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Childhood maltreatment is associated with altered frontolimbic neurobiological activity during wakefulness in adulthood

Published online by Cambridge University Press:  22 July 2015

Salvatore P. Insana ,
Layla Banihashemi ,
Ryan J. Herringa ,
David J. Kolko  and
Anne Germain
Salvatore P. Insana
Affiliation:
University of Pittsburgh School of Medicine
Layla Banihashemi
Affiliation:
University of Pittsburgh School of Medicine
Ryan J. Herringa
Affiliation:
University of Pittsburgh School of Medicine University of Wisconsin School of Medicine and Public Health
David J. Kolko
Affiliation:
University of Pittsburgh School of Medicine
Anne Germain*
Affiliation:
University of Pittsburgh School of Medicine
*
Address correspondence and reprint requests to: Anne Germain, Western Psychiatric Institute and Clinic, University of Pittsburgh, 3811 O'Hara Street, Sterling Plaza 239, Pittsburgh, PA 15213; E-mail: [email protected].
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Abstract

Childhood maltreatment can disturb brain development and subsequently lead to adverse socioemotional and mental health problems across the life span. The long-term association between childhood maltreatment and resting–wake brain activity during adulthood is unknown and was examined in the current study. Forty-one medically stable and medication-free military veterans (M = 29.31 ± 6.01 years, 78% male) completed a battery of clinical assessments and had [18F]-fluorodeoxyglucose positron emission tomography neuroimaging scans during quiet wakefulness. After statistically adjusting for later-life trauma and mental health problems, childhood maltreatment was negatively associated with brain activity within a priori defined regions that included the left orbital frontal cortex and left hippocampus. Childhood maltreatment was significantly associated with increased and decreased brain activity within six additional whole-brain clusters that included the frontal, parietal–temporal, cerebellar, limbic, and midbrain regions. Childhood maltreatment is associated with altered neural activity in adulthood within regions that are involved in executive functioning and cognitive control, socioemotional processes, autonomic functions, and sleep/wake regulation. This study provides support for taking a life span developmental approach to understanding the effects of early-life maltreatment on later-life neurobiology, socioemotional functioning, and mental health.

Type
Regular Articles
Information
Development and Psychopathology , Volume 28 , Issue 2 , May 2016 , pp. 551 - 564
Copyright
Copyright © Cambridge University Press 2015 

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References

Adler, C. M., DelBello, M. P., & Strakowski, S. M. (2006). Brain network dysfunction in bipolar disorder. CNS Spectrums, 11, 312–320.Google Scholar
Allen, G., McColl, R., Barnard, H., Ringe, W. K., Fleckenstein, J., & Cullum, C. M. (2005). Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. NeuroImage, 28, 39–48.Google Scholar
Allman, J. M., Hakeem, A., Erwin, J. M., Nimchinsky, E., & Hof, P. (2001). The anterior cingulate cortex: The evolution of an interface between emotion and cognition. Annals of the New York Academy of Sciences, 935, 107–117.CrossRefGoogle ScholarPubMed
Andersen, S. L., & Teicher, M. H. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neurosciences, 31, 183–191.Google Scholar
Anderson, C. M., Teicher, M. H., Polcari, A., & Renshaw, P. F. (2002). Abnormal T2 relaxation time in the cerebellar vermis of adults sexually abused in childhood: Potential role of the vermis in stress-enhanced risk for drug abuse. Psychoneuroendocrinology, 27, 231–244.Google Scholar
Andreasen, N. C., Arndt, S., Cizadlo, T., O'Leary, D. S., Watkins, G. L., & Ponto, L. L., et al. (1996). Sample size and statistical power in [15O]H2O studies of human cognition. Journal of Cerebral Blood Flow and Metabolism, 16, 804–816.CrossRefGoogle ScholarPubMed
Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry—The methods. NeuroImage, 11, 805–821.CrossRefGoogle ScholarPubMed
Baker, L. M., Williams, L. M., Korgaonkar, M. S., Cohen, R. A., Heaps, J. M., & Paul, R. H. (2013). Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging and Behavior, 7, 196–203.Google Scholar
Balleine, B. W., Delgado, M. R., & Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. Journal of Neuroscience, 27, 8161–8165.Google Scholar
Banihashemi, L., Sheu, L. K., Midei, A. J., & Gianaros, P. J. (2014). Childhood physical abuse predicts stressor-evoked activity within central visceral control regions. Social Cognitive and Affective Neuroscience. Advance online publication.Google Scholar
Baumann, O., & Mattingley, J. B. (2012). Functional topography of primary emotion processing in the human cerebellum. NeuroImage, 61, 805–811.Google Scholar
Baxter, L. R. Jr., Phelps, M. E., Mazziotta, J. C., Schwartz, J. M., Gerner, R. H., & Selin, C. E., et al. (1985). Cerebral metabolic rates for glucose in mood disorders: Studies with positron emission tomography and fluorodeoxyglucose F 18. Archives of General Psychiatry, 42, 441–447.Google Scholar
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561–571.CrossRefGoogle ScholarPubMed
Bernstein, D. P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., Wenzel, K., et al. (1994). Initial reliability and validity of a new retrospective measure of child abuse and neglect. Amercian Journal of Psychiatry, 151, 1132–1136.Google Scholar
Blake, D. K., Weathers, F. W., Nagy, L. M., Kaloupek, D. G., Klauminzer, G., Charney, D. S., et al. (1990). A clinician rating scale for assessing current and lifetime PTSD: The CAPS-1. Behavior Therapist, 13, 187–188.Google Scholar
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012). Control of sleep and wakefulness. Physiology Review, 92, 1087–1187.Google Scholar
Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Science, 4, 215–222.Google Scholar
Card, J. P., Levitt, P., Gluhovsky, M., & Rinaman, L. (2005). Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. Journal of Neuroscience, 25, 9102–9111.Google Scholar
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129, 564–583.Google Scholar
Chugani, H. T., Behen, M. E., Muzik, O., Juhasz, C., Nagy, F., & Chugani, D. C. (2001). Local brain functional activity following early deprivation: A study of postinstitutionalized Romanian orphans. NeuroImage, 14, 1290–1301.Google Scholar
Cicchetti, D., & Cannon, T. D. (1999). Neurodevelopmental processes in the ontogenesis and epigenesis of psychopathology. Development and Psychopathology, 11, 375–393.Google Scholar
Cohen, J. (1988). Statistical power analysis for behavioral sciences (2nd ed.) Hillsdale, NJ: Erlbaum.Google Scholar
Crockford, D. N., Goodyear, B., Edwards, J., Quickfall, J., & el-Guebaly, N. (2005). Cue-induced brain activity in pathological gamblers. Biological Psychiatry, 58, 787–795.Google Scholar
Cuijpers, P., Smit, F., Unger, F., Stikkelbroek, Y., Ten, H. M., & de, G. R. (2011). The disease burden of childhood adversities in adults: A population-based study. Child Abuse and Neglect, 35, 937–945.Google Scholar
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., et al. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286–293.Google Scholar
Davidson, R. J. (2002). Anxiety and affective style: Role of prefrontal cortex and amygdala. Biological Psychiatry, 51, 68–80.CrossRefGoogle ScholarPubMed
De Bellis, 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
De Bellis, M. D., & Kuchibhatla, M. (2006). Cerebellar volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry, 60, 697–703.Google Scholar
De Brito, S. A., Viding, E., Sebastian, C. L., Kelly, P. A., Mechelli, A., Maris, H., et al. (2013). Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children. Journal of Child Psychology and Psychiatry, 54, 105–112.Google Scholar
Edmiston, E. E., Wang, F., Mazure, C. M., Guiney, J., Sinha, R., Mayes, L. C., et al. (2011). Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. Archives of Pediatric and Adolescent Medicine, 165, 1069–1077. doi:10.1001/archpediatrics.2011.565 Google Scholar
Edwards, V. J., Holden, G. W., Felitti, V. J., & Anda, R. F. (2003). Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: Results from the adverse childhood experiences study. American Journal of Psychiatry, 160, 1453–1460.Google Scholar
Fleisher, A. S., Sherzai, A., Taylor, C., Langbaum, J. B., Chen, K., & Buxton, R. B. (2009). Resting-state BOLD networks versus task-associated functional MRI for distinguishing Alzheimer's disease risk groups. NeuroImage, 47, 1678–1690.Google Scholar
Friston, K. J., Ashburner, J. T., Kiebel, S. J., Nichols, T. E., & Penny, W. D. (2006). Statistical parametric mapping: The analysis of functional brain images. Oxford: Elsevier.Google Scholar
Funahashi, S. (2001). Neuronal mechanisms of executive control by the prefrontal cortex. Neuroscience Research, 39, 147–165.Google Scholar
Ganzel, B. L., Kim, P., Gilmore, H., Tottenham, N., & Temple, E. (2013). Stress and the healthy adolescent brain: Evidence for the neural embedding of life events. Development and Psychopathology, 25, 879–889.Google Scholar
Germain, A. (2013). Sleep disturbances as the hallmark of PTSD: Where are we now? American Journal of Psychiatry, 170, 372–382.Google Scholar
Germain, A., Buysse, D. J., & Nofzinger, E. (2008). Sleep-specific mechanisms underlying posttraumatic stress disorder: Integrative review and neurobiological hypotheses. Sleep Medicine Reviews, 12, 185–195.Google Scholar
Germain, A., James, J., Insana, S. P., Oommen, M., Price, J., & Nofzinger, E. (2013). A window into the invisible wound of war: Functional neuroimaging of REM sleep in returning combat veterans with PTSD. Psychiatry Research: Neuroimaging, 211, 176–179.Google Scholar
Gewirtz, J. C., McNish, K. A., & Davis, M. (2000). Is the hippocampus necessary for contextual fear conditioning? Behavioural Brain Research, 110, 83–95.Google Scholar
Gianaros, P. J., Horenstein, J. A., Hariri, A. R., Sheu, L. K., Manuck, S. B., Matthews, K. A., et al. (2008). Potential neural embedding of parental social standing. Social, Cognitive, and Affective Neuroscience, 3, 91–96.CrossRefGoogle ScholarPubMed
Gianaros, P. J., Manuck, S. B., Sheu, L. K., Kuan, D. C., Votruba-Drzal, E., Craig, A. E., et al. (2011). Parental education predicts corticostriatal functionality in adulthood. Cerebral Cortex, 21, 896–910.Google Scholar
Gilbert, R., Widom, C. S., Browne, K., Fergusson, D., Webb, E., & Janson, S. (2009). Burden and consequences of child maltreatment in high-income countries. Lancet, 373, 68–81.Google Scholar
Glickstein, M. (2007). What does the cerebellum really do? Current Biology, 17, R824–R827.Google Scholar
Green, B. L. (1996). Trauma History Questionnaire. In Stamm, B. H. (Ed.), Measurement of stress, trauma and adaptation (pp. 366–369). Lutherville, MD: Sidran Press.Google Scholar
Hackman, D. A., Farah, M. J., & Meaney, M. J. (2010). Socioeconomic status and the brain: Mechanistic insights from human and animal research. Nature Reviews Neuroscience, 11, 651–659.Google Scholar
Hanson, J. L., Chung, M. K., Avants, B. B., Shirtcliff, E. A., Gee, J. C., Davidson, R. J., et al. (2010). Early stress is associated with alterations in the orbitofrontal cortex: A tensor-based morphometry investigation of brain structure and behavioral risk. Journal of Neuroscience, 30, 7466–7472.Google Scholar
Hariri, A. R., Bookheimer, S. Y., & Mazziotta, J. C. (2000). Modulating emotional responses: Effects of a neocortical network on the limbic system. NeuroReport, 11, 43–48.CrossRefGoogle ScholarPubMed
Hart, H., & Rubia, K. (2012). Neuroimaging of child abuse: A critical review. Frontiers in Human Neuroscience, 6, 52.CrossRefGoogle ScholarPubMed
Haxby, J. V., Horwitz, B., Ungerleider, L. G., Maisog, J. M., Pietrini, P., & Grady, C. L. (1994). The functional organization of human extrastriate cortex: A PET-rCBF study of selective attention to faces and locations. Journal of Neuroscience, 14, 6336–6353.Google Scholar
Hayes, J. P., Hayes, S. M., & Mikedis, A. M. (2012). Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biological Mood and Anxiety Disorders, 2, 9.CrossRefGoogle ScholarPubMed
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010). Neurobiological and psychiatric consequences of child abuse and neglect. Development and Psychobiology, 52, 671–690.Google Scholar
Herringa, R. J., Brin, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., et al. (2013). Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences, 110, 19119–19124.Google Scholar
Herringa, R. J., Phillips, M., Almeida, J., Insana, S. P., & Germain, A. (2012). Post-traumatic stress symptom severity correlates with smaller subgenual cingulate, caudate, and insula in combat veterans. Psychiatry Research: Neuroimaging, 203, 139–145.Google Scholar
Herringa, R. J., Phillips, M. L., Fournier, J. C., Kronhaus, D. M., & Germain, A. (2013). Childhood and adult trauma both correlate with dorsal anterior cingulate activation to threat in combat veterans. Psychological Medicine, 43, 1533–1542.Google Scholar
Hsieh, T. C., Lin, W. Y., Ding, H. J., Sun, S. S., Wu, Y. C., Yen, K. Y., et al. (2012). Sex- and age-related differences in brain FDG metabolism of healthy adults: An SPM analysis. Journal of Neuroimaging, 22, 21–27.Google Scholar
Hussey, J. M., Chang, J. J., & Kotch, J. B. (2006). Child maltreatment in the United States: Prevalence, risk factors, and adolescent health consequences. Pediatrics, 118, 933–942.Google Scholar
Insana, S., Kolko, D., & Germain, A. (2012). Early-life trauma is associated with rapid eye movement sleep fragmentation among military veterans. Biological Psychology, 89, 570–579.Google Scholar
Juster, R. P., Bizik, G., Picard, M., Arsenault-Lapierre, G., Sindi, S., Trepanier, L., et al. (2011). A transdisciplinary perspective of chronic stress in relation to psychopathology throughout life span development. Development and Psychopathology, 23, 725–776.Google Scholar
Keane, T. M., Fairbank, J. A., Caddell, J. M., Zimering, R. T., Taylor, K. L., & Mora, C. A. (1989). Clinical evaluation of a measure to assess combat exposure. Psychological Assessment, 1, 53–55.Google Scholar
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., et al. (2011). The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research, 223, 403–410.Google Scholar
Konarski, J. Z., McIntyre, R. S., Grupp, L. A., & Kennedy, S. H. (2005). Is the cerebellum relevant in the circuitry of neuropsychiatric disorders? Journal of Psychiatry and Neuroscience, 30, 178–186.Google Scholar
Krienen, F. M., & Buckner, R. L. (2009). Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cerebral Cortex, 19, 2485–2497.Google Scholar
Lanius, R. A., Williamson, P. C., Densmore, M., Boksman, K., Neufeld, R. W., Gati, J. S., et al. (2004). The nature of traumatic memories: A 4-T FMRI functional connectivity analysis. American Journal of Psychiatry, 161, 36–44.Google Scholar
Liao, C., Feng, Z., Zhou, D., Dai, Q., Xie, B., Ji, B., et al. (2012). Dysfunction of fronto-limbic brain circuitry in depression. Neuroscience, 201, 231–238.CrossRefGoogle ScholarPubMed
Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies. Neuroscience & Biobehavioral Reviews, 35, 1219–1236.CrossRefGoogle ScholarPubMed
Llinas, R. R., & Steriade, M. (2006). Bursting of thalamic neurons and states of vigilance. Journal of Neurophysiology, 95, 3297–3308.Google Scholar
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445.Google Scholar
Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19, 1233–1239.Google Scholar
Maren, S., Phan, K. L., & Liberzon, I. (2013). The contextual brain: Implications for fear conditioning, extinction and psychopathology. Nature Reviews Neuroscience, 14, 417–428.Google Scholar
Mayberg, H. S., Brannan, S. K., Mahurin, R. K., Jerabek, P. A., Brickman, J. S., Tekell, J. L., et al. (1997). Cingulate function in depression: A potential predictor of treatment response. NeuroReport, 8, 1057–1061.Google Scholar
Mayberg, H. S., Brannan, S. K., Tekell, J. L., Silva, J. A., Mahurin, R. K., McGinnis, S., et al. (2000). Regional metabolic effects of fluoxetine in major depression: Serial changes and relationship to clinical response. Biological Psychiatry, 48, 830–843.Google Scholar
McCrory, E., De Brito, S. A., & Viding, E. (2011). The impact of childhood maltreatment: A review of neurobiological and genetic factors. Front Psychiatry, 2, 48.Google Scholar
Mead, H. K., Beauchaine, T. P., & Shannon, K. E. (2010). Neurobiological adaptations to violence across development. Development and Psychopathology, 22, 1–22.Google Scholar
Milad, M. R., & Quirk, G. J. (2012). Fear extinction as a model for translational neuroscience: Ten years of progress. Annual Review of Psychology, 63, 129–151.CrossRefGoogle Scholar
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.Google Scholar
Nofzinger, E. A., Mintun, M. A., Price, J., Meltzer, C. C., Townsend, D., Buysse, D. J., et al. (1998). A method for the assessment of the functional neuroanatomy of human sleep using FDG PET. Brain Research Protocols, 2, 191–198.Google Scholar
Nofzinger, E. A., Mintun, M. A., Wiseman, M., Kupfer, D. J., & Moore, R. Y. (1997). Forebrain activation in REM sleep: An FDG PET study. Brain Research, 770, 192–201.CrossRefGoogle ScholarPubMed
Norman, R. E., Byambaa, M., De, R., Butchart, A., Scott, J., & Vos, T. (2012). The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLOS Medicine, 9, e1001349.Google Scholar
Norris, C. J., Chen, E. E., Zhu, D. C., Small, S. L., & Cacioppo, J. T. (2004). The interaction of social and emotional processes in the brain. Journal of Cognitive Neuroscience, 16, 1818–1829.Google Scholar
Ochsner, K. N., & Gross, J. J. (2005). The cognitive control of emotion. Trends in Cognitive Science, 9, 242–249.CrossRefGoogle ScholarPubMed
Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D., et al. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23, 483–499.Google Scholar
Ongur, D., & Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex, 10, 206–219.Google Scholar
Parr, L. A., Boudreau, M., Hecht, E., Winslow, J. T., Nemeroff, C. B., & Sanchez, M. M. (2012). Early life stress affects cerebral glucose metabolism in adult rhesus monkeys (Macaca mulatta). Development and Cognitive Neuroscience, 2, 181–193.Google Scholar
Phan, K. L., Britton, J. C., Taylor, S. F., Fig, L. M., & Liberzon, I. (2006). Corticolimbic blood flow during nontraumatic emotional processing in posttraumatic stress disorder. Archives of General Psychiatry, 63, 184–192.Google Scholar
Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331–348.CrossRefGoogle ScholarPubMed
Phillips, M. L., Ladouceur, C. D., & Drevets, W. C. (2008). A neural model of voluntary and automatic emotion regulation: Implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry, 13, 829, 833–829, 857.Google Scholar
Pohl, J., Olmstead, M. C., Wynne-Edwards, K. E., Harkness, K., & Menard, J. L. (2007). Repeated exposure to stress across the childhood-adolescent period alters rats’ anxiety- and depression-like behaviors in adulthood: The importance of stressor type and gender. Behavioral Neuroscience, 121, 462–474.Google Scholar
Pollak, S. D. (2005). Early adversity and mechanisms of plasticity: Integrating affective neuroscience with developmental approaches to psychopathology. Development and Psychopathology, 17, 735–752.Google Scholar
Posner, M. I., Rothbart, M. K., Sheese, B. E., & Tang, Y. (2007). The anterior cingulate gyrus and the mechanism of self-regulation. Cognitive and Affective Behavioral Neuroscience, 7, 391–395.Google Scholar
Price, J. L., & Drevets, W. C. (2012). Neural circuits underlying the pathophysiology of mood disorders. Trends in Cognitive Science, 16, 61–71.Google Scholar
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Pare, D. (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. Journal of Neuroscience, 23, 8800–8807.Google Scholar
Rigucci, S., Serafini, G., Pompili, M., Kotzalidis, G. D., & Tatarelli, R. (2010). Anatomical and functional correlates in major depressive disorder: The contribution of neuroimaging studies. World Journal of Biological Psychiatry, 11, 165–180.Google Scholar
Rinaman, L., Levitt, P., & Card, J. P. (2000). Progressive postnatal assembly of limbic-autonomic circuits revealed by central transneuronal transport of pseudorabies virus. Journal of Neuroscience, 20, 2731–2741.Google Scholar
Runyan, D. K., Cox, C. E., Dubowitz, H., Newton, R. R., Upadhyaya, M., Kotch, J. B., et al. (2005). Describing maltreatment: Do child protective service reports and research definitions agree? Child Abuse and Neglect, 29, 461–477.Google Scholar
Salkind, M. R. (1969). Beck Depression Inventory in general practice. Journal of the Royal College of General Practitioners, 18, 267–271.Google Scholar
Sanchez, 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
Schutter, D. J., & Van, H. J. (2005). The cerebellum on the rise in human emotion. Cerebellum, 4, 290–294.Google Scholar
Sotres-Bayon, F., Bush, D. E., & LeDoux, J. E. (2004). Emotional perseveration: An update on prefrontal–amygdala interactions in fear extinction. Learning and Memory, 11, 525–535.CrossRefGoogle ScholarPubMed
Steriade, M. (1997). Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cerebral Cortex, 7, 583–604.Google Scholar
Stoodley, C. J., & Schmahmann, J. D. (2009). Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. NeuroImage, 44, 489–501.Google Scholar
Stoodley, C. J., & Schmahmann, J. D. (2010). Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex, 46, 831–844.Google Scholar
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639.CrossRefGoogle ScholarPubMed
Taylor, S. E., Eisenberger, N. I., Saxbe, D., Lehman, B. J., & Lieberman, M. D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry, 60, 296–301.Google Scholar
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003). The neurobiological consequences of early stress and childhood maltreatment. Neuroscience & Biobehavioral Reviews, 27, 33–44.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., & Samson, J. A. (2013). Childhood maltreatment and psychopathology: A case for ecophenotypic variants as clinically and neurobiologically distinct sybtypes. American Journal of Psychiatry, 170, 1114–1133.Google Scholar
Teicher, M. H., Samson, J. A., Polcari, A., & McGreenery, C. E. (2006). Sticks, stones, and hurtful words: Relative effects of various forms of childhood maltreatment. American Journal of Psychiatry, 163, 993–1000.Google Scholar
Thompson, R. A., & Nelson, C. A. (2001). Developmental science and the media: Early brain development. American Psychologist, 56, 5–15.Google Scholar
Tiemeier, H., Lenroot, R. K., Greenstein, D. K., Tran, L., Pierson, R., & Giedd, J. N. (2010). Cerebellum development during childhood and adolescence: A longitudinal morphometric MRI study. NeuroImage, 49, 63–70.Google Scholar
Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011). Elevated amygdala response to faces following early deprivation. Developmental Science, 14, 190–204.Google Scholar
van der Werff, S. J., Pannekoek, J. N., Veer, I. M., van Tol, M. J., Aleman, A., Veltman, D. J., et al. (2013a). Resting-state functional connectivity in adults with childhood emotional maltreatment. Psychological Medicine, 43, 1825–1836.Google Scholar
van der Werff, S. J., Pannekoek, J. N., Veer, I. M., van Tol, M. J., Aleman, A., Veltman, D. J., et al. (2013b). Resilience to childhood maltreatment is associated with increased resting-state functional connectivity of the salience network with the lingual gyrus. Child Abuse & Neglect, 37, 1021–1029.Google Scholar
van Harmelen, A. L., Hauber, K., Gunther Moor, B., Spinhoven, P., Boon, A. E., Crone, E. A., et al. (2014). Child emotional maltreatment severity is associated with dorsal medial prefronal cortex responsivity to social exclusion in young adults. PLOS ONE, 9, e85107.Google Scholar
van Harmelen, A. L., van Tol, M. J., Dalgleish, T., van der Wee, N. J., Veltman, D. J., Aleman, A., et al. (in press). Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Social Cognitive and Affective Neuroscience.Google Scholar
van Harmelen, A. L., van Tol, M. J., van der Wee, N. J., 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
Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51, 32–58.Google Scholar
Villanueva, R. (2012). The cerebellum and neuropsychiatric disorders. Psychiatry Research, 198, 527–532.Google Scholar
Weathers, F. W., Ruscio, A. M., & Keane, T. M. (1999). Psychometric properties of nine scoring rules for the Clinician-Administered Posttraumatic Stress Disorder Scale. Psychological Assessment, 11, 124–133.Google Scholar
Whittle, S., Dennison, M., Vijayakumar, N., Simmons, J. G., Yücel, M., Lubman, DI., et al. (2013). Childhood maltreatment and psychopathology affect brain development during adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 940–952.Google Scholar
Wilkin, M. M., Waters, P., McCormick, C. M., & Menard, J. L. (2012). Intermittent physical stress during early- and mid-adolescence differentially alters rats’ anxiety- and depression-like behaviors in adulthood. Behavioral Neuroscience, 126, 344–360.Google Scholar
Winegar, R. K., & Lipschitz, D. S. (1999). Agreement between hospitalized adolescents’ self-reports of maltreatment and witnessed home violence and clinician reports and medical records. Comprehensive Psychiatry, 40, 347–352.Google Scholar
Woods, R. P., Cherry, S. R., & Mazziotta, J. C. (1992). Rapid automated algorithm for aligning and reslicing PET images. Journal of Computer Assisted Tomography, 16, 620–633.Google Scholar
Yucel, M., Wood, S. J., Fornito, A., Riffkin, J., Velakoulis, D., & Pantelis, C. (2003). Anterior cingulate dysfunction: Implications for psychiatric disorders? Journal of Psychiatry and Neuroscience, 28, 350–354.Google ScholarPubMed
Zielinski, D. S. (2009). Child maltreatment and adult socioeconomic well-being. Child Abuse and Neglect, 33, 666–678.CrossRefGoogle ScholarPubMed
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