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Maternal separation with early weaning: A rodent model providing novel insights into neglect associated developmental deficits

Published online by Cambridge University Press:  15 October 2012

Becky C. Carlyle ,
Alvaro Duque ,
Robert R. Kitchen ,
Kelly A. Bordner ,
Daniel Coman ,
Eliza Doolittle ,
Xenophonios Papademetris ,
Fahmeed Hyder ,
Jane R. Taylor  and
Arthur A. Simen
Becky C. Carlyle*
Affiliation:
Yale University School of Medicine
Alvaro Duque
Affiliation:
Yale University School of Medicine
Robert R. Kitchen
Affiliation:
Yale University School of Medicine
Kelly A. Bordner
Affiliation:
Yale University School of Medicine Southern Connecticut State University
Daniel Coman
Affiliation:
Yale University School of Medicine
Eliza Doolittle
Affiliation:
Yale University School of Medicine
Xenophonios Papademetris
Affiliation:
Yale University School of Medicine
Fahmeed Hyder
Affiliation:
Yale University School of Medicine
Jane R. Taylor
Affiliation:
Yale University School of Medicine
Arthur A. Simen*
Affiliation:
Yale University School of Medicine Merck Research Labs
*
Address correspondence and reprint requests to: Becky C. Carlyle, Connecticut Mental Health Centre, Room 309, 34 Park Street, New Haven, CT 06508; E-mail: becky.carlyle@yale.edu; or Arthur Simen, Merck Research Labs, 351 North Sumneytown Pike, North Wales, PA 19454; E-mail: arthur.simen@merck.com.
Address correspondence and reprint requests to: Becky C. Carlyle, Connecticut Mental Health Centre, Room 309, 34 Park Street, New Haven, CT 06508; E-mail: becky.carlyle@yale.edu; or Arthur Simen, Merck Research Labs, 351 North Sumneytown Pike, North Wales, PA 19454; E-mail: arthur.simen@merck.com.
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Abstract

Child neglect is the most prevalent form of child maltreatment in the United States, and poses a serious public health concern. Children who survive such episodes go on to experience long-lasting psychological and behavioral problems, including higher rates of post-traumatic stress disorder symptoms, depression, alcohol and drug abuse, attention-deficit/hyperactivity disorder, and cognitive deficits. To date, most research into the causes of these life-long problems has focused on well-established targets such as stress responsive systems, including the hypothalamus–pituitary–adrenal axis. Using the maternal separation and early weaning model, we have attempted to provide comprehensive molecular profiling of a model of early-life neglect in an organism amenable to genomic manipulation: the mouse. In this article, we report new findings generated with this model using chromatin immunoprecipitation sequencing, diffuse tensor magnetic resonance imaging, and behavioral analyses. We also review the validity of the maternal separation and early weaning model, which reflects behavioral deficits observed in neglected humans including hyperactivity, anxiety, and attentional deficits. Finally, we summarize the molecular characterization of these animals, including RNA profiling and label-free proteomics, which highlight protein translation and myelination as novel pathways of interest.

Type
Articles
Information
Development and Psychopathology , Volume 24 , Issue 4: Contributions of the Genetic/Genomic Sciences to Developmental Psychopathology , November 2012 , pp. 1401 - 1416
Copyright
Copyright © Cambridge University Press 2012

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References

Agid, O., Shapira, B., Zislin, J., Ritsner, M., Hanin, B., Murad, H., et al. (1999). Environment and vulnerability to major psychiatric illness: A case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Molecular Psychiatry, 4, 163–72.Google Scholar
Akbarian, S., & Huang, H.-S. (2009). Epigenetic regulation in human brain-focus on histone lysine methylation. Biological Psychiatry, 65, 198–203.Google Scholar
Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., et al. (2006). The enduring effects of abuse and related adverse experiences in childhood: A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience, 256, 174–186.Google Scholar
Anders, S., & Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biology, 11, R106.Google Scholar
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998). Do early-life events permanently alter behavioral and hormonal responses to stressors? International Journal of Developmental Neuroscience, 16, 149–164.CrossRefGoogle ScholarPubMed
Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., & Kuster, B. (2007). Quantitative mass spectrometry in proteomics: a critical review. Analytical and Bioanalytical Chemistry, 389, 1017–1031.Google Scholar
Bari, A., & Robbins, T. W. (2011). Animal models of ADHD. Current Topics in Behavioral Neurosciences, 7, 149–185.Google Scholar
Bartsch, S., Montag, D., Schachner, M., & Bartsch, U. (1997). Increased number of unmyelinated axons in optic nerves of adult mice deficient in the myelin-associated glycoprotein (MAG). Brain Research, 762, 231–234.Google Scholar
Beers, S. R., & DeBellis, M. D. (2002). Neuropsychological function in children with maltreatment-related posttraumatic stress disorder. American Journal of Psychiatry, 159, 483–486.Google Scholar
Blundell, J., Kouser, M., & Powell, C. M. (2008). Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation. Neurobiology of Learning and Memory, 90, 28–35.Google Scholar
Bordner, K. A., George, E. D., Carlyle, B. C., Duque, A., Kitchen, R. R., Lam, T. T., et al. (2011). Functional genomic and proteomic analysis reveals disruption of myelin-related genes and translation in a mouse model of early life neglect. Frontiers in Psychiatry/Frontiers Research Foundation, 2, 18.Google Scholar
Bordner, K. A., Kitchen, R. R., Carlyle, B., George, E. D., Mahajan, M. C., Mane, S. M., et al. (2011). Parallel declines in cognition, motivation, and locomotion in aging mice: Association with immune gene upregulation in the medial prefrontal cortex. Experimental Gerontology, 46, 643–659.Google Scholar
Bradl, M., & Lassmann, H. (2010). Oligodendrocytes: Biology and pathology. Acta Neuropathologica, 119, 37–53.CrossRefGoogle Scholar
Braff, D. L., Geyer, M. A., & Swerdlow, N. R. (2001). Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies. Psychopharmacology, 156, 234–258.Google Scholar
Bremner, J. D. (2006a). Traumatic stress: effects on the brain. Dialogues in Clinical Neuroscience, 8, 445–461.CrossRefGoogle ScholarPubMed
Bremner, J. D. (2006b). The relationship between cognitive and brain changes in posttraumatic stress disorder. Annals of the New York Academy of Sciences, 1071, 80–86.Google Scholar
Buschman, T. J., & Miller, E. K. (2007). Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science, 315(5820), 1860–1862.Google Scholar
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., et al. (2001). Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder. Biological Psychiatry, 50, 943–951.Google Scholar
Chahboune, H., Mishra, A. M., DeSalvo, M. N., Staib, L. H., Purcaro, M., Scheinost, D., et al. (2009). DTI abnormalities in anterior corpus callosum of rats with spike-wave epilepsy. NeuroImage, 47, 459–466.Google Scholar
Chahboune, H., Ment, L. R., Stewart, W. B., Ma, X., Rothman, D. L., & Hyder, F. (2007). Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging. NMR in Biomedicine, 20, 375–382.Google Scholar
Chahboune, H., Ment, L. R., Stewart, W. B., Rothman, D. L., Vaccarino, F. M., Hyder, F., et al. (2009). Hypoxic injury during neonatal development in murine brain: Correlation between in vivo DTI findings and behavioral assessment. Cerebral Cortex, 19, 2891–2901.Google Scholar
Cheung, I., Shulha, H. P., Jiang, Y., Matevossian, A., Wang, J., Weng, Z., et al. (2010). Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proceedings of the National Academy of Sciences, 107, 8824–8829.Google Scholar
Chiu, K., Lau, W. M., Lau, H. T., So, K.-F., & Chang, R. C.-C. (2007). Micro-dissection of rat brain for RNA or protein extraction from specific brain region. Journal of Visualized Experiments, 7, 269.Google Scholar
Cierpial, M. A., Shasby, D. E., Murphy, C. A., Borom, A. H., Stewart, R. E., Swithers, S. E et al. (1989). Open-field behavior of spontaneously hypertensive and wistar-kyoto normotensive rats: Effects of reciprocal cross-fostering. Behavioral and Neural Biology, 51, 203–210.Google Scholar
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004). Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates. Neuroscience & Biobehavioral Reviews, 28, 771–784.Google Scholar
Das, S., & Maitra, U. (2000). Mutational analysis of mammalian translation initiation factor 5 (eIF5): Role of interaction between the beta subunit of eIF2 and eIF5 in eIF5 function in vitro and in vivo. Molecular and Cellular Biology, 20, 3942–3950.Google Scholar
Davids, E., Zhang, K., Tarazi, F. I., & Baldessarini, R. J. (2003). Animal models of attention-deficit hyperactivity disorder. Brain Research. Brain Research Reviews, 42, 1–21.Google Scholar
DeBellis, M. D. (2001). Developmental traumatology: A contributory mechanism for alcohol and substance use disorders. Psychoneuroendocrinology, 27, 155–170.CrossRefGoogle Scholar
DeBellis, M. D. (2005). The psychobiology of neglect. Child Maltreatment, 10, 150–172.Google Scholar
DeBellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N., Boring, A. M., et al. (1999). A. E. Bennett Research Award. Developmental traumatology. Part II: Brain development. Biological Psychiatry, 45, 1271–1284.CrossRefGoogle Scholar
DeBellis, M. D., Keshavan, M. S., Spencer, S., & Hall, J. (2000). N-Acetylaspartate concentration in the anterior cingulate of maltreated children and adolescents with PTSD. American Journal of Psychiatry, 157, 1175–1177.Google Scholar
DeBellis, M. D., Keshavan, M. S., Shifflett, H., Iyengar, S., Beers, S. R., Hall, J., et al. (2002). Brain structures in pediatric maltreatment-related posttraumatic stress disorder: A sociodemographically matched study. Biological Psychiatry, 52, 1066–1078.Google Scholar
DeBellis, M. D., & Thomas, L. A. (2003). Biologic findings of post-traumatic stress disorder and child maltreatment. Current Psychiatry Reports, 5, 108–117.Google Scholar
de Kloet, E. R., Sibug, R. M., Helmerhorst, F. M., Schmidt, M. V., & Schmidt, M. (2005). Stress, genes and the mechanism of programming the brain for later life. Neuroscience and Biobehavioral Reviews, 29, 271–281.Google Scholar
Dugas, J. C., Tai, Y. C., Speed, T. P., Ngai, J., & Barres, B. A. (2006). Functional genomic analysis of oligodendrocyte differentiation. Journal of Neuroscience, 26, 10967–10983.Google Scholar
Duque, A., Coman, D., Carlyle, B. C., Bordner, K. A., George, E. D., Papademetris, X., et al. (2012). Neuroanatomical changes in a mouse model of early life neglect. Brain Structure and Function, 217, 459–472.Google Scholar
Edgar, J. M., McLaughlin, M., Barrie, J. A., McCulloch, M. C., Garbern, J., & Griffiths, I. R. (2004). Age-related axonal and myelin changes in the rumpshaker mutation of the Plp gene. Acta Neuropathologica, 107, 331–335.Google Scholar
Ellenbroek, B. A., & Cools, A. R. (2002). Early maternal deprivation and prepulse inhibition: The role of the postdeprivation environment. Pharmacology, Biochemistry, & Behavior, 73, 177–184.Google Scholar
Ellenbroek, B. A., de Bruin, N. M. W. J., van den Kroonenburg, P. T. J. M., van Luijtelaar, E. L. J. M., & Cools, A. R. (2004). The effects of early maternal deprivation on auditory information processing in adult Wistar rats. Biological Psychiatry, 55, 701–707.Google Scholar
Famularo, R., Kinscherff, R., & Fenton, T. (1992). Psychiatric diagnoses of maltreated children: Preliminary findings. Journal of the American Academy of Child & Adolescent Psychiatry, 31, 863–867.Google Scholar
Ferguson, S. A. (1996). Neuroanatomical and functional alterations resulting from early postnatal cerebellar insults in rodents. Pharmacology, Biochemistry, & Behavior, 55, 663–671.Google Scholar
Fields, R. D. (2008). White matter in learning, cognition and psychiatric disorders. Trends in Neurosciences, 31, 361–370.Google Scholar
Ford, J. D., Racusin, R., Ellis, C. G., Daviss, W. B., Reiser, J., Fleischer, A., et al. (2000). Child maltreatment, other trauma exposure, and posttraumatic symptomatology among children with oppositional defiant and attention deficit hyperactivity disorders. Child Maltreatment, 5, 205–217.CrossRefGoogle ScholarPubMed
Frodl, T., Reinhold, E., Koutsouleris, N., Reiser, M., & Meisenzahl, E. M. (2010). Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. Journal of Psychiatric Research, 44, 799–807.Google Scholar
Gentsch, C., Lichtsteiner, M., & Feer, H. (1987). Open field and elevated plus-maze: A behavioural comparison between spontaneously hypertensive (SHR) and Wistar–Kyoto (WKY) rats and the effects of chlordiazepoxide. Behavioural Brain Research, 25, 101–107.Google Scholar
George, E. D., Bordner, K. A., Elwafi, H. M., & Simen, A. A. (2010). Maternal separation with early weaning: A novel mouse model of early life neglect. BMC Neuroscience, 11, 123.Google Scholar
Gibb, B. E., Chelminski, I., & Zimmerman, M. (2007). Childhood emotional, physical, and sexual abuse, and diagnoses of depressive and anxiety disorders in adult psychiatric outpatients. Depression and Anxiety, 24, 256–263.Google Scholar
Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: Etymology and strategic intentions. American Journal of Psychiatry, 160, 636–645.Google Scholar
Griffiths, I., Klugmann, M., Anderson, T., Yool, D., Thomson, C., Schwab, M. H., et al. (1998). Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science, 280(5369), 1610–163.Google Scholar
Gupta, A., & Tsai, L.-H. (2003). Cyclin-dependent kinase 5 and neuronal migration in the neocortex. Neurosignals, 12, 173–179.Google Scholar
Hasan, K. M., Basser, P. J., Parker, D. L., & Alexander, A. L. (2001). Analytical computation of the eigenvalues and eigenvectors in DT-MRI. Journal of Magnetic Resonance, 152, 41–47.Google Scholar
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039.Google Scholar
Hildyard, K. L., & Wolfe, D. A. (2002). Child neglect: Developmental issues and outcomes. Child Abuse and Neglect, 26, 679–695.Google Scholar
Hinshaw, S. P. (2002). Preadolescent girls with attention-deficit/hyperactivity disorder: I. Background characteristics, comorbidity, cognitive and social functioning, and parenting practices. Journal of Consulting and Clinical Psychology, 70, 1086–1098.Google Scholar
Hodos, W., & Kalman, G. (1963). Effects of increment size and reinforcer volume on progressive ratio performance. Journal of the Experimental Analysis of Behavior, 6, 387–392.Google Scholar
Hoeffer, C. A., & Klann, E. (2010). mTOR signaling: At the crossroads of plasticity, memory and disease. Trends in Neurosciences, 33, 67–75.Google Scholar
Holmes, A., le Guisquet, A. M., Vogel, E., Millstein, R. A., Leman, S., & Belzung, C. (2005). Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neuroscience & Biobehavioral Reviews, 29, 1335–1346.Google Scholar
Huang, H.-S., Matevossian, A., Whittle, C., Kim, S. Y., Schumacher, A., Baker, S. P., et al. (2007). Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. Journal of Neuroscience, 27, 11254–11262.CrossRefGoogle ScholarPubMed
Hulvershorn, L. A., Cullen, K., & Anand, A. (2011). Toward dysfunctional connectivity: A review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging and Behavior, 5, 307–328.Google Scholar
Hunter, R. G., McCarthy, K. J., Milne, T. A., Pfaff, D. W., & McEwen, B. S. (2009). Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proceedings of the National Academy of Sciences, 106, 20912–20917.Google Scholar
Inoue, K. (2005). PLP1-related inherited dysmyelinating disorders: Pelizaeus–Merzbacher disease and spastic paraplegia type 2. Neurogenetics, 6, 1–16.Google Scholar
Jones, D. K., Horsfield, M. A., & Simmons, A. (1999). Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magnetic Resonance in Medicine, 42, 515–525.Google Scholar
Kapp, L. D., & Lorsch, J. R. (2004). The molecular mechanics of eukaryotic translation. Annual Review of Biochemistry, 73, 657–704.Google Scholar
Kaufman, J. (1991). Depressive disorders in maltreated children. Journal of the American Academy of Child & Adolescent Psychiatry, 30, 257–265.Google Scholar
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.Google Scholar
Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P. E., et al. (2003). Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nature Genetics, 33, 366–374.Google Scholar
Lee, D., Rushworth, M. F. S., Walton, M. E., Watanabe, M., & Sakagami, M. (2007). Functional specialization of the primate frontal cortex during decision making. Journal of Neuroscience, 27, 8170–8173.Google Scholar
Lee, M. G., Wynder, C., Schmidt, D. M., McCafferty, D. G., & Shiekhattar, R. (2006). Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chemistry and Biology, 13, 563–567.Google Scholar
Lehman, B. J., Taylor, S. E., Kiefe, C. I., & Seeman, T. E. (2009). Relationship of early life stress and psychological functioning to blood pressure in the CARDIA study. Health Psychology, 28, 338–346.Google Scholar
Li, B., Carey, M., & Workman, J. L. (2007). The role of chromatin during transcription. Cell, 128, 707–719.Google Scholar
Lovic, V., & Fleming, A. S. (2004). Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behavioural Brain Research, 148, 209–219.Google Scholar
Macrì, S., & Laviola, G. (2004). Single episode of maternal deprivation and adult depressive profile in mice: Interaction with cannabinoid exposure during adolescence. Behavioural Brain Research, 154, 231–238.Google Scholar
Magara, F., Ricceri, L., Wolfer, D. P., & Lipp, H. P. (2000). The acallosal mouse strain I/LnJ: A putative model of ADHD? Neuroscience & Biobehavioral Reviews, 24, 45–50.Google Scholar
Mamah, D., Conturo, T. E., Harms, M. P., Akbudak, E., Wang, L., McMichael, A. R., et al. (2010). Anterior thalamic radiation integrity in schizophrenia: A diffusion-tensor imaging study. Psychiatry Research, 183, 144–150.Google Scholar
Mathews, C. A., Kaur, N., & Stein, M. B. (2008). Childhood trauma and obsessive–compulsive symptoms. Depression and Anxiety, 25, 742–751.Google Scholar
Millstein, R. A., Ralph, R. J., Yang, R. J., & Holmes, A. (2006). Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes, Brain, & Behavior, 5, 346–354.Google Scholar
Millstein, R. A., & Holmes, A. (2007). Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neuroscience & Biobehavioral Reviews, 31, 3–17.Google Scholar
Moradi, A. R., Doost, H. T., Taghavi, M. R., Yule, W., & Dalgleish, T. (1999). Everyday memory deficits in children and adolescents with PTSD: Performance on the Rivermead Behavioural Memory Test. Journal of Child Psychology and Psychiatry and Allied Disciplines, 40, 357–361.CrossRefGoogle ScholarPubMed
Nave, K.-A., & Trapp, B. D. (2008). Axon-glial signaling and the glial support of axon function. Annual Review of Neuroscience, 31, 535–561.Google Scholar
Ouyang, L., Fang, X., Mercy, J., Perou, R., & Grosse, S. D. (2008). Attention-deficit/hyperactivity disorder symptoms and child maltreatment: A population-based study. Journal of Pediatrics, 153, 851–856.Google Scholar
Parfitt, D. B., Levin, J. K., Saltstein, K. P., Klayman, A. S., Greer, L. M., & Helmreich, D. L. (2004). Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Research, 1016, 111–118.Google Scholar
Parfitt, D. B., Walton, J. R., Corriveau, E. A., & Helmreich, D. L. (2007). Early life stress effects on adult stress-induced corticosterone secretion and anxiety-like behavior in the C57BL/6 mouse are not as robust as initially thought. Hormones and Behavior, 52, 417–426.Google Scholar
Pascual, R., & Zamora-León, S. P. (2007). Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiologiae Experimentalis, 67, 471–479.Google Scholar
Pearson, W. R., Wood, T., Zhang, Z., & Miller, W. (1997). Comparison of DNA sequences with protein sequences. Genomics, 46, 24–36.Google Scholar
Pinheiro, D. B. J. (2000). NLME: Mixed-effects models in S and S-PLUS. New York: Springer.Google Scholar
Readhead, C., Popko, B., Takahashi, N., Shine, H. D., Saavedra, R. A., Sidman, R. L., et al. (1987). Expression of a myelin basic protein gene in transgenic shiverer mice: Correction of the dysmyelinating phenotype. Cell, 48, 703–712.Google Scholar
Robbins, T. W. (2002). The 5-choice serial reaction time task: Behavioural pharmacology and functional neurochemistry. Psychopharmacology, 163, 362–380.Google Scholar
Romeo, R. D., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., & Brake, W. G. (2003). Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Hormones and Behavior, 43, 561–567.Google Scholar
Rozowsky, J., Euskirchen, G., Auerbach, R. K., Zhang, Z. D., Gibson, T., Bjornson, R., et al. (2009). PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nature Biotechnology, 27, 66–75.Google Scholar
Sánchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13, 419–449.Google Scholar
Schnaar, R. L., & Lopez, P. H. H. (2009). Myelin-associated glycoprotein and its axonal receptors. Journal of Neuroscience Research, 87, 3267–3276.Google Scholar
Sengupta, S., Peterson, T. R., & Sabatini, D. M. (2010). Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Molecular Cell, 40, 310–322.Google Scholar
Shaw, P., Lerch, J., Greenstein, D., Sharp, W., Clasen, L., Evans, A., et al. (2006). Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 63, 540–549.Google Scholar
Sprooten, E., Sussmann, J. E., Clugston, A., Peel, A., McKirdy, J., Moorhead, T. W. J., et al. (2011). White matter integrity in individuals at high genetic risk of bipolar disorder. Biological Psychiatry, 70, 350–356.Google Scholar
Sun, C., Todorovic, A., Querol-Audí, J., Bai, Y., Villa, N., Snyder, M., et al. (2011). Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3). Proceedings of the National Academy of Sciences, 108, 20473–20478.Google Scholar
Sussmann, J. E., Lymer, G. K. S., McKirdy, J., Moorhead, T. W. J., Muñoz Maniega, S., Job, D., et al. (2009). White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disorders, 11, 11–18.Google Scholar
Szyf, M. (2009). Epigenetics, DNA methylation, and chromatin modifying drugs. Annual Review of Pharmacology and Toxicology, 49, 243–263.Google Scholar
Team, R. D. C. (2011). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Teicher, M. H., Ito, Y., Glod, C. A., Andersen, S. L., Dumont, N., & Ackerman, E. (1997). Preliminary evidence for abnormal cortical development in physically and sexually abused children using EEG coherence and MRI. Annals of the New York Academy of Sciences, 821, 160–175.Google Scholar
Teicher, M. H., Anderson, C. M., & Polcari, A. (2012). Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proceedings of the National Academy of Sciences, 109, E563–E572.Google Scholar
Teicher, M. H., Dumont, N. L., Ito, Y., Vaituzis, C., Giedd, J. N., & Andersen, S. L. (2004). Childhood neglect is associated with reduced corpus callosum area. Biological Psychiatry, 56, 80–85.Google Scholar
Thompson-Schill, S. L., Jonides, J., Marshuetz, C., Smith, E. E., D'Esposito, M., Kan, I. P., et al. (2002). Effects of frontal lobe damage on interference effects in working memory. Cognitive, Affective, and Behavioral Neuroscience, 2, 109–120.Google Scholar
Togao, O., Yoshiura, T., Nakao, T., Nabeyama, M., Sanematsu, H., Nakagawa, A., et al. (2010). Regional gray and white matter volume abnormalities in obsessive–compulsive disorder: A voxel-based morphometry study. Psychiatry Research, 184, 29–37.Google Scholar
Tomoda, A., Suzuki, H., Rabi, K., Sheu, Y.-S., Polcari, A., & Teicher, M. H. (2009). Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment. NeuroImage, 47(Suppl. 2), T66–T71.Google Scholar
US Department of Health and Human Services. (2011). Child maltreatment 2010.Washington, DC: US Government Printing Office.Google Scholar
van Harmelen, A.-L., van Tol, M.-J., van der Wee, N. J. A., Veltman, D. J., Aleman, A., Spinhoven, P., et al. (2010). Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment. Biological Psychiatry, 68, 832–838.Google Scholar
Veenema, A. H. (2009). Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: What can we learn from animal models? Frontiers in Neuroendocrinology, 30, 497–518.Google Scholar
Velíšek, L., Shang, E., Velíšková, J., Chachua, T., Macchiarulo, S., Maglakelidze, G., et al. (2011). GABAergic neuron deficit as an idiopathic generalized epilepsy mechanism: The role of BRD2 haploinsufficiency in juvenile myoclonic epilepsy. PloS One, 6, e23656.Google Scholar
Venerosi, A., Cirulli, F., Capone, F., & Alleva, E. (2003). Prolonged perinatal AZT administration and early maternal separation: Effects on social and emotional behaviour of periadolescent mice. Pharmacology, Biochemistry, & Behavior, 74, 671–681.Google Scholar
Vermetten, E., & Bremner, J. D. (2002). Circuits and systems in stress. I. Preclinical studies. Depression and Anxiety, 15, 126–147.Google Scholar
Wang, P., Lin, C., Smith, E. R., Guo, H., Sanderson, B. W., Wu, M., et al. (2009). Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Molecular and Cellular Biology, 29, 6074–6085.Google Scholar
Watts-English, T., Fortson, B. L., Gibler, N., Hooper, S. R., & De Bellis, M. D. (2006). The psychobiology of maltreatment in childhood. Journal of Social Issues, 62, 717–736.Google Scholar
Woon, F. L., & Hedges, D. W. (2008). Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: A meta-analysis. Hippocampus, 18, 729–736.Google Scholar
Wu, M., Hernandez, M., Shen, S., Sabo, J. K., Kelkar, D., Wang, J., et al. (2012). Differential modulation of the oligodendrocyte transcriptome by Sonic Hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. Journal of Neuroscience, 32, 6651–6664.Google Scholar
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