In tribute to Bob Blanchard: Divergent behavioral phenotypes of 16p11.2 deletion mice reared in same-genotype versus mixed-genotype cages

Physiology and Behavior

Volumn 146, Issue , 2015, Pages 16-27

  Yang, Mu ^a   Lewis, Freeman ^a   Foley, Gillian ^a   Crawley, Jacqueline N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

16p11.2; Autism; Mouse models; Mouse social behaviors; Ultrasonic vocalizations

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTISM; BEHAVIOR GENETICS; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; DEPRESSION; EXPLORATORY BEHAVIOR; FEAR; FEMALE; GENE DELETION; GENOTYPE; HETEROZYGOTE; HUMAN; HUMAN CHROMOSOME; LATENT PERIOD; LOXP SITE; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECOGNITION; SOCIAL DOMINANCE; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; SOCIAL STRESS; VOCALIZATION; ANIMAL; ANIMAL BEHAVIOR; CHROMOSOME 16; CHROMOSOME DELETION; DISEASE MODEL; GENETICS; HUMAN RELATION; MAZE TEST; MENTAL DISEASE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VISUAL ADAPTATION;

PHOTOPROTEIN;

ADAPTATION, OCULAR; ANIMALS; BEHAVIOR, ANIMAL; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, PAIR 16; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE; HUMANS; INTERPERSONAL RELATIONS; LUMINESCENT PROTEINS; MALE; MAZE LEARNING; MENTAL DISORDERS; MICE; MICE, TRANSGENIC; PHENOTYPE; RECOGNITION (PSYCHOLOGY); VOCALIZATION, ANIMAL;

EID: 84937966684     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.04.023     Document Type: Article

References (107)

1. Blanchard R.J., McKittrick C.R., Blanchard D.C. Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol. Behav. 2001, 73:261-271.
2. Blanchard D.C., Blanchard R.J., Takahashi L.K., Takahashi T. Septal lesions and aggressive behavior. Behav. Biol. 1977, 21:157-161.
3. Blanchard D.C., Blanchard R.J., Lee E.M., Nakamura S. Defensive behaviors in rats following septal and septal-amygdala lesions. J. Comp. Physiol. Psychol. 1979, 93:378-390.
4. Blanchard D.C., Blanchard R.J., Carobrez Ade P., Veniegas R., Rodgers R.J., Shepherd J.K. MK-801 produces a reduction in anxiety-related antipredator defensiveness in male and female rats and a gender-dependent increase in locomotor behavior. Psychopharmacology 1992, 108:352-362.
5. Blanchard R.J., Blanchard D.C., Flannelly K.J. Social stress, mortality and aggression in colonies and burrowing habitats. Behav. Process. 1985, 11:209-213.
6. Blanchard R.J., Hori K., Flannelly K., Blanchard D.C. The effects of ethanol on the offense and defensive behaviors of male and female rats during group formation. Pharmacol. Biochem. Behav. 1987, 26:61-64.
7. Blanchard R.J., Flannelly K.J., Blanchard D.C. Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiol. Behav. 1988, 43:1-7.
8. Blanchard R.J., Blanchard D.C., Rodgers J., Weiss S.M. The characterization and modelling of antipredator defensive behavior. Neurosci. Biobehav. Rev. 1990, 14:463-472.
9. Yang M., Augustsson H., Markham C.M., Hubbard D.T., Webster D., Wall P.M., et al. The rat exposure test: a model of mouse defensive behaviors. Physiol. Behav. 2004, 81:465-473.
10. Blanchard R.J., Flannelly K.J., Blanchard D.C. Defensive behavior of laboratory and wild Rattus norvegicus. J. Comp. Psychol. 1986, 100:101-107.
11. Blanchard R.J., Hebert M.A., Ferrari P.F., Palanza P., Figueira R., Blanchard D.C., et al. Defensive behaviors in wild and laboratory (Swiss) mice: the mouse defense test battery. Physiol. Behav. 1998, 65:201-209.
12. Blanchard D.C., Griebel G., Blanchard R.J. The Mouse Defense Test Battery: pharmacological and behavioral assays for anxiety and panic. Eur. J. Pharmacol. 2003, 463:97-116.
13. Blanchard R.J., Dulloog L., Markham C., Nishimura O., Nikulina Compton J., Jun A., et al. Sexual and aggressive interactions in a visible burrow system with provisioned burrows. Physiol. Behav. 2001, 72:245-254.
14. Blanchard D.C., Blanchard R.J. What can animal aggression research tell us about human aggression?. Horm. Behav. 2003, 44:171-177.
15. Huerta M., Lord C. Diagnostic evaluation of autism spectrum disorders. Pediatr. Clin. N. Am. 2012, 59:103-111.
16. American Psychiatric Association, Washington, D.C. Diagnostic and Statistical Manual of Mental Disorders (DSM-V) 2013.
17. Huguet G., Ey E., Bourgeron T. The genetic landscapes of autism spectrum disorders. Annu. Rev. Genomics Hum. Genet. 2013, 14:191-213.
18. Jeste S.S., Geschwind D.H. Disentangling the heterogeneity of autism spectrum disorder through genetic findings. Nat. Rev. Neurol. 2014, 10:74-81.
19. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502.
20. Spooren W., Lindemann L., Ghosh A., Santarelli L. Synapse dysfunction in autism: a molecular medicine approach to drug discovery in neurodevelopmental disorders. Trends Pharmacol. Sci. 2012, 33:669-684.
21. Griebel G., Blanchard D.C., Blanchard R.J. Predator-elicited flight responses in Swiss-Webster mice: an experimental model of panic attacks. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 1996, 20:185-205.
22. Holmes P.V., Blanchard D.C., Blanchard R.J., Brady L.S., Crawley J.N. Chronic social stress increases levels of preprogalanin mRNA in the rat locus coeruleus. Pharmacol. Biochem. Behav. 1995, 50:655-660.
23. Arakawa H., Arakawa K., Blanchard D.C., Blanchard R.J. Scent marking behavior in male C57BL/6J mice: sexual and developmental determination. Behav. Brain Res. 2007, 182:73-79.
24. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 1995, 19:303-314.
25. Crawley J.N. Designing mouse behavioral tasks relevant to autistic-like behaviors. Ment. Retard. Dev. Disabil. Res. Rev. 2004, 10:248-258.
26. McFarlane H.G., Kusek G.K., Yang M., Phoenix J.L., Bolivar V.J., Crawley J.N. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 2008, 7:152-163.
27. Moy S.S., Nadler J.J., Perez A., Barbaro R.P., Johns J.M., Magnuson T.R., et al. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004, 3:287-302.
28. Scattoni M.L., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav. 2011, 10:44-56.
29. Crawley J.N. Translational animal models of autism and neurodevelopmental disorders. Dialogues Clin. Neurosci. 2012, 14:293-305.
30. Wohr M., Roullet F.I., Crawley J.N. Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism. Genes Brain Behav. 2011, 10:35-43.
31. Portmann T., Yang M., Mao R., Panagiotakos G., Ellegood J., Dolen G., et al. Behavioral abnormalities and circuit defects in the basal ganglia of a mouse model of 16p11.2 deletion syndrome. Cell Rep. 2014, 7:1077-1092.
32. Yang M., Silverman J.L., Crawley J.N. Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci. 2011, 26. (Chapter 8:Unit 8).
33. Bolivar V.J., Walters S.R., Phoenix J.L. Assessing autism-like behavior in mice: variations in social interactions among inbred strains. Behav. Brain Res. 2007, 176:21-26.
34. Silverman J.L., Smith D.G., Rizzo S.J., Karras M.N., Turner S.M., Tolu S.S., et al. Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism. Sci. Transl. Med. 2012, 4:131ra51.
35. Pearson B.L., Pobbe R.L., Defensor E.B., Oasay L., Bolivar V.J., Blanchard D.C., et al. Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism. Genes Brain Behav. 2011, 10:228-235.
36. Defensor E.B., Pearson B.L., Pobbe R.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. A novel social proximity test suggests patterns of social avoidance and gaze aversion-like behavior in BTBR T+ tf/J mice. Behav. Brain Res. 2011, 217:302-308.
37. Meyza K.Z., Blanchard D.C., Pearson B.L., Pobbe R.L., Blanchard R.J. Fractone-associated N-sulfated heparan sulfate shows reduced quantity in BTBR T+tf/J mice: a strong model of autism. Behav. Brain Res. 2012, 228:247-253.
38. Pearson B.L., Corley M.J., Vasconcellos A., Blanchard D.C., Blanchard R.J. Heparan sulfate deficiency in autistic postmortem brain tissue from the subventricular zone of the lateral ventricles. Behav. Brain Res. 2013, 243:138-145.
39. Pobbe R.L., Pearson B.L., Defensor E.B., Bolivar V.J., Young W.S., Lee H.J., et al. Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors. Horm. Behav. 2012, 61:436-444.
40. Martinez R.C., Carvalho-Netto E.F., Amaral V.C., Nunes-de-Souza R.L., Canteras N.S. Investigation of the hypothalamic defensive system in the mouse. Behav. Brain Res. 2008, 192:185-190.
41. Silva B.A., Mattucci C., Krzywkowski P., Murana E., Illarionova A., Grinevich V., et al. Independent hypothalamic circuits for social and predator fear. Nat. Neurosci. 2013, 16:1731-1733.
42. Yang M., Farrokhi C., Vasconcellos A., Blanchard R.J., Blanchard D.C. Central infusion of ovine CRF (oCRF) potentiates defensive behaviors in CD-1 mice in the Mouse Defense Test Battery (MDTB). Behav. Brain Res. 2006, 171:1-8.
43. Lord C., Bishop S.L. Recent advances in autism research as reflected in DSM-5 criteria for autism spectrum disorder. Annu. Rev. Clin. Psychol. 2015, 53-70.
44. Lai M.C., Lombardo M.V., Baron-Cohen S. Autism. Lancet 2014, 383:896-910.
45. Reilly C., Atkinson P., Das K.B., Chin R.F., Aylett S.E., Burch V., et al. Neurobehavioral comorbidities in children with active epilepsy: a population-based study. Pediatrics 2014, 133(6):1586-1593.
46. Wohr M., Scattoni M.L. Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments. Behav. Brain Res. 2013, 251:5-17.
47. Moy S.S., Nadler J.J., Magnuson T.R., Crawley J.N. Mouse models of autism spectrum disorders: the challenge for behavioral genetics. Am. J. Med. Genet. C: Semin. Med. Genet. 2006, 142C:40-51.
48. Silver L.M. Mouse Genetics Concepts and Applications 1995, Oxford University Press.
49. Noyes R.F., Barrett G.W., Taylor D.H. Social structure of feral house mouse (Mus musculus L.) populations: effects of resource partitioning. Behav. Ecol. Sociobiol. 1982, 10:157-163.
50. Berry R.J. The natural history of the house mouse. Field Study 1970, 3:219-262.
51. Monteiro B.M., Moreira F.A., Massensini A.R., Moraes M.F., Pereira G.S. Enriched environment increases neurogenesis and improves social memory persistence in socially isolated adult mice. Hippocampus 2014, 24:239-248.
52. Arndt S.S., Laarakker M.C., van Lith H.A., van der Staay F.J., Gieling E., Salomons A.R., et al. Individual housing of mice-impact on behaviour and stress responses. Physiol. Behav. 2009, 97:385-393.
53. Brain P. What does individual housing mean to a mouse?. Life Sci. 1975, 16:187-200.
54. Matsumoto K., Pinna G., Puia G., Guidotti A., Costa E. Social isolation stress-induced aggression in mice: a model to study the pharmacology of neurosteroidogenesis. Stress 2005, 8:85-93.
55. O'Donnell V., Blanchard R.J., Blanchard D.C. Mouse aggression increases after 24hours of isolation or housing with females. Behav. Neural Biol. 1981, 32:89-103.
56. Latham N., Mason G. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl. Anim. Behav. Sci. 2004, 86:261-289.
57. Crawley J.N. What's Wrong With My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice 2007, John Wiley & Sons, Inc., Hoboken, NJ. second ed.
58. Van Loo P.L., Van Zutphen L.F., Baumans V. Male management: coping with aggression problems in male laboratory mice. Lab. Anim. 2003, 37:300-313.
59. Smith A.L., Corrow D.J. Modifications to husbandry and housing conditions of laboratory rodents for improved well-being. ILAR 2005, 46:140-147.
60. Yang M., Perry K., Weber M.D., Katz A.M., Crawley J.N. Social peers rescue autism-relevant sociability deficits in adolescent mice. Autism Res. 2011, 4:17-27.
61. Weiss L.A., Shen Y., Korn J.M., Arking D.E., Miller D.T., Fossdal R., et al. Association between microdeletion and microduplication at 16p11.2 and autism. N. Engl. J. Med. 2008, 358:667-675.
62. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., et al. Structural variation of chromosomes in autism spectrum disorder. Am. J. Hum. Genet. 2008, 82:477-488.
63. Blumenthal I., Ragavendran A., Erdin S., Klei L., Sugathan A., Guide J.R., et al. Transcriptional consequences of 16p11.2 deletion and duplication in mouse cortex and multiplex autism families. Am. J. Hum. Genet. 2014, 94:870-883.
64. Tabet A.C., Pilorge M., Delorme R., Amsellem F., Pinard J.M., Leboyer M., et al. Autism multiplex family with 16p11.2p12.2 microduplication syndrome in monozygotic twins and distal 16p11.2 deletion in their brother. Eur. J. Hum. Genet. 2012, 20:540-546.
65. Horev G., Ellegood J., Lerch J.P., Son Y.E., Muthuswamy L., Vogel H., et al. Dosage-dependent phenotypes in models of 16p11.2 lesions found in autism. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17076-17081.
66. Yang M., Mahrt E.J., Lewis F.C., Foley G., Portmann T., Dolmetsch R.E., et al. 16p11.2 deletion syndrome mice display sensory deficits and reduced ultrasonic vocalizations during social interactions. Autism Res. 2015.
67. Pucilowska J., Vithayathil J., Tavares E.J., Kelly C., Karlo J.C., Landreth G.E. The 16p11.2 deletion mouse model of autism exhibits altered cortical progenitor proliferation and brain cytoarchitecture linked to the ERK MAPK pathway. J. Neurosci. 2015, 35:3190-3200.
68. Tian D., Stoppel L.J., Heynen A.J., Lindemann L., Jaeschke G., Mills A.A., et al. Contribution of mGluR5 to pathophysiology in a mouse model of human chromosome 16p11.2 microdeletion. Nat. Neurosci. 2015, 18:182-184.
69. Yang M., Bozdagi O., Scattoni M.L., Wohr M., Roullet F.I., Katz A.M., et al. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. J. Neurosci. 2012, 32:6525-6541.
70. Silverman J.L., Pride M.C., Hayes J.E., Puhger K.R., Butler-Struben H., Baker S., et al. GABA receptor agonist R-baclofen reverses social deficits and reduces repetitive behavior in two mouse models of autism. Neuropsychopharmacology 2015.
71. Brielmaier J., Matteson P.G., Silverman J.L., Senerth J.M., Kelly S., Genestine M., et al. Autism-relevant social abnormalities and cognitive deficits in engrailed-2 knockout mice. PLoS One 2012, 7:e40914.
72. Chadman K.K., Gong S., Scattoni M.L., Boltuck S.E., Gandhy S.U., Heintz N., et al. Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 2008, 1:147-158.
73. Ey E., Yang M., Katz A.M., Woldeyohannes L., Silverman J.L., Leblond C.S., et al. Absence of deficits in social behaviors and ultrasonic vocalizations in later generations of mice lacking neuroligin4. Genes Brain Behav. 2012, 928-941.
74. Yang M., Loureiro D., Kalikhman D., Crawley J.N. Male mice emit distinct ultrasonic vocalizations when the female leaves the social interaction arena. Front. Behav. Neurosci. 2013, 7:159.
75. Silverman J.L., Turner S.M., Barkan C.L., Tolu S.S., Saxena R., Hung A.Y., et al. Sociability and motor functions in Shank1 mutant mice. Brain Res. 2011, 1380:120-137.
76. Brielmaier J., Senerth J.M., Silverman J.L., Matteson P.G., Millonig J.H., DiCicco-Bloom E., et al. Chronic desipramine treatment rescues depression-related, social and cognitive deficits in Engrailed-2 knockout mice. Genes Brain Behav. 2014, 13:286-298.
77. Vogel-Ciernia A., Wood M.A. Examining object location and object recognition memory in mice. Curr. Protoc. Neurosci. 2014, 69. (8 31 1-8 17).
78. Wimmer M.E., Hernandez P.J., Blackwell J., Abel T. Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiol. Aging 2012, 33:2220-2224.
79. Kesner R.P., Hunt M.E., Williams J.M., Long J.M. Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb. Cortex 1996, 6:311-318.
80. Lucas L.R., Celen Z., Tamashiro K.L., Blanchard R.J., Blanchard D.C., Markham C., et al. Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behavior. Neuroscience 2004, 124:449-457.
81. McKittrick C.R., Magarinos A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000, 36:85-94.
82. Albeck D.S., McKittrick C.R., Blanchard D.C., Blanchard R.J., Nikulina J., McEwen B.S., et al. Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain. J. Neurosci. 1997, 17:4895-4903.
83. Spencer R.L., Miller A.H., Moday H., McEwen B.S., Blanchard R.J., Blanchard D.C., et al. Chronic social stress produces reductions in available splenic type II corticosteroid receptor binding and plasma corticosteroid binding globulin levels. Psychoneuroendocrinology 1996, 21:95-109.
84. Blanchard D.C., Spencer R.L., Weiss S.M., Blanchard R.J., McEwen B., Sakai R.R. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 1995, 20:117-134.
85. Chao H.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. The effect of social stress on hippocampal gene expression. Mol. Cell. Neurosci. 1993, 4:543-548.
86. Hardy M.P., Sottas C.M., Ge R., McKittrick C.R., Tamashiro K.L., McEwen B.S., et al. Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biol. Reprod. 2002, 67:1750-1755.
87. Goto T., Kubota Y., Tanaka Y., Iio W., Moriya N., Toyoda A. Subchronic and mild social defeat stress accelerates food intake and body weight gain with polydipsia-like features in mice. Behav. Brain Res. 2014, 270:339-348.
88. Iniguez S.D., Riggs L.M., Nieto S.J., Dayrit G., Zamora N.N., Shawhan K.L., et al. Social defeat stress induces a depression-like phenotype in adolescent male c57BL/6 mice. Stress 2014, 17:247-255.
89. Koolhaas J.M., De Boer S.F., De Rutter A.J., Meerlo P., Sgoifo A. Social stress in rats and mice. Acta Physiol. Scand. Suppl. 1997, 640:69-72.
90. Bartolomucci A., Palanza P., Gaspani L., Limiroli E., Panerai A.E., Ceresini G., et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol. Behav. 2001, 73:401-410.
91. Lumley L.A., Sipos M.L., Charles R.C., Charles R.F., Meyerhoff J.L. Social stress effects on territorial marking and ultrasonic vocalizations in mice. Physiol. Behav. 1999, 67:769-775.
92. D'Amato F.R., Pavone F. Role of anxiety in subordinate male mice sexual behavior. Pharmacol. Biochem. Behav. 1992, 43:181-185.
93. Wang F., Zhu J., Zhu H., Zhang Q., Lin Z., Hu H. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 2011, 334:693-697.
94. Nyby J., Dizinno G.A., Whitney G. Social status and ultrasonic vocalizations of male mice. Behav. Biol. 1976, 18:285-289.
95. Francia N., Cirulli F., Chiarotti F., Antonelli A., Aloe L., Alleva E. Spatial memory deficits in middle-aged mice correlate with lower exploratory activity and a subordinate status: role of hippocampal neurotrophins. Eur. J. Neurosci. 2006, 23:711-728.
96. Fitchett A.E., Collins S.A., Barnard C.J., Cassaday H.J. Subordinate male mice show long-lasting differences in spatial learning that persist when housed alone. Neurobiol. Learn. Mem. 2005, 84:247-251.
97. Krugers H.J., Douma B.R., Andringa G., Bohus B., Korf J., Luiten P.G. Exposure to chronic psychosocial stress and corticosterone in the rat: effects on spatial discrimination learning and hippocampal protein kinase Cgamma immunoreactivity. Hippocampus 1997, 7:427-436.
98. Dubrovina N.I., Tomilenko R.A. Characteristics of extinction of a conditioned passive avoidance reflex in mice with different levels of anxiety. Neurosci. Behav. Physiol. 2007, 37:27-32.
99. Sterlemann V., Rammes G., Wolf M., Liebl C., Ganea K., Muller M.B., et al. Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 2010, 20:540-549.
100. Barnard C.J., Luo N. Acquisition of dominance status affects maze learning in mice. Behav. Process. 2002, 60:53-59.
101. Snyder K.P., Barry M., Valentino R.J. Cognitive impact of social stress and coping strategy throughout development. Psychopharmacology 2015, 232:185-195.
102. Reed D.R., Lawler M.P., Tordoff M.G. Reduced body weight is a common effect of gene knockout in mice. BMC Genet. 2008, 9:4.
103. Branchi I. The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci. Biobehav. Rev. 2009, 33:551-559.
104. Roth T.L., Sweatt J.D. Annual research review: epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development. J. Child Psychol. Psychiatry 2011, 52:398-408.
105. Crews D. Epigenetics and its implications for behavioral neuroendocrinology. Front. Neuroendocrinol. 2008, 29:344-357.
106. Zhang T.Y., Labonte B., Wen X.L., Turecki G., Meaney M.J. Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology 2013, 38:111-123.
107. Champagne F.A. Interplay between social experiences and the genome: epigenetic consequences for behavior. Adv. Genet. 2012, 77:33-57.