted of brain serotonin display social impairments, communication deficits and repetitive behaviors: Possible relevance to autism. PLoS One, 7(11), e48975.PubMedPubMedCentralCrossRefGoogle Scholar
  166. Kannan, K., Corsolini, S., Falandysz, J., Fillmann, G., Kumar, K. S., Loganathan, B. G., et al. (2004). Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environmental Science & Technology, 38(17), 4489–4495.CrossRefGoogle Scholar
  167. Kavaliers, M., Choleris, E., Agmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2005a). Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice. Animal Behaviour, 70(3), 693–702.CrossRefGoogle Scholar
  168. Kavaliers, M., Choleris, E., & Colwell, D. D. (2001). Learning from others to cope with biting flies: Social learning of fear-induced conditioned analgesia and active avoidance. Behavioral Neuroscience, 115(3), 661–674.PubMedCrossRefGoogle Scholar
  169. Kavaliers, M., Choleris, E., & Pfaff, D. W. (2005b). Recognition and avoidance of the odors of parasitized conspecifics and predators: Differential genomic correlates. Neuroscience & Biobehavioral Reviews, 29(8), 1347–1359.CrossRefGoogle Scholar
  170. Kavaliers, M., & Colwell, D. D. (1995). Odours of parasitized males induce aversive responses in female mice. Animal Behaviour, 50(5), 1161–1169.CrossRefGoogle Scholar
  171. Kelley, A. E., & Berridge, K. C. (2002). The neuroscience of natural rewards: Relevance to addictive drugs. The Journal of Neuroscience, 22(9), 3306–3311.PubMedGoogle Scholar
  172. Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386(6624), 493–495.PubMedCrossRefGoogle Scholar
  173. Kendig, M. D., Bowen, M. T., Kemp, A. H., & McGregor, I. S. (2011). Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience. Behavioural Brain Research, 225(2), 405–414.PubMedCrossRefGoogle Scholar
  174. Kerley-Hamilton, J. S., Trask, H. W., Ridley, C. J. A., DuFour, E., Lesseur, C., Ringelberg, C. S., et al. (2012). Inherent and benzo[a]pyrene-induced differential aryl hydrocarbon receptor signaling greatly affects life span, atherosclerosis, cardiac gene expression, and body and heart growth in mice. Toxicological Sciences, 126(2), 391–404.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Kigar, S., & Auger, A. (2013). Epigenetic mechanisms may underlie the aetiology of sex differences in mental health risk and resilience. Journal of Neuroendocrinology, 25(11), 1141–1150.PubMedPubMedCentralCrossRefGoogle Scholar
  176. Kim, K. C., Choi, C. S., Kim, J.-W., Han, S.-H., Cheong, J. H., Ryu, J. H., et al. (2016). MeCP2 modulates sex differences in the postsynaptic development of the valproate animal model of autism. Molecular Neurobiology, 53(1), 40–56.PubMedCrossRefGoogle Scholar
  177. Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010). Social transmission of fear in rats: The role of 22-kHz ultrasonic distress vocalization. PLoS One, 5(12), e15077.PubMedPubMedCentralCrossRefGoogle Scholar
  178. Kim, B. S., Lee, J., Bang, M., Am Seo, B., Khalid, A., Jung, M. W., et al. (2014). Differential regulation of observational fear and neural oscillations by serotonin and dopamine in the mouse anterior cingulate cortex. Psychopharmacology, 231(22), 4371–4381.PubMedCrossRefGoogle Scholar
  179. Kim, Y. S., Leventhal, B. L., Koh, Y. J., Fombonne, E., Laska, E., Lim, E. C., et al. (2011). Prevalence of autism spectrum disorders in a total population sample. American Journal of Psychiatry, 168(9), 904–912.PubMedCrossRefGoogle Scholar
  180. Kim, S., Mátyás, F., Lee, S., Acsády, L., & Shin, H.-S. (2012). Lateralization of observational fear learning at the cortical but not thalamic level in mice. Proceedings of the National Academy of Sciences, 109(38), 15497–15501.CrossRefGoogle Scholar
  181. Kinney, D. K., Munir, K. M., Crowley, D. J., & Miller, A. M. (2008). Prenatal stress and risk for autism. Neuroscience & Biobehavioral Reviews, 32(8), 1519–1532.CrossRefGoogle Scholar
  182. Koh, S., Magid, R., Chung, H., Stine, C. D., & Wilson, D. N. (2007). Depressive behavior and selective down-regulation of serotonin receptor expression after early-life seizures: Reversal by environmental enrichment. Epilepsy & Behavior: E&B, 10(1), 26.CrossRefGoogle Scholar
  183. Kondo, M., Gray, L. J., Pelka, G. J., Christodoulou, J., Tam, P. P., & Hannan, A. J. (2008). Environmental enrichment ameliorates a motor coordination deficit in a mouse model of Rett syndrome–Mecp2 gene dosage effects and BDNF expression. European Journal of Neuroscience, 27(12), 3342–3350.PubMedCrossRefGoogle Scholar
  184. Kooy, R. F., D’Hooge, R., Reyniers, E., Bakker, C. E., Nagels, G., De Boulle, K., et al. (1996). Transgenic mouse model for the fragile X syndrome. American Journal of Medical Genetics, 64(2), 241–245.PubMedCrossRefGoogle Scholar
  185. Krech, D., Rosenzweig, M. R., & Bennett, E. L. (1960). Effects of environmental complexity and training on brain chemistry. Journal of Comparative and Physiological Psychology, 53(6), 509.PubMedCrossRefGoogle Scholar
  186. Kumar, R. A., & Christian, S. L. (2009). Genetics of autism spectrum disorders. Current Neurology and Neuroscience Reports, 9(3), 188–197.PubMedCrossRefGoogle Scholar
  187. Kumsta, R., Hummel, E., Chen, F. S., & Heinrichs, M. (2013). Epigenetic regulation of the oxytocin receptor gene: Implications for behavioral neuroscience. Frontiers in Neuroscience, 7.Google Scholar
  188. Kundakovic, M., Gudsnuk, K., Herbstman, J. B., Tang, D., Perera, F. P., & Champagne, F. A. (2014). DNA methylation of BDNF as a biomarker of early-life adversity. Proceedings of the National Academy of Sciences, 112(22), 6807–6813.CrossRefGoogle Scholar
  189. Kurian, J. R., Bychowski, M. E., Forbes-Lorman, R. M., Auger, C. J., & Auger, A. P. (2008). Mecp2 organizes juvenile social behavior in a sex-specific manner. The Journal of Neuroscience, 28(28), 7137–7142.PubMedPubMedCentralCrossRefGoogle Scholar
  190. Kurian, J. R., Forbes-Lorman, R. M., & Auger, A. P. (2007). Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics, 2(3), 173–178.PubMedCrossRefGoogle Scholar
  191. Lahvis, G. P., Alleva, E., & Scattoni, M. L. (2010). Translating mouse vocalizations: Prosody and frequency modulation. Genes, Brain and Behavior, 10(1), 4–16.CrossRefGoogle Scholar
  192. Lahvis, G. P., & Black, L. M. (2011). Social interactions in the clinic and the cage: Toward a more valid mouse model of autism. In R. Jacob (Ed.), Animal models of behavioral analysis (Vol. 50, pp. 153–192). Totowa: Humana Press.CrossRefGoogle Scholar
  193. Lahvis, G. P., & Bradfield, C. A. (1998). Ahr null alleles: Distinctive or different? Biochemical Pharmacology, 56(7), 781–787.PubMedCrossRefGoogle Scholar
  194. Lahvis, G. P., Lindell, S. L., Thomas, R. S., McCuskey, R. S., Murphy, C., Glover, E., et al. (2000). Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 97(19), 10442–10447.PubMedPubMedCentralCrossRefGoogle Scholar
  195. Lam, K. S., Bodfish, J. W., & Piven, J. (2008). Evidence for three subtypes of repetitive behavior in autism that differ in familiality and association with other symptoms. Journal of Child Psychology & Psychiatry & Allied Disciplines, 49(11), 1193–1200.CrossRefGoogle Scholar
  196. Landrigan, P. J. (2010). What causes autism? Exploring the environmental contribution. Current Opinion in Pediatrics, 22(2), 219–225.PubMedCrossRefGoogle Scholar
  197. Langford, D. J., Bailey, A. L., Chanda, M. L., Clarke, S. E., Drummond, T. E., Echols, S., et al. (2010). Coding of facial expressions of pain in the laboratory mouse. Nature Methods, 7(6), 447–449.PubMedCrossRefGoogle Scholar
  198. Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., et al. (2006). Social modulation of pain as evidence for empathy in mice. Science, 312(5782), 1967–1970.PubMedCrossRefGoogle Scholar
  199. Latham, N., & Mason, G. (2004). From house mouse to mouse house: The behavioural biology of free-living Mus musculus and its implications in the laboratory. Applied Animal Behaviour Science, 86(3), 261–289.CrossRefGoogle Scholar
  200. Lazic, S., Grote, H., Blakemore, C., Hannan, A., van Dellen, A., Phillips, W., et al. (2006). Neurogenesis in the R6/1 transgenic mouse model of Huntington’s disease: Effects of environmental enrichment. The European Journal of Neuroscience, 23(7), 1829.PubMedCrossRefGoogle Scholar
  201. Lewis, M. H., & Bodfish, J. W. (1998). Repetitive behavior disorders in autism. Mental Retardation and Developmental Disabilities Research Reviews, 4(2), 80–89. doi: 10.1002/(sici)1098-2779(1998)4:2<80::aid-mrdd4>3.0.co;2-0.
  202. Li, Y., Hamilton, K. J., Lai, A. Y., Burns, K. A., Li, L., Wade, P. A., et al. (2014). Diethylstilbestrol (DES)-stimulated hormonal toxicity is mediated by ERα alteration of target gene methylation patterns and epigenetic modifiers (DNMT3A, MBD2, and HDAC2) in the mouse seminal vesicle. Environmental Health Perspectives, 122(3), 262.PubMedGoogle Scholar
  203. Lind, L., Penell, J., Luttropp, K., Nordfors, L., Syvänen, A.-C., Axelsson, T., et al. (2013). Global DNA hypermethylation is associated with high serum levels of persistent organic pollutants in an elderly population. Environment International, 59, 456–461.PubMedCrossRefGoogle Scholar
  204. Liu, H.-X., Lopatina, O., Higashida, C., Fujimoto, H., Akther, S., Inzhutova, A., et al. (2013). Displays of paternal mouse pup retrieval following communicative interaction with maternal mates. Nature Communications, 4, 1346.PubMedPubMedCentralCrossRefGoogle Scholar
  205. Liu, X.-Q., Paterson, A. D., Szatmari, P., & Autism Genome Project Consortium. (2008). Genome-wide linkage analyses of quantitative and categorical autism subphenotypes. Biological Psychiatry, 64(7), 561–570.PubMedPubMedCentralCrossRefGoogle Scholar
  206. Lonetti, G., Angelucci, A., Morando, L., Boggio, E. M., Giustetto, M., & Pizzorusso, T. (2010). Early environmental enrichment moderates the behavioral and synaptic phenotype of MeCP2 null mice. Biological Psychiatry, 67(7), 657–665.PubMedCrossRefGoogle Scholar
  207. Lord, C., Leventhal, B. L., & Cook, E. H., Jr. (2001). Quantifying the phenotype in autism spectrum disorders. American Journal of Medical Genetics, 105(1), 36–38.PubMedCrossRefGoogle Scholar
  208. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685.PubMedCrossRefGoogle Scholar
  209. Lynn, D. A., & Brown, G. R. (2009). The ontogeny of exploratory behavior in male and female adolescent rats (Rattus norvegicus). Developmental Psychobiology, 51(6), 513–520. doi: 10.1002/dev.20386.PubMedPubMedCentralCrossRefGoogle Scholar
  210. Maesako, M., Uemura, K., Kubota, M., Kuzuya, A., Sasaki, K., Asada, M., et al. (2012). Environmental enrichment ameliorated high-fat diet-induced Aβ deposition and memory deficit in APP transgenic mice. Neurobiology of Aging, 33(5), 1011. e1011–1011. e1023.PubMedCrossRefGoogle Scholar
  211. Magnee, M. J., de Gelder, B., van Engeland, H., & Kemner, C. (2008). Atypical processing of fearful face-voice pairs in pervasive developmental disorder: An ERP study. Clinical Neurophysiology, 119(9), 2004–2010.CrossRefGoogle Scholar
  212. Martin, L. J., Hathaway, G., Isbester, K., Mirali, S., Acland, E. L., Niederstrasser, N., et al. (2015). Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Current Biology, 25(3), 326–332. doi: 10.1016/j.cub.2014.11.028.PubMedCrossRefGoogle Scholar
  213. Martinez-Zamudio, R., & Ha, H. C. (2011). Environmental epigenetics in metal exposure. Epigenetics, 6(7), 820–827.PubMedPubMedCentralCrossRefGoogle Scholar
  214. Matsuda, K. I. (2014). Epigenetic changes in the estrogen receptor α gene promoter: Implications in sociosexual behaviors. Frontiers in Neuroscience, 8, 344.PubMedPubMedCentralCrossRefGoogle Scholar
  215. Mbadiwe, T., & Millis, R. M. (2014). In C Payne (Ed.), Epigenetic mechanisms in autism spectrum disorders, epigenetics and epigenomics. InTech, doi: 10.5772/57195. Retrieved from http://www.intechopen.com/books/epigenetics-and-epigenomics/epigenetic-mechanisms-in-autism-spectrum-disorders.
  216. McCann, J., & Peppe, S. (2003). Prosody in autism spectrum disorders: A critical review. International Journal of Language & Communication Disorders, 38(4), 325–350.CrossRefGoogle Scholar
  217. McCann, J., Peppe, S., Gibbon, F. E., O’Hare, A., & Rutherford, M. (2007). Prosody and its relationship to language in school-aged children with high-functioning autism. International Journal of Language & Communication Disorders, 42(6), 682–702.CrossRefGoogle Scholar
  218. McFadden, S. A. (1996). Phenotypic variation in xenobiotic metabolism and adverse environmental response: Focus on sulfur-dependent detoxification pathways. Toxicology, 111(1–3), 43–65.PubMedCrossRefGoogle Scholar
  219. McGraw, L. A., & Young, L. J. (2010). The prairie vole: An emerging model organism for understanding the social brain. Trends in Neurosciences, 33(2), 103–109. doi: 10.1016/j.tins.2009.11.006.PubMedCrossRefGoogle Scholar
  220. McNaughton, C. H., Moon, J., Strawderman, M. S., Maclean, K. N., Evans, J., & Strupp, B. J. (2008). Evidence for social anxiety and impaired social cognition in a mouse model of fragile X syndrome. Behavioral Neuroscience, 122(2), 293–300.PubMedCrossRefGoogle Scholar
  221. McOmish, C., Burrows, E., Howard, M., Scarr, E., Kim, D., Shin, H., et al. (2008). Phospholipase C-β1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Molecular Psychiatry, 13(7), 661–672.PubMedCrossRefGoogle Scholar
  222. Meaney, M. J. (2010). Epigenetics and the biological definition of gene x environment interactions. Child Development, 81(1), 41–79.PubMedCrossRefGoogle Scholar
  223. Meaney, M. J., Dodge, A. M., & Beatty, W. W. (1981). Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats. Physiology & Behavior, 26(3), 467–472.CrossRefGoogle Scholar
  224. Meaney, M. J., & McEwen, B. S. (1986). Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Research, 398(2), 324–328.PubMedCrossRefGoogle Scholar
  225. Meaney, M. J., & Stewart, J. (1981). Neonatal androgens influence the social play of prepubescent rats. Hormones and Behavior, 15(2), 197–213.PubMedCrossRefGoogle Scholar
  226. Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity? Trends in Neurosciences, 28(9), 456–463.PubMedCrossRefGoogle Scholar
  227. Michalon, A., Sidorov, M., Ballard, T. M., Ozmen, L., Spooren, W., Wettstein, J. G., et al. (2012). Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice. Neuron, 74(1), 49–56.PubMedCrossRefGoogle Scholar
  228. Milestone, C. B., Maclatchy, D. L., & Hewitt, M. L. (2013). Process for refining chemicals from pulp and paper mill wastewaters. US Patent 20,130,072,724.Google Scholar
  229. Miranda-Contreras, L., Davila-Ovalles, R., Benitez-Diaz, P., Pena-Contreras, Z., & Palacios-Pru, E. (2005). Effects of prenatal paraquat and mancozeb exposure on amino acid synaptic transmission in developing mouse cerebellar cortex. Developmental Brain Research, 160(1), 19–27. doi: 10.1016/j.devbrainres.2005.08.001.PubMedCrossRefGoogle Scholar
  230. Mitchell, M. M., Woods, R., Chi, L. H., Schmidt, R. J., Pessah, I. N., Kostyniak, P. J., et al. (2012). Levels of select PCB and PBDE congeners in human postmortem brain reveal possible environmental involvement in 15q11‐q13 duplication autism spectrum disorder. Environmental and Molecular Mutagenesis, 53(8), 589–598.PubMedPubMedCentralCrossRefGoogle Scholar
  231. Miyake, K., Hirasawa, T., Koide, T., & Kubota, T. (2012). Epigenetics in autism and other neurodevelopmental diseases. In S. I. Ahmed (Ed.), Neurodegenerative diseases (pp. 91–98). New York: Springer.CrossRefGoogle Scholar
  232. Moles, A., Kieffer, B. L., & D’Amato, F. R. (2004). Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science, 304(5679), 1983–1986.PubMedCrossRefGoogle Scholar
  233. Moretti, P., Bouwknecht, J. A., Teague, R., Paylor, R., & Zoghbi, H. Y. (2005). Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Human Molecular Genetics, 14(2), 205–220.PubMedCrossRefGoogle Scholar
  234. Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. European Journal of Neuroscience, 18(12), 3367–3374.PubMedCrossRefGoogle Scholar
  235. Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2004). Sexual differentiation of the vertebrate nervous system. Nature Neuroscience, 7(10), 1034–1039.PubMedCrossRefGoogle Scholar
  236. Moy, S. S., Nadler, J. J., Young, N. B., Perez, A., Holloway, L. P., Barbaro, R. P., et al. (2007). Mouse behavioral tasks relevant to autism: Phenotypes of 10 inbred strains. Behavioural Brain Research, 176(1), 4–20. doi: 10.1016/j.bbr.2006.07.030.PubMedCrossRefGoogle Scholar
  237. Mychasiuk, R., Zahir, S., Schmold, N., Ilnytskyy, S., Kovalchuk, O., & Gibb, R. (2012). Parental enrichment and offspring development: Modifications to brain, behavior and the epigenome. Behavioural Brain Research, 228(2), 294–298. doi: 10.1016/j.bbr.2011.11.036.PubMedCrossRefGoogle Scholar
  238. Nader, J., Claudia, C., El Rawas, R., Favot, L., Jaber, M., Thiriet, N., et al. (2014). Loss of environmental enrichment increases vulnerability to cocaine addiction. Neuropsychopharmacology, 39(3), 780.PubMedPubMedCentralCrossRefGoogle Scholar
  239. Nadler, J., Moy, S., Dold, G., Trang, D., Simmons, N., Perez, A., et al. (2004). Automated apparatus for quantitation of social approach behaviors in mice. Genes, Brain and Behavior, 3(5), 303–314.CrossRefGoogle Scholar
  240. Nag, N., Moriuchi, J. M., Peitzman, C. G., Ward, B. C., Kolodny, N. H., & Berger-Sweeney, J. E. (2009). Environmental enrichment alters locomotor behaviour and ventricular volume in Mecp2 1lox mice. Behavioural Brain Research, 196(1), 44–48.PubMedCrossRefGoogle Scholar
  241. Nagarajan, R., Hogart, A., Gwye, Y., Martin, M. R., & LaSalle, J. M. (2006). Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics, 1(4), 172–182.CrossRefGoogle Scholar
  242. Naka, F., Narita, N., Okado, N., & Narita, M. (2005). Modification of AMPA receptor properties following environmental enrichment. Brain and Development, 27(4), 275–278.PubMedCrossRefGoogle Scholar
  243. Nguyen, A., Rauch, T. A., Pfeifer, G. P., & Hu, V. W. (2010). Global methylation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA, whose protein product is reduced in autistic brain. The FASEB Journal, 24(8), 3036–3051.PubMedPubMedCentralCrossRefGoogle Scholar
  244. Nithianantharajah, J., & Hannan, A. J. (2006). Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature Reviews Neuroscience, 7(9), 697–709.PubMedCrossRefGoogle Scholar
  245. Nunes, S., Muecke, E.-M., Anthony, J. A., & Batterbee, A. S. (1999). Endocrine and energetic mediation of play behavior in free-living belding’s ground squirrels. Hormones and Behavior, 36(2), 153–165. doi: 10.1006/hbeh.1999.1538.PubMedCrossRefGoogle Scholar
  246. O’Roak, B. J., Deriziotis, P., Lee, C., Vives, L., Schwartz, J. J., Girirajan, S., et al. (2011). Exome sequencing in sporadic autism spectrum disorders identifies severe de novo mutations. Nature Genetics, 43(6), 585–589. doi: 10.1038/ng.835.PubMedPubMedCentralCrossRefGoogle Scholar
  247. Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of prepubescent rats. Physiology & Behavior, 20(2), 113–115. doi: 10.1016/0031-9384(78)90060-4.CrossRefGoogle Scholar
  248. Ostrovsky, Y., Andalman, A., & Sinha, P. (2006). Vision following extended congenital blindness. Psychological Science, 17(12), 1009–1014. doi: 10.1111/j.1467-9280.2006.01827.x.PubMedCrossRefGoogle Scholar
  249. Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., et al. (2011). Recurrence risk for autism spectrum disorders: A baby siblings research consortium study. Pediatrics, 128(3), e488–e495.PubMedPubMedCentralGoogle Scholar
  250. Palanza, P., Morley-Fletcher, S., & Laviola, G. (2001). Novelty seeking in periadolescent mice: Sex differences and influence of intrauterine position. Physiology & Behavior, 72(1–2), 255–262. doi: 10.1016/S0031-9384(00)00406-6.CrossRefGoogle Scholar
  251. Panksepp, J. B., Jochman, K., Kim, J. U., Koy, J. J., Wilson, E. D., Chen, Q., et al. (2007). Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS One [Electronic Resource], 2, e351. doi: 10.1371/journal.pone.0000351.CrossRefGoogle Scholar
  252. Panksepp, J. B., & Lahvis, G. P. (2007). Social reward among juvenile mice. Genes, Brain and Behavior, 6(7), 661–671. doi: 10.1111/j.1601-183X.2006.00295.x.CrossRefGoogle Scholar
  253. Panksepp, J. B., & Lahvis, G. P. (2011). Rodent empathy and affective neuroscience. Neuroscience & Biobehavioral Reviews, 35(9), 1864–1875. doi: 10.1016/j.neubiorev.2011.05.013.CrossRefGoogle Scholar
  254. Panksepp, J. B., & Lahvis, G. P. (2016). Differential influence of social versus isolate housing on vicarious fear learning in adolescent mice. Behavioral Neuroscience, 130(2), 206.PubMedPubMedCentralCrossRefGoogle Scholar
  255. Parent, C. I., & Meaney, M. J. (2008). The influence of natural variations in maternal care on play fighting in the rat. Developmental Psychobiology, 50(8), 767–776.PubMedCrossRefGoogle Scholar
  256. Passineau, M. J., Green, E. J., & Dietrich, W. D. (2001). Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Experimental Neurology, 168(2), 373–384.PubMedCrossRefGoogle Scholar
  257. Pearson, B., Defensor, E., Pobbe, R., Yamamoto, L., Bolivar, V., Blanchard, D., et al. (2012). Mecp2 truncation in male mice promotes affiliative social behavior. Behavior Genetics, 42(2), 299–312.PubMedCrossRefGoogle Scholar
  258. Pellis, S. (2002). Sex differences in play fighting revisited: Traditional and nontraditional mechanisms of sexual differentiation in rats. Archives of Sexual Behavior, 31(1), 17–26. doi: 10.1023/a:1014070916047.PubMedCrossRefGoogle Scholar
  259. Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1994). Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens. Journal of Comparative Psychology, 108(1), 68.PubMedCrossRefGoogle Scholar
  260. Persico, A., Levitt, P., & Pimenta, A. (2006). Polymorphic GGC repeat differentially regulates human reelin gene expression levels. Journal of Neural Transmission, 113(10), 1373–1382.PubMedCrossRefGoogle Scholar
  261. Pessah, I. N., Seegal, R. F., Lein, P. J., LaSalle, J., Yee, B. K., Van De Water, J., et al. (2008). Immunologic and neurodevelopmental susceptibilities of autism. Neurotoxicology, 29(3), 532–545.PubMedCrossRefGoogle Scholar
  262. Peters, S. U., Gordon, R. L., & Key, A. P. (2014). Induced gamma oscillations differentiate familiar and novel voices in children with MECP2 duplication and Rett syndromes. Journal of Child Neurology, 30(2), 145–152.PubMedPubMedCentralCrossRefGoogle Scholar
  263. Phiel, C. J., Zhang, F., Huang, E. Y., Guenther, M. G., Lazar, M. A., & Klein, P. S. (2001). Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. Journal of Biological Chemistry, 276(39), 36734–36741.PubMedCrossRefGoogle Scholar
  264. Picker, J. D., Yang, R., Ricceri, L., & Berger-Sweeney, J. (2006). An altered neonatal behavioral phenotype in Mecp2 mutant mice. Neuroreport, 17(5), 541–544.PubMedCrossRefGoogle Scholar
  265. Pietropaolo, S., Branchi, I., Cirulli, F., Chiarotti, F., Aloe, L., & Alleva, E. (2004). Long-term effects of the periadolescent environment on exploratory activity and aggressive behaviour in mice: Social versus physical enrichment. Physiology & Behavior, 81(3), 443–453. doi: 10.1016/j.physbeh.2004.02.022.CrossRefGoogle Scholar
  266. Pobbe, R. L., Pearson, B. L., Defensor, E. B., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2010). Expression of social behaviors of C57BL/6J versus BTBR inbred mouse strains in the visible burrow system. Behavioural Brain Research, 214(2), 443–449.PubMedPubMedCentralCrossRefGoogle Scholar
  267. Poland, A., Palen, D., & Glover, E. (1994). Analysis of the four alleles of the murine aryl hydrocarbon receptor. Molecular Pharmacology, 46(5), 915–921.PubMedGoogle Scholar
  268. Pollock, J. D., Wu, D.-Y., & Satterlee, J. S. (2014). Molecular neuroanatomy: A generation of progress. Trends in Neurosciences, 37(2), 106–123.PubMedCrossRefGoogle Scholar
  269. Pound, P., Ebrahim, S., Sandercock, P., Bracken, M. B., & Roberts, I. (2004). Where is the evidence that animal research benefits humans? BMJ, 328(7438), 514–517.PubMedPubMedCentralCrossRefGoogle Scholar
  270. Preston, S. D., & de Waal, F. B. (2002). Empathy: Its ultimate and proximate bases. Behavioral and Brain Sciences, 25(1), 1–20.PubMedGoogle Scholar
  271. Ramalhinho, M. G., Mathias, M. L., & Muccillo-Baisch, A. L. (2012). Physiological damage in Algerian mouse Mus spretus (Rodentia: muridae) exposed to crude oil. Journal of BioScience and Biotechnology, 1(2), 125–133.Google Scholar
  272. Ramocki, M. B., Peters, S. U., Tavyev, Y. J., Zhang, F., Carvalho, C., Schaaf, C. P., et al. (2009). Autism and other neuropsychiatric symptoms are prevalent in individuals with MeCP2 duplication syndrome. Annals of Neurology, 66(6), 771–782.PubMedPubMedCentralCrossRefGoogle Scholar
  273. Rampon, C., Jiang, C. H., Dong, H., Tang, Y.-P., Lockhart, D. J., Schultz, P. G., et al. (2000). Effects of environmental enrichment on gene expression in the brain. Proceedings of the National Academy of Sciences, 97(23), 12880–12884.CrossRefGoogle Scholar
  274. Rao, D. B., Jortner, B. S., & Sills, R. C. (2014). Animal models of peripheral neuropathy due to environmental toxicants. Ilar Journal, 54(3), 315–323.PubMedPubMedCentralCrossRefGoogle Scholar
  275. Rauh, V. A., Perera, F. P., Horton, M. K., Whyatt, R. M., Bansal, R., Hao, X., et al. (2012). Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proceedings of the National Academy of Sciences, 109(20), 7871–7876. doi: 10.1073/pnas.1203396109.CrossRefGoogle Scholar
  276. Reynolds, S., Urruela, M., & Devine, D. P. (2013). Effects of environmental enrichment on repetitive behaviors in the BTBR T+tf/J mouse model of autism. Autism Research: Official Journal of the International Society for Autism Research, 6(5), 337–343. doi: 10.1002/aur.1298.CrossRefGoogle Scholar
  277. Richter, S. H., Garner, J. P., Auer, C., Kunert, J., & Wurbel, H. (2010). Systematic variation improves reproducibility of animal experiments. Nature Methods, 7(3), 167–168.PubMedCrossRefGoogle Scholar
  278. Richter, S. H., Garner, J. P., & Wurbel, H. (2009). Environmental standardization: Cure or cause of poor reproducibility in animal experiments? Nature Methods, 6(4), 257–261.PubMedCrossRefGoogle Scholar
  279. Richter, S. H., Zeuch, B., Riva, M. A., Gass, P., & Vollmayr, B. (2013). Environmental enrichment ameliorates depressive-like symptoms in young rats bred for learned helplessness. Behavioural Brain Research, 252, 287–292.PubMedCrossRefGoogle Scholar
  280. Roberts, S. A., Davidson, A. J., Beynon, R. J., & Hurst, J. L. (2014). Female attraction to male scent and associative learning: The house mouse as a mammalian model. Animal Behaviour, 97, 313–321.CrossRefGoogle Scholar
  281. Roberts, E. M., English, P. B., Grether, J. K., Windham, G. C., Somberg, L., & Wolff, C. (2007). Maternal residence near agricultural pesticide applications and autism spectrum disorders among children in the California Central Valley. Environmental Health Perspectives, 115(10), 1482–1489.PubMedPubMedCentralGoogle Scholar
  282. Robins, D. L., Casagrande, K. s., Barton, M., Chen, C.-M. A., Dumont-Mathieu, T., & Fein, D. (2014). Validation of the modified checklist for autism in toddlers, revised with follow-up (M-CHAT-R/F). Pediatrics, 133(1), 37–45.PubMedPubMedCentralCrossRefGoogle Scholar
  283. Rogers, S. J. (1999). An examination of the imitation deficit in autism. In J. N. G. Butterworth (Ed.), Imitation in infancy (pp. 254–283). New York, NY: Cambridge University Press.Google Scholar
  284. Rosenberg, R., Law, J., Yenokyan, G., McGready, J., Kaufmann, W. E., & Law, P. A. (2009). Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Archives of Pediatrics & Adolescent Medicine, 163(10), 907–914. doi: 10.1001/archpediatrics.2009.98.CrossRefGoogle Scholar
  285. Rosenzweig, M. R., Krech, D., Bennett, E. L., & Diamond, M. C. (1962a). Effects of environmental complexity and training on brain chemistry and anatomy: A replication and extension. Journal of Comparative and Physiological Psychology, 55(4), 429.PubMedCrossRefGoogle Scholar
  286. Rosenzweig, M. R., Krech, D., Bennett, E. L., & Zolman, J. F. (1962b). Variation in environmental complexity and brain measures. Journal of Comparative and Physiological Psychology, 55(6), 1092.PubMedCrossRefGoogle Scholar
  287. Rottman, S. J., & Snowdon, C. T. (1972). Demonstration and analysis of an alarm pheromone in mice. Journal of Comparative and Physiological Psychology, 81(3), 483–490.PubMedCrossRefGoogle Scholar
  288. Roze, E., Meijer, L., Bakker, A., Van Braeckel, K. N., Sauer, P. J., & Bos, A. F. (2009). Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environmental Health Perspectives, 117(12), 1953–1958. Epub 2009 Aug 1931.PubMedPubMedCentralCrossRefGoogle Scholar
  289. Samaco, R. C., Hogart, A., & LaSalle, J. M. (2005). Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Human Molecular Genetics, 14(4), 483–492.PubMedCrossRefGoogle Scholar
  290. Samaco, R. C., Mandel-Brehm, C., McGraw, C. M., Shaw, C. A., McGill, B. E., & Zoghbi, H. Y. (2012). Crh and Oprm1 mediate anxiety-related behavior and social approach in a mouse model of MECP2 duplication syndrome. Nature Genetics, 44(2), 206–211.PubMedPubMedCentralCrossRefGoogle Scholar
  291. Sanders, J., Mayford, M., & Jeste, D. (2013). Empathic fear responses in mice are triggered by recognition of a shared experience. PLoS One, 8(9), e74609.PubMedPubMedCentralCrossRefGoogle Scholar
  292. Sanders, S. J., Murtha, M. T., Gupta, A. R., Murdoch, J. D., Raubeson, M. J., Willsey, A. J., et al. (2012). De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature, 485(7397), 237–241. doi: 10.1038/nature10945.PubMedPubMedCentralCrossRefGoogle Scholar
  293. Sasson, N. J., Turner-Brown, L. M., Holtzclaw, T. N., Lam, K. S. L., & Bodfish, J. W. (2008). Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Research, 1(1), 31–42. doi: 10.1002/aur.4.PubMedCrossRefGoogle Scholar
  294. Scattoni, M. L., Crawley, J., & Ricceri, L. (2009). Ultrasonic vocalizations: A tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neuroscience & Biobehavioral Reviews, 33(4), 508–515.CrossRefGoogle Scholar
  295. Schaevitz, L. R., Moriuchi, J. M., Nag, N., Mellot, T. J., & Berger-Sweeney, J. (2010). Cognitive and social functions and growth factors in a mouse model of rett syndrome. Physiology & Behavior, 100(3), 255–263.CrossRefGoogle Scholar
  296. Schanen, N. C. (2006). Epigenetics of autism spectrum disorders. Human Molecular Genetics, 15(Suppl. 2), R138–R150.PubMedCrossRefGoogle Scholar
  297. Schneider, T., Turczak, J., & Przewłocki, R. (2006). Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: Issues for a therapeutic approach in autism. Neuropsychopharmacology, 31(1), 36–46.PubMedGoogle Scholar
  298. Scholz, J., Allemang-Grand, R., Dazai, J., & Lerch, J. (2015). Environmental enrichment is associated with rapid volumetric brain changes in adult mice. Neuroimage, 109, 190–198.PubMedCrossRefGoogle Scholar
  299. Sebat, J., Lakshmi, B., Malhotra, D., Troge, J., Lese-Martin, C., Walsh, T., et al. (2007). Strong association of de novo copy number mutations with autism. Science, 316(5823), 445–449.PubMedPubMedCentralCrossRefGoogle Scholar
  300. Shah, C. R., Forsberg, C. G., Kang, J. Q., & Veenstra‐VanderWeele, J. (2013). Letting a typical mouse judge whether mouse social interactions are atypical. Autism Research, 6(3), 212–220.PubMedPubMedCentralCrossRefGoogle Scholar
  301. Shahbazian, M. D., Young, J. I., Yuva-Paylor, L. A., Spencer, C. M., Antalffy, B. A., Noebels, J. L., et al. (2002). Mice with truncated MeCP2 recapitulate many rett syndrome features and display hyperacetylation of histone H3. Neuron, 35, 243–254.PubMedCrossRefGoogle Scholar
  302. Shih, J., May, L. D., Gonzalez, H. E., Lee, E. W., Alvi, R. S., Sall, J. W., et al. (2012). Delayed environmental enrichment reverses sevoflurane-induced memory impairment in rats. Anesthesiology, 116(3), 586.PubMedPubMedCentralCrossRefGoogle Scholar
  303. Shriberg, L. D., Paul, R., McSweeny, J. L., Klin, A., & Cohen, D. J. (2001). Speech and prosody characteristics of adolescents and adults with high-functioning autism and Asperger syndrome. Journal of Speech Language and Hearing Research, 44(5), 1097–1115.CrossRefGoogle Scholar
  304. Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303(5661), 1157–1162.PubMedCrossRefGoogle Scholar
  305. Singer, T., Seymour, B., O’Doherty, J. P., Stephan, K. E., Dolan, R. J., & Frith, C. D. (2006). Empathic neural responses are modulated by the perceived fairness of others. Nature, 439(7075), 466–469.PubMedPubMedCentralCrossRefGoogle Scholar
  306. Slotkin, T. A., & Seidler, F. J. (2007). Prenatal chlorpyrifos exposure elicits presynaptic serotonergic and dopaminergic hyperactivity at adolescence: Critical periods for regional and sex-selective effects. Reproductive Toxicology, 23(3), 421–427. doi: 10.1016/j.reprotox.2006.07.010.PubMedCrossRefGoogle Scholar
  307. So, M. K., Taniyasu, S., Yamashita, N., Giesy, J. P., Zheng, J., Fang, Z., et al. (2004). Perfluorinated compounds in coastal waters of Hong Kong, South China, and Korea. Environmental Science & Technology, 38(15), 4056–4063.CrossRefGoogle Scholar
  308. Solinas, M., Chauvet, C., Thiriet, N., El Rawas, R., & Jaber, M. (2008). Reversal of cocaine addiction by environmental enrichment. Proceedings of the National Academy of Sciences, 105(44), 17145–17150.CrossRefGoogle Scholar
  309. Solinas, M., Thiriet, N., Chauvet, C., & Jaber, M. (2010). Prevention and treatment of drug addiction by environmental enrichment. Progress in Neurobiology, 92(4), 572–592.PubMedCrossRefGoogle Scholar
  310. Spencer, C. M., Graham, D. F., Yuva-Paylor, L. A., Nelson, D. L., & Paylor, R. (2008). Social behavior in Fmr1 knockout mice carrying a human FMR1 transgene. Behavioral Neuroscience, 122(3), 710–715.PubMedCrossRefGoogle Scholar
  311. Stairs, D. J., & Bardo, M. T. (2009). Neurobehavioral effects of environmental enrichment and drug abuse vulnerability. Pharmacology Biochemistry and Behavior, 92(3), 377–382.CrossRefGoogle Scholar
  312. Stamou, M., Streifel, K. M., Goines, P. E., & Lein, P. J. (2013). Neuronal connectivity as a convergent target of gene × environment interactions that confer risk for Autism Spectrum Disorders. Neurotoxicology and Teratology, 36, 3–16.PubMedCrossRefGoogle Scholar
  313. Steffenburg, S., Gillberg, C., Hellgren, L., Andersson, L., Gillberg, I. C., Jakobsson, G., et al. (1989). A twin study of autism in Denmark, Finland, Iceland, Norway and Sweden. Journal of Child Psychology and Psychiatry, 30(3), 405–416. doi: 10.1111/j.1469-7610.1989.tb00254.x.PubMedCrossRefGoogle Scholar
  314. Sun, H., Li, F., Zhang, T., Zhang, X., He, N., Song, Q., et al. (2011). Perfluorinated compounds in surface waters and WWTPs in Shenyang, China: Mass flows and source analysis. Water Research, 45(15), 4483–4490.PubMedCrossRefGoogle Scholar
  315. Szeligo, F., & Leblond, C. (1977). Response of the three main types of glial cells of cortex and corpus callosum in rats handled during suckling or exposed to enriched, control and impoverished environments following weaning. Journal of Comparative Neurology, 172(2), 247–263.PubMedCrossRefGoogle Scholar
  316. Sztainberg, Y., Kuperman, Y., Tsoory, M., Lebow, M., & Chen, A. (2010). The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Molecular Psychiatry, 15(9), 905–917.PubMedCrossRefGoogle Scholar
  317. Tang, A. C., Akers, K. G., Reeb, B. C., Romeo, R. D., & McEwen, B. S. (2006). Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proceedings of the National Academy of Sciences, 103(42), 15716–15721.CrossRefGoogle Scholar
  318. Tantra, M., Hammer, C., Kästner, A., Dahm, L., Begemann, M., Bodda, C., et al. (2014). Mild expression differences of MECP2 influencing aggressive social behavior. EMBO Molecular Medicine, 6(5), 662–684. doi: 10.1002/emmm.201303744.PubMedPubMedCentralGoogle Scholar
  319. Tarantini, L., Bonzini, M., Apostoli, P., Pegoraro, V., Bollati, V., Marinelli, B., et al. (2008). Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environmental Health Perspectives, 117(2), 217–222.PubMedPubMedCentralCrossRefGoogle Scholar
  320. Thiriet, N., Amar, L., Toussay, X., Lardeux, V., Ladenheim, B., Becker, K. G., et al. (2008). Environmental enrichment during adolescence regulates gene expression in the striatum of mice. Brain Research, 1222, 31–41. doi: 10.1016/j.brainres.2008.05.030.PubMedPubMedCentralCrossRefGoogle Scholar
  321. Thonhauser, K. E., Raveh, S., Hettyey, A., Beissmann, H., & Penn, D. J. (2013). Scent marking increases male reproductive success in wild house mice. Animal Behaviour, 86(5), 1013–1021.PubMedPubMedCentralCrossRefGoogle Scholar
  322. Toth, K., Munson, J., Meltzoff, A., & Dawson, G. (2006). Early predictors of communication development in young children with autism spectrum disorder: Joint attention, imitation, and toy play. Journal of Autism and Developmental Disorders, 36(8), 993–1005. doi: 10.1007/s10803-006-0137-7.PubMedPubMedCentralCrossRefGoogle Scholar
  323. Tsilidis, K. K., Panagiotou, O. A., Sena, E. S., Aretouli, E., Evangelou, E., Howells, D. W., et al. (2013). Evaluation of excess significance bias in animal studies of neurological diseases. PLoS Biology, 11(7), e1001609.PubMedPubMedCentralCrossRefGoogle Scholar
  324. Valsecchi, P., Bosellini, I., Sabatini, F., Mainardi, M., & Fiorito, G. (2002). Behavioral analysis of social effects on the problem-solving ability in the house mouse. Ethology, 108(12), 1115–1134.CrossRefGoogle Scholar
  325. Van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of environmental enrichment. Nature Reviews Neuroscience, 1(3), 191–198.PubMedCrossRefGoogle Scholar
  326. Van Santen, J. P. H., Prud’hommeaux, E. T., Black, L. M., & Mitchell, M. (2010). Computational prosodic markers for autism. Autism, 14(3), 215–236.PubMedPubMedCentralCrossRefGoogle Scholar
  327. Volk, H. E., Hertz-Picciotto, I., Delwiche, L., Lurmann, F., & McConnell, R. (2011). Residential proximity to freeways and autism in the CHARGE study. Environmental Health Perspectives, 119(6), 873.PubMedCrossRefGoogle Scholar
  328. Vom Saal, F. S., & Bronson, F. (1978). In utero proximity of female mouse fetuses to males: Effect on reproductive performance during later life. Biology of Reproduction, 19(4), 842–853.PubMedCrossRefGoogle Scholar
  329. von Ehrenstein, O. S., Fenton, S. E., Kato, K., Kuklenyik, Z., Calafat, A. M., & Hines, E. P. (2009). Polyfluoroalkyl chemicals in the serum and milk of breastfeeding women. Reproductive Toxicology, 27(3–4), 239–245.CrossRefGoogle Scholar
  330. Vyssotski, A. L., Serkov, A. N., Itskov, P. M., Dell’Omo, G., Latanov, A. V., Wolfer, D. P., et al. (2006). Miniature neurologgers for flying pigeons: Multichannel EEG and action and field potentials in combination with GPS recording. Journal of Neurophysiology, 95(2), 1263–1273.PubMedCrossRefGoogle Scholar
  331. Wang, F., Liu, W., Jin, Y., Dai, J., Yu, W., Liu, X., et al. (2010). Transcriptional effects of prenatal and neonatal exposure to PFOS in developing rat brain. Environmental Science & Technology, 44(5), 1847–1853. doi: 10.1021/es902799f.CrossRefGoogle Scholar
  332. Will, B., Galani, R., Kelche, C., & Rosenzweig, M. R. (2004). Recovery from brain injury in animals: Relative efficacy of environmental enrichment, physical exercise or formal training (1990–2002). Progress in Neurobiology, 72(3), 167–182.PubMedCrossRefGoogle Scholar
  333. Williams, B. M., Luo, Y., Ward, C., Redd, K., Gibson, R., Kuczaj, S. A., et al. (2001). Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity. Physiology & Behavior, 73(4), 649–658.CrossRefGoogle Scholar
  334. Winneke, G. (2011). Developmental aspects of environmental neurotoxicology: Lessons from lead and polychlorinated biphenyls. Journal of the Neurological Sciences, 308(1–2), 9–15. doi: 10.1016/j.jns.2011.05.020.PubMedCrossRefGoogle Scholar
  335. Winslow, J. T., & Insel, T. R. (2002). The social deficits of the oxytocin knockout mouse. Neuropeptides, 36(2–3), 221–229.PubMedCrossRefGoogle Scholar
  336. Wöhr, M., Roullet, F. I., Hung, A. Y., Sheng, M., & Crawley, J. N. (2011a). Communication impairments in mice lacking Shank1: Reduced levels of ultrasonic vocalizations and scent marking behavior. PLoS One, 6(6), e20631.PubMedPubMedCentralCrossRefGoogle Scholar
  337. Wöhr, M., Roullet, F. I., & Crawley, J. N. (2011b). Reduced scent marking and ultrasonic vocalizations in the BTBR T+ tf/J mouse model of autism. Genes, Brain and Behavior, 10(1), 35–43.CrossRefGoogle Scholar
  338. Würbel, H. (2002). Behavioral phenotyping enhanced—beyond (environmental) standardization. Genes, Brain and Behavior, 1(1), 3–8. doi: 10.1046/j.1601-1848.2001.00006.x.CrossRefGoogle Scholar
  339. Yang, M., Perry, K., Weber, M. D., Katz, A. M., & Crawley, J. N. (2011). Social peers rescue autism‐relevant sociability deficits in adolescent mice. Autism Research, 4(1), 17–27.PubMedCrossRefGoogle Scholar
  340. Yauk, C., Polyzos, A., Rowan-Carroll, A., Somers, C. M., Godschalk, R. W., Van Schooten, F. J., et al. (2008). Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proceedings of the National Academy of Sciences, 105(2), 605–610.CrossRefGoogle Scholar
  341. Yeh, C. T., & Yen, G. C. (2005). Effect of vegetables on human phenolsulfotransferases in relation to their antioxidant activity and total phenolics. Free Radical Research, 39(8), 893–904.PubMedCrossRefGoogle Scholar
  342. Young, L. J. (2002). The neurobiology of social recognition, approach, and avoidance. Biological Psychiatry, 51(1), 18–26.PubMedCrossRefGoogle Scholar
  343. Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001). Cellular mechanisms of social attachment. Hormones and Behavior, 40(2), 133–138. doi: 10.1006/hbeh.2001.1691.PubMedCrossRefGoogle Scholar
  344. Yu, M. L., Hsu, C. C., Gladen, B. C., & Rogan, W. J. (1991). In utero PCB/PCDF exposure: Relation of developmental delay to dysmorphology and dose. Neurotoxicology and Teratology, 13(2), 195–202.PubMedCrossRefGoogle Scholar
  345. Yusufishaq, S., & Rosenkranz, J. A. (2013). Post-weaning social isolation impairs observational fear conditioning. Behavioural Brain Research, 242, 142–149.PubMedPubMedCentralCrossRefGoogle Scholar
  346. Zakharova, E., Miller, J., Unterwald, E., Wade, D., & Izenwasser, S. (2009). Social and physical environment alter cocaine conditioned place preference and dopaminergic markers in adolescent male rats. Neuroscience, 163(3), 890–897. doi: 10.1016/j.neuroscience.2009.06.068.PubMedPubMedCentralCrossRefGoogle Scholar
  347. Zeng, H.-C., Zhang, L., Li, Y.-Y., Wang, Y.-J., Xia, W., Lin, Y., et al. (2011). Inflammation-like glial response in rat brain induced by prenatal PFOS exposure. Neurotoxicology, 32((1), 130–139. doi: 10.1016/j.neuro.2010.10.001.CrossRefGoogle Scholar
  348. Zerwas, M., Trouche, S., Richetin, K., Escudé, T., Halley, H., Gerardy-Schahn, R., et al. (2016). Environmental enrichment rescues memory in mice deficient for the polysialytransferase ST8SiaIV. Brain Structure and Function, 221(3), 1591–1605.PubMedCrossRefGoogle Scholar
  349. Zhang, D., Dong, Y., Li, M., & Wang, H. (2012a). A radio-telemetry system for navigation and recording neuronal activity in free-roaming rats. Journal of Bionic Engineering, 9(4), 402–410.CrossRefGoogle Scholar
  350. Zhang, T.-Y., & Meaney, M. J. (2010). Epigenetics and the environmental regulation of the genome and its function. Annual Review of Psychology, 61, 439–466.PubMedCrossRefGoogle Scholar
  351. Zhang, X.-F., Zhang, L.-J., Feng, Y.-N., Chen, B., Feng, Y.-M., Liang, G.-J., et al. (2012b). Bisphenol A exposure modifies DNA methylation of imprint genes in mouse fetal germ cells. Molecular Biology Reports, 39(9), 8621–8628.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Behavioral NeuroscienceOregon Health & Sciences UniversityPortlandUSA

Personalised recommendations