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Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates

Published online by Cambridge University Press:  11 January 2021

Elyse L. Morin ,
Brittany R. Howell ,
Eric Feczko ,
Eric Earl ,
Melanie Pincus ,
Katherine Reding ,
Zsofia A. Kovacs-Balint ,
Jerrold S. Meyer ,
Martin Styner  and
Damien Fair
...Show all authors
Elyse L. Morin
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Brittany R. Howell
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA Fralin Biomedical Research Institute at VTC, Roanoke, VA, USA Department of Human Development and Family Science, Virginia Tech, Blacksburg, VA, USA
Eric Feczko
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Eric Earl
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Melanie Pincus
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Katherine Reding
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA
Zsofia A. Kovacs-Balint
Affiliation:
Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
Jerrold S. Meyer
Affiliation:
Department of Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, USA
Martin Styner
Affiliation:
Departments of Psychiatry and Computer Science, University of North Carolina, Chapel Hill, NC, USA
Damien Fair
Affiliation:
Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR, USA
Mar M. Sanchez*
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA Department of Psychiatry & Behavioral Sciences, Emory University, Atlanta, GA, USA
*
Author for Correspondence: Dr. Mar Sanchez, Department of Psychiatry and Behavioral Sciences, and Yerkes National Primate Research Center, Emory University, 954 Gatewood Drive NE, NS 4216, Atlanta, GA30329; E-mail: mmsanch@emory.edu.
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Abstract

Despite the strong link between childhood maltreatment and psychopathology, the underlying neurodevelopmental mechanisms are poorly understood and difficult to disentangle from heritable and prenatal factors. This study used a translational macaque model of infant maltreatment in which the adverse experience occurs in the first months of life, during intense maturation of amygdala circuits important for stress and emotional regulation. Thus, we examined the developmental impact of maltreatment on amygdala functional connectivity (FC) longitudinally, from infancy through the juvenile period. Using resting state functional magnetic resonance imaging (MRI) we performed amygdala–prefrontal cortex (PFC) region-of-interest and exploratory whole-brain amygdala FC analyses. The latter showed (a) developmental increases in amygdala FC with many regions, likely supporting increased processing of socioemotional-relevant stimuli with age; and (b) maltreatment effects on amygdala coupling with arousal and stress brain regions (locus coeruleus, laterodorsal tegmental area) that emerged with age. Maltreated juveniles showed weaker FC than controls, which was negatively associated with infant hair cortisol concentrations. Findings from the region-of-interest analysis also showed weaker amygdala FC with PFC regions in maltreated animals than controls since infancy, whereas bilateral amygdala FC was stronger in maltreated animals. These effects on amygdala FC development may underlie the poor behavioral outcomes associated with this adverse experience.

Keywords

amygdala functional connectivitychildhood maltreatmentearly life stressprefrontal cortexrhesus monkey
Type
Special Section 1: 2019 Minnesota Symposium on Child Psychology
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1579 - 1596
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abercrombie, E. D., & Jacobs, B. L. (1987). Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. Journal of Neuroscience, 7, 2837–2843.CrossRefGoogle ScholarPubMed
Amano, T., Duvarci, S., Popa, D., & Pare, D. (2011). The fear circuit revisited: Contributions of the basal amygdala nuceli to conditioned fear. Journal of Neuroscience, 31, 15481–15489.CrossRefGoogle Scholar
Amaral, D. G., & Price, J. L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). Journal of Comparative Neurology, 230, 465–496. doi:10.1002/cne.902300402CrossRefGoogle 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
Asan, E. (1998). The catecholaminergic innervation of the rat amygdala. Advances in Anatomy, Embryology and Cell Biology, 142, 1–118.CrossRefGoogle ScholarPubMed
Asok, A., Bernard, K., Roth, T., Rosen, J., & Dozier, M. (2013). Parental responsiveness moderates the association between early-life stress and reduced telomere length. Development and Psychopathology, 25, 577–585. doi:10.1017/s0954579413000011CrossRefGoogle ScholarPubMed
Aston-Jones, G., Chiang, C., & Alexinsky, T. (1991). Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Progress in Brain Research, 88, 501–520.CrossRefGoogle ScholarPubMed
Barbas, H., Saha, S., Rempel-Clower, N., & Ghashghaei, T. (2003). Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neuroscience, 4, 25. Epub 2003/10/11. doi: 10.1186/1471-2202-4-25. PubMed PMID: 14536022. PMCID: PMCPMC270042.CrossRefGoogle ScholarPubMed
Borges, S., Coimbra, B., Soares-Cunha, C., Ventura-Silva, A. P., Pinto, L., Carvalho, M. M., … Sousa, N. (2013). Glucocorticoid programing of the mesopontine cholinergic system. Frontiers in Endocrinology (Lausanne), 4, 190. doi:10.3389/fendo.2013.00190Google ScholarPubMed
Bramlett, S., Morin, E. L., Guzman, D, Howell, B. R., Meyer, J. S., & Sanchez, M. M. (2017). Effects of adverse maternal care on the development of hypothalamic-pituitary-adrenal (HPA) axis function in nonhuman primates. Paper presented at the 47th Annual Meeting of the Society for Neuroscience (SfN), Washington, DC.Google Scholar
Bramlett, S., Wakeford, A., Morin, E., Guzman, D. G., Siebert, E., Howell, B., ... Sanchez, M. M. (2018). Early hypothalamic-pituitary-adrenal axis activity predicts anxiety and sensitivity to the reinforcing effects of cocaine in adolescent macaques: early life stress as a risk factor. Paper presented at the 48th Annual Meeting of the Society for Neuroscience (SfN), San Diego, CA.Google Scholar
Brent, L., Koban, T., & Ramirez, S. (2002). Abnormal, abusive, and stress-related behaviors in baboon mothers. Biolofical Psychiatry, 52, 1047–1056.Google ScholarPubMed
Britton, J. C., Grillon, C., Lissek, S., Norcross, M. A., Szuhany, K. L., Chen, G., … Pine, D. S. (2013). Response to learned threat: an fMRI study in adolescent and adult anxiety. American Journal of Psychiatry, 170, 1195–1204.CrossRefGoogle ScholarPubMed
Buffalari, D. M., & Grace, A. A. (2007). Noradrenergic modulation of basolateral amygdala neuronal activity: Opposing influences of alpha-2 and beta receptor activation. Journal of Neuroscience, 27, 12358–12366. doi:10.1523/jneurosci.2007-07.2007CrossRefGoogle ScholarPubMed
Burgess, G. C., Kandala, S., Nolan, D., Laumann, T. O., Power, J. D., Adeyemo, B., ... Barch, D. M. (2016). Evaluation of denoising strategies to address motion-correlated artifacts in resting-state functional magnetic resonance imaging data from the human connectome project. Brain Connect, 6(9), 669–680.CrossRefGoogle ScholarPubMed
Busso, D. S., Mclaughlin, K, & Sheridan, M. A. (2017). Dimensions of adversity, physiological reactivity, and externalizing psychopathology in adolescence: Deprivation and threat. Psychosomatic Medicine, 79(2), 162–171.CrossRefGoogle ScholarPubMed
Casey, B. J., Duhoux, S., & Malter Cohen, M. (2010). Adolescence: What do transmission, transition, and translation have to do with it? Neuron, 67, 749–760. doi:10.1016/j.neuron.2010.08.033CrossRefGoogle Scholar
Chen, Y., Dube, C. M., Rice, C. J., & Baram, T. Z. (2008). Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. Journal of Neuroscience, 28, 2903–2911. doi:10.1523/jneurosci.0225-08.2008CrossRefGoogle ScholarPubMed
Ciric, R., Wolf, D. H., Power, J. D., Roalf, D. R., Baum, G. L., Ruparel, K., … Satterthwaite, T. D. (2017). Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity. Neuroimage, 154, 174–187. doi:10.1016/j.neuroimage.2017.03.020CrossRefGoogle ScholarPubMed
Coe, C. L., & Shirtcliff, E. A. (2004). Growth trajectory evident at birth affects age of first delivery in female monkeys. Pediatric Research, 55, 914–920. doi:10.1203/01.Pdr.0000125259.45025.4dCrossRefGoogle ScholarPubMed
Costa Dias, T. G., Iyer, S. P., Carpenter, S. D., Cary, R. P., Wilson, V. B., Mitchell, S. H., Nigg, J. T., & Fair, D. A. (2015). Characterizing heterogeneity in children with and without ADHD based on reward system connectivity. Developmental Cognitive Neuroscience, 11, 155–174. doi:10.1016/j.dcn.2014.12.005CrossRefGoogle ScholarPubMed
D'Andrea, W., Pole, N., DePierro, J., Freed, S., & Wallace, D. B. (2013). Heterogeneity of defensive responses after exposure to trauma: Blunted autonomic reactivity in response to startling sounds. International Journal of Psychophysiology, 90(1), 80–89.CrossRefGoogle ScholarPubMed
Danese, A., & Tan, M. (2014). Childhood maltreatment and obesity: Systematic review and meta-analysis. Molecular Psychiatry, 19, 544–554. doi:10.1038/mp.2013.54CrossRefGoogle ScholarPubMed
Deoni, S. C., Dean, D. C. 3rd, O'Muircheartaigh, J., Dirks, H., & Jerskey, B. A. (2012). Investigating white matter development in infancy and early childhood using myelin water faction and relaxation time mapping. Neuroimage, 63, 1038–1053. doi:10.1016/j.neuroimage.2012.07.037CrossRefGoogle ScholarPubMed
Drury, S. S., Howell, B. R., Jones, C., Esteves, K., Morin, E., Schlesinger, R., … Sanchez, M. M. (2017). Shaping long-term primate development: Telomere length trajectory as an indicator of early maternal maltreatment and predictor of future physiologic regulation. Developmental Psychopathology, 29, 1539–1551. doi:10.1017/s0954579417001225CrossRefGoogle ScholarPubMed
Drury, S. S., Sanchez, M. M., & Gonzalez, A. (2016). When mothering goes awry: Challenges and opportunities for utilizing evidence across rodent, nonhuman primate and human studies to better define the biological consequences of negative early caregiving. Hormones and Behavior, 77, 182–192. doi:10.1016/j.yhbeh.2015.10.007CrossRefGoogle ScholarPubMed
Drury, S., Theall, K., Gleason, M., Smyke, A., De Vivo, I., Wong, J., ... Nelson, C. (2012). Telomere length and early severe social deprivation: Linking early adversity and cellular aging. Molecular Psychiatry, 17(7), 719–727.CrossRefGoogle ScholarPubMed
Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Huppi, P. S., & Hertz-Pannier, L. (2014). The early development of brain white matter: A review of imaging studies in fetuses, newborns and infants. Neuroscience, 276, 48–71. doi:10.1016/j.neuroscience.2013.12.044CrossRefGoogle ScholarPubMed
Egan, T. M., & North, R. A. (1985). Acetylcholine acts on m2-muscarinic receptors to excite rat locus coeruleus neurones. British Journal of Pharmacology, 85, 733–735.CrossRefGoogle ScholarPubMed
Eluvathingal, T. J., Chugani, H. T., Behen, M. E., Juhasz, C., Muzik, O., Maqbool, M., … Makki, M. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 2093–2100. doi:10.1542/peds.2005-1727CrossRefGoogle ScholarPubMed
Engberg, G., & Svensson, T. H. (1980). Pharmacological analysis of a cholinergic receptor mediated regulation of brain norepinephrine neurons. Journal of Neural Transmission, 49, 137–150.CrossRefGoogle ScholarPubMed
Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U., Church, J. A., Miezin, F. M., … Petersen, S. E. (2009). Functional brain networks develop from a “local to distributed” organization. PLoS Computational Biology, 5, e1000381. doi:10.1371/journal.pcbi.1000381CrossRefGoogle Scholar
Fair, D. A., Dosenbach, N. U., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., … Schlaggar, B. L. (2007). Development of distinct control networks through segregation and integration. Proceedings of the National Academy of Sciences USA, 104, 13507–13512. doi:10.1073/pnas.0705843104CrossRefGoogle ScholarPubMed
Fair, D. A., Nigg, J. T., Iyer, S., Bathula, D., Mills, K. L., Dosenbach, N. U., … Milham, M. P. (2012). Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Frontiers in Systems Neuroscience, 6, 80. doi:10.3389/fnsys.2012.00080Google ScholarPubMed
Fairbanks, LA. (1996). Individual differences in maternal styles: Causes and consequences for mothers and offspring. Advances in the Study of Behavior, 579–611.CrossRefGoogle Scholar
Fields, R. D. (2008). White matter in learning, cognition and psychiatric disorders. Trends in Neurosciences, 31, 361–370. doi:10.1016/j.tins.2008.04.001CrossRefGoogle ScholarPubMed
Finkelhor, D., Turner, H. A., Shattuck, A., & Hamby, S. L. (2013). Violence, crime, and abuse exposure in a national sample of children and youth: An update. JAMA Pediatrics, 167, 614–621. doi:10.1001/jamapediatrics.2013.42CrossRefGoogle Scholar
Finlay, J. M., Jedema, H. P., Rabinovic, A. D., Mana, M. J., Zigmond, M. J., & Sved, A. F. (1997). Impact of corticotropin-releasing hormone on extracellular norepinephrine in prefrontal cortex after chronic cold stress. Journal of Neurochemistry, 69, 144–150.CrossRefGoogle ScholarPubMed
Foa, E. B., & Kozak, M. J. (1986). Emotional processing of fear: Exposure to corrective information. Psychological Bulletin, 99, 20–35.CrossRefGoogle ScholarPubMed
Fonzo, G. A., Simmons, A. N., Thorp, S. R., Norman, S. B., Paulus, M. P., & Stein, M. B. (2010a). Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biological Psychiatry, 68, 433–441. doi:10.1016/j.biopsych.2010.04.028CrossRefGoogle Scholar
Fonzo, G. A., Simmons, A. N., Thorp, S. R., Norman, S. B., Paulus, M. P., & Stein, M. B. (2010b). Exaggerated and disconnected insular-amygdalar BOLD response to threat-related emotional faces in women with intimate-partner violence PTSD. Biological Psychiatry, 68, 433–441.CrossRefGoogle Scholar
Foster, D. J., & Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature, 440, 680–683. doi:10.1038/nature04587CrossRefGoogle ScholarPubMed
Franklin, T. B., Russig, H., Weiss, I. C., Graff, J., Linder, N., Michalon, A., … Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408–415. doi:10.1016/j.biopsych.2010.05.036CrossRefGoogle Scholar
Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., … Tottenham, N. (2014). The development of human amygdala functional connectivity at rest from 4 to 23 years: A cross-sectional study. Neuroimage, 95, 193–207. doi:10.1016/j.neuroimage.2014.03.038CrossRefGoogle ScholarPubMed
Gallagher, M., Kapp, B. S., Musty, R. E., & Driscoll, P. A. (1977). Memory formation: Evidence for a specific neurochemical system in the amygdala. Science, 198, 423–425.CrossRefGoogle ScholarPubMed
Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., … Tottenham, N. (2013). Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proceedings of the National Academy of Sciences USA, 110, 15638–15643. doi:10.1073/pnas.1307893110CrossRefGoogle ScholarPubMed
Gee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., … Tottenham, N. (2014). Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychological Science, 25, 2067–2078. doi:10.1177/0956797614550878CrossRefGoogle Scholar
Geng, X., Gouttard, S., Sharma, A., Gu, H., Styner, M., Lin, W., … Gilmore, J. H. (2012). Quantitative tract-based white matter development from birth to age 2years. Neuroimage, 61, 542–557. doi:10.1016/j.neuroimage.2012.03.057CrossRefGoogle ScholarPubMed
Goldstein, L. E., Rasmusson, A. M., Bunney, B. S., & Roth, R. H. (1996). Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. Journal of Neuroscience, 16, 4787–4798.CrossRefGoogle ScholarPubMed
Gorgolewski, K., Burns, C. D., Madison, C., Clark, D., Halchenko, Y. O., Waskom, M. L., & Ghosh, S. S. (2011). Nipype: A flexible, lightweight and extensible neuroimaging data processing framework in python. Frontiers in Neuroinformatics, 5, 13. doi:10.3389/fninf.2011.00013CrossRefGoogle ScholarPubMed
Govindan, R. M., Behen, M. E., Helder, E., Makki, M. I., & Chugani, H. T. (2010). Altered water diffusivity in cortical association tracts in children with early deprivation identified with Tract-Based Spatial Statistics (TBSS). Cerebral Cortex, 20, 561–569. doi:10.1093/cercor/bhp122CrossRefGoogle Scholar
Grant, S. J., Aston-Jones, G., & Redmond, D. E. Jr. (1988). Responses of primate locus coeruleus neurons to simple and complex sensory stimuli. Brain Research Bulletin, 21, 401–410.CrossRefGoogle ScholarPubMed
Grayson, D. S., Bliss-Moreau, E., Machado, C. J., Bennett, J., Shen, K., Grant, K. A., … Amaral, D. G. (2016). The rhesus monkey connectome predicts disrupted functional networks resulting from pharmacogenetic inactivation of the amygdala. Neuron, 91, 453–466. doi:10.1016/j.neuron.2016.06.005CrossRefGoogle ScholarPubMed
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015). Parental buffering of fear and stress neurobiology: Reviewing parallels across rodent, monkey, and human models. Social Neuroscience, 10, 474–478. doi:10.1080/17470919.2015.1070198CrossRefGoogle ScholarPubMed
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Reviews of Psychology, 58, 145–173. doi:10.1146/annurev.psych.58.110405.085605CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Sullivan, R. M. (2017). The neurodevelopment of social buffering and fear learning: Integration and crosstalk. Social Neuroscience, 12, 1–7. doi:10.1080/17470919.2016.1151824CrossRefGoogle ScholarPubMed
Hare, T. A., Tottenham, N., Galvan, A., Voss, H. U., Glover, G. H., & Casey, B. J. (2008). Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biological Psychiatry, 63, 927–934. doi:10.1016/j.biopsych.2008.03.015CrossRefGoogle ScholarPubMed
Heleniak, C., Mclaughlin, K. A., Ormel, J, & Riese, H. (2016). Cardiovascular reactivity as a mechanism linking child trauma to adolescent psychopathology. Biological Psychology, 120, 108–119.CrossRefGoogle ScholarPubMed
Henckens, M. J., van Wingen, G. A., Joels, M., & Fernandez, G. (2012). Corticosteroid induced decoupling of the amygdala in men. Cerebral Cortex, 22, 2336–2345. doi:10.1093/cercor/bhr313CrossRefGoogle ScholarPubMed
Hinde, R. A., & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behavior, 15, 169–196.CrossRefGoogle ScholarPubMed
Howell, B. R., Ahn, M., Shi, Y., Godfrey, J. R., Hu, X., Zhu, H., … Sanchez, M. M. (2019). Disentangling the effects of early caregiving experience and heritable factors on brain white matter development in rhesus monkeys. Neuroimage, 197, 625–642. doi:10.1016/j.neuroimage.2019.04.013.CrossRefGoogle ScholarPubMed
Howell, B. R., Grand, A. P., McCormack, K. M., Shi, Y., LaPrarie, J. L., Maestripieri, D., … Sanchez, M. M. (2014). Early adverse experience increases emotional reactivity in juvenile rhesus macaques: Relation to amygdala volume. Developmental Psychobiology, 56, 1735–1746. doi:10.1002/dev.21237CrossRefGoogle ScholarPubMed
Howell, B. R., McCormack, K. M., Grand, A. P., Sawyer, N. T., Zhang, X., Maestripieri, D., … Sanchez, M. M. (2013). Brain white matter microstructure alterations in adolescent rhesus monkeys exposed to early life stress: Associations with high cortisol during infancy. Biology of Mood and Anxiety Disorders, 3, 21. doi:10.1186/2045-5380-3-21CrossRefGoogle ScholarPubMed
Howell, B. R., McMurray, M. S., Guzman, D. B., Nair, G., Shi, Y., McCormack, K. M., … Sanchez, M. M. (2017). Maternal buffering beyond glucocorticoids: Impact of early life stress on corticolimbic circuits that control infant responses to novelty. Social Neuroscience, 12, 50–64. doi:10.1080/17470919.2016.1200481CrossRefGoogle ScholarPubMed
Howell, B. R., Neigh, G. N., & Sánchez, M. M. (2016). Animal models of developmental psychopathology. In D., Cicchetti (Ed.), Developmental Psychopathology (pp. 166–201). John Wiley & Sons.Google Scholar
Howell, B. R., & Sanchez, M. M. (2011). Understanding behavioral effects of early life stress using the reactive scope and allostatic load models. Developmental Psychopathology, 23, 1001–1016. doi:10.1017/s0954579411000460CrossRefGoogle ScholarPubMed
Huizinga, D., Haberstick, B. C., Smolen, A., Menard, S., Young, S. E., Corley, R. P., … Hewitt, J. K. (2006). Childhood maltreatment, subsequent antisocial behavior, and the role of monoamine oxidase A genotype. Biological Psychiatry, 60, 677–683. doi:10.1016/j.biopsych.2005.12.022CrossRefGoogle ScholarPubMed
Hutchison, R. M., Hutchison, M., Manning, K. Y., Menon, R. S., & Everling, S. (2014). Isoflurane induces dose-dependent alterations in the cortical connectivity profiles and dynamic properties of the brain's functional architecture. Human Brain Mapping, 35, 5754–5775. doi:10.1002/hbm.22583CrossRefGoogle ScholarPubMed
Hutchison, R., Womelsdorf, T., Gati, J., Everling, S., & Menon, R. S. (2013). Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Human Brain Mapping, 34(9), 2154–2177.CrossRefGoogle ScholarPubMed
Hutchison, R. M., Womelsdorf, T., Gati, J. S., Leung, L. S., Menon, R. S., & Everling, S. (2012). Resting-state connectivity identifies distinct functional networks in macaque cingulate cortex. Cerebral Cortex, 22, 1294–1308. doi:10.1093/cercor/bhr181CrossRefGoogle ScholarPubMed
Iyer, S. P., Shafran, I., Grayson, D., Gates, K., Nigg, J. T., & Fair, D. A. (2013). Inferring functional connectivity in MRI using Bayesian network structure learning with a modified PC algorithm. Neuroimage, 75, 165–175. doi:10.1016/j.neuroimage.2013.02.054CrossRefGoogle ScholarPubMed
Jauregui-Huerta, F., Ruvalcaba-Delgadillo, Y., Gonzalez-Castaneda, R., Garcia-Estrada, J., Gonzalez-Perez, O., & Luquin, S. (2010). Responses of glial cells to stress and glucocorticoids. Current Immunology Reviews, 6(3), 195–204.CrossRefGoogle ScholarPubMed
Johnson, E. O., Kamilaris, T. C., Calogero, A. E., Gold, P. W., & Chrousos, G. P. (1996). Effects of early parenting on growth and development in a small primate. Pediatric Research, 39, 999–1005. doi:10.1203/00006450-199606000-00012CrossRefGoogle Scholar
Jones, B. E., & Yang, T. Z. (1985). The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. Journal of Comparative Neurology, 242, 56–92. doi:10.1002/cne.902420105CrossRefGoogle ScholarPubMed
Kaplow, J. B., & Widom, C. S. (2007). Age of onset of child maltreatment predicts long-term mental health outcomes. Journal of Abnormal Psychology, 116, 176–187. doi:10.1037/0021-843x.116.1.176CrossRefGoogle ScholarPubMed
Kaufer, D., Friedman, A., Seidman, S., & Soreq, H. (1998). Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature, 393, 373–377. doi:10.1038/30741CrossRefGoogle ScholarPubMed
Kelly, A. M., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2008). Competition between functional brain networks mediates behavioral variability. Neuroimage, 39, 527–537. doi:10.1016/j.neuroimage.2007.08.008CrossRefGoogle ScholarPubMed
Kisiel, C. L., Fehrenbach, T., Torgersen, E., Stolbach, B., McClelland, G., Griffin, G., & Burkman, K. (2014). Constellations of interpersonal trauma and symptoms in child welfare: Implications for a developmental trauma framework. Journal of Family Violence, 29, 1–14.CrossRefGoogle Scholar
Koch, H., McCormack, K., Sanchez, M. M., & Maestripieri, D. (2014). The development of the hypothalamic-pituitary-adrenal axis in rhesus monkeys: Effects of age, sex, and early experience. Developmental Psychobiology, 56, 86–95. doi:10.1002/dev.21093CrossRefGoogle ScholarPubMed
Kovacs-Balint, Z., Feczko, E., Pincus, M., Earl, E., Miranda-Dominguez, O., Howell, B., … Sanchez, M. (2018). Early developmental trajectories of functional connectivity along the visual pathways in rhesus monkeys. Cerebral Cortex, 29(8), 3514–3526.CrossRefGoogle Scholar
Kumar, A., Behen, M. E., Singsoonsud, P., Veenstra, A. L., Wolfe-Christensen, C., Helder, E., & Chugani, H. T. (2014). Microstructural abnormalities in language and limbic pathways in orphanage-reared children: A diffusion tensor imaging study. Journal of Child Neurology, 29, 318–325. doi:10.1177/0883073812474098CrossRefGoogle ScholarPubMed
Kumar, S., Cole, R., Chiappelli, F., & de Vellis, J. (1989). Differential regulation of oligodendrocyte markers by glucocorticoids: Post-transcriptional regulation of both proteolipid protein and myelin basic protein and transcriptional regulation of glycerol phosphate dehydrogenase. Proceedings of the National Academy of Sciences USA, 86, 6807–6811.CrossRefGoogle ScholarPubMed
Kuwahata, H., Adachi, I., Fujita, K., Tomonaga, M., & Matsuzawa, T. (2004). Development of schematic face preference in macaque monkeys. Behavioral Processes, 66, 17–21. doi:10.1016/j.beproc.2003.11.002CrossRefGoogle ScholarPubMed
LeDoux, J. (2007). The amygdala. Current Biology, 17, R868–R874. doi:10.1016/j.cub.2007.08.005CrossRefGoogle ScholarPubMed
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Reviews Neuroscience, 23, 155–184. doi:10.1146/annurev.neuro.23.1.155CrossRefGoogle Scholar
Lewis, J. W., & Van Essen, D. C. (2000). Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. Journal of Comparative Neurology, 428, 79–111.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Li, C. X., Patel, S., Auerbach, E. J., & Zhang, X. (2013). Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys. Neuroscience Letters, 541, 58–62. doi:10.1016/j.neulet.2013.02.007CrossRefGoogle ScholarPubMed
Liang, Z., King, J., & Zhang, N. (2012). Anticorrelated resting-state functional connectivity in awake rat brain. Neuroimage, 59, 1190–1199. doi:10.1016/j.neuroimage.2011.08.009CrossRefGoogle ScholarPubMed
Liston, C., Cichon, J. M., Jeanneteau, F., Jia, Z., Chao, M. V., & Gan, W. B. (2013). Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nature Neuroscience, 16, 698–705. doi:10.1038/nn.3387CrossRefGoogle ScholarPubMed
Liston, C., & Gan, W. B. (2011). Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proceedings of the National Academy of Sciences USA, 108, 16074–16079. doi:10.1073/pnas.1110444108CrossRefGoogle ScholarPubMed
Logothetis, N. K., & Saleem, K. S. (2012). A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.Google Scholar
Lovallo, W. R., Farag, N. H., Sorocco, K. H., Cohoon, A. J., & Vincent, A. S. (2012). Lifetime adversity leads to blunted stress axis reactivity: Studies from the Oklahoma Family Health Patterns Project. Biological Psychiatry, 71(4), 344–349.CrossRefGoogle ScholarPubMed
Lutz, C. K., Lockard, J. S., Gunderson, V. M., & Grant, K. S. (1998). Infant monkeys’ visual responses to drawings of normal and distorted faces. American Journal of Primatology, 44, 169–174. doi:10.1002/(sici)1098-2345(1998)44:2 < 169::aid-ajp7 > 3.0.co;2-u3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Machlin, L., Miller, A. B., Snyder, J, Mclaughlin, K. A., & Sheridan, M. A. (2019). Differential associations of deprivation and threat with cognitive control and fear conditioning in early childhood. Frontiers in Behavioral Neuroscience, 13, 80. doi:10.3389/fnbeh.2019.00080CrossRefGoogle ScholarPubMed
Macmillan, H. L., Georgiades, K., Duku, E. K., Shea, A., Steiner, M., Niec, A., ... Schmidt, L. A. (2009). Cortisol response to stress in female youths exposed to childhood maltreatment: Results of the youth mood project. Biological Psychiatry, 66(1), 62–68.CrossRefGoogle ScholarPubMed
Maestripieri, D. (1998). Parenting styles of abusive mothers in group-living rhesus macaques. Animal Behavior, 55, 1–11.CrossRefGoogle ScholarPubMed
Maestripieri, D. (1999). The biology of human parenting: Insights from nonhuman primates. Neuroscience & Biobehavioral Reviews, 23, 411–422.CrossRefGoogle ScholarPubMed
Maestripieri, D. (2005). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences USA, 102, 9726–9729. doi:10.1073/pnas.0504122102CrossRefGoogle ScholarPubMed
Maestripieri, D., & Carroll, K. A. (1998). Risk factors for infant abuse and neglect in group-living rhesus monkeys. Psychological Science, 9, 143–145.CrossRefGoogle Scholar
Margulies, D. S., Vincent, J. L., Kelly, C., Lohmann, G., Uddin, L. Q., Biswal, B. B., … Petrides, M. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proceedings of the National Academy of Sciences USA, 106, 20069–20074. doi:10.1073/pnas.0905314106CrossRefGoogle ScholarPubMed
Markov, N. T., Misery, P., Falchier, A., Lamy, C., Vezoli, J., Quilodran, R., … Knoblauch, K. (2011). Weight consistency specifies regularities of macaque cortical networks. Cerebral Cortex, 21, 1254–1272. doi:10.1093/cercor/bhq201CrossRefGoogle ScholarPubMed
Matthews, M., & Fair, D. A. (2015). Research review: Functional brain connectivity and child psychopathology–overview and methodological considerations for investigators new to the field. Journal of Child Psychology and Psychiatry, 56, 400–414. doi:10.1111/jcpp.12335CrossRefGoogle ScholarPubMed
Mavigner, M., Raper, J., Kovacs-Balint, Z., Gumber, S., O'Neal, J. T., Bhaumik, S. K., … Chahroudi, A. (2018). Postnatal Zika virus infection is associated with persistent abnormalities in brain structure, function, and behavior in infant macaques. Science Translational Medicine, 10(435), eaao6975. doi:10.1126/scitranslmed.aao6975.CrossRefGoogle ScholarPubMed
McCormack, K., Howell, B. R., Guzman, D., Villongco, C., Pears, K., Kim, H., … Sanchez, M. M. (2015). The development of an instrument to measure global dimensions of maternal care in rhesus macaques (Macaca mulatta). American Journal of Primatology, 77, 20–33. doi:10.1002/ajp.22307CrossRefGoogle Scholar
McCormack, K., Newman, T. K., Higley, J. D., Maestripieri, D., & Sanchez, M. M. (2009). Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Hormones and Behavior, 55, 538–547. doi:10.1016/j.yhbeh.2009.01.009CrossRefGoogle ScholarPubMed
McCormack, K., Sanchez, M. M., Bardi, M., & Maestripieri, D. (2006). Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Developmental Psychobiology, 48, 537–550. doi:10.1002/dev.20157CrossRefGoogle ScholarPubMed
McEwen, B. S. (2004). Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Annals of the New York Academy of Sciences, 1032, 1–7. doi:10.1196/annals.1314.001CrossRefGoogle Scholar
McGaugh, J. L. (2002). Memory consolidation and the amygdala: A systems perspective. Trends in Neuroscience, 25, 456.CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Sheridan, M. A., Gold, A. L., Duys, A., Lambert, H. K., Peverill, M., … Pine, D. S. (2016). Maltreatment exposure, brain structure, and fear conditioning in children and adolescents. Neuropsychopharmacology, 41, 1956–1964. doi:10.1038/npp.2015.365CrossRefGoogle ScholarPubMed
Mclaughlin, K., Sheridan, M., Tibu, F., Fox, N., Zeanah, C., & Nelson, C. (2015). Causal effects of the early caregiving environment on development of stress response systems in children. Proceedings of the National Academy of Sciences, 112, 5637–5642. doi:10.1073/pnas.1423363112CrossRefGoogle ScholarPubMed
Mcteague, L. M., & Lang, P. J. (2012). The anxiety spectrum and the reflex physiology of defense: From circumscribed fear to broad distress. Depression & Anxiety, 29(4), 264–281. doi:10.1002/da.21891CrossRefGoogle ScholarPubMed
Meyer, J., Novak, M., Hamel, A., & Rosenberg, K. (2014). Extraction and analysis of cortisol from human and monkey hair. Journal of Visualized Experiments, 83, e50882. doi:10.3791/50882Google Scholar
Miranda-Dominguez, O., Mills, B. D., Carpenter, S. D., Grant, K. A., Kroenke, C. D., Nigg, J. T., & Fair, D. A. (2014a). Connectotyping: Model based fingerprinting of the functional connectome. PLoS One, 9, e111048. doi:10.1371/journal.pone.0111048CrossRefGoogle Scholar
Miranda-Dominguez, O., Mills, B. D., Grayson, D., Woodall, A., Grant, K. A., Kroenke, C. D., & Fair, D. A. (2014b). Bridging the gap between the human and macaque connectome: A quantitative comparison of global interspecies structure-function relationships and network topology. Journal of Neuroscience, 34, 5552–5563. doi:10.1523/jneurosci.4229-13.2014CrossRefGoogle Scholar
Moriceau, S., & Sullivan, R. M. (2006). Maternal presence serves as a switch between learning fear and attraction in infancy. Nature Neuroscience, 9, 1004–1006. doi:10.1038/nn1733CrossRefGoogle ScholarPubMed
Morin, E. L., Howell, B. R., Meyer, J. S., & Sanchez, M. M. (2019). Effects of early maternal care on adolescent attention bias to threat in nonhuman primates. Developmental Cognitive Neuroscience, 38, 100643. https://doi.org/10.1016/j.dcn.2019.100643.CrossRefGoogle ScholarPubMed
Morin, E. L., Howell, B. R., Reding, K., Guzman, D. B., Feczko, E., Earl, E., … Shi, Y. (2015). Early Maternal Care Modulates the Development of Emotional Neurocircuitry in Nonhuman Primates: Amygdala Functional Connectivity. 45th Annual Meeting of the Society for Neuroscience (SfN).Google Scholar
Morin, E. L., Wakeford, A. G. P., Howell, B. R., Guzman, D. B., Siebert, E., Kazama, A. M., ... Sanchez, M. (2018). Maternal care controls the development of fear learning in adolescent nonhuman primates: relationship with prefrontal 5ht1a receptor binding. Paper presented at the 48th Annual Meeting of the Society for Neuroscience (SfN), San Diego, CA.Google Scholar
Morris, J. S., Ohman, A., & Dolan, R. J. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467–470. doi:10.1038/30976CrossRefGoogle ScholarPubMed
Murphy, K, & Fox, M. (2017). Towards a consensus regarding global signal regression for resting state functional connectivity MRI. Neuroimage, 154, 169–173.CrossRefGoogle ScholarPubMed
Muschinski, J., Feczko, E., Brooks, J. M., Collantes, M., Heitz, T. R., & Parr, L. A. (2016). The development of visual preferences for direct versus averted gaze faces in infant macaques (Macaca mulatta). Developmental Psychobiology, 58, 926–936. doi:10.1002/dev.21421CrossRefGoogle Scholar
Nalci, A., Rao, B. D., & Liu, T. T. (2017). Global signal regression acts as a temporal downweighting process in resting-state fMRI. Neuroimage, 152, 602–618. doi:10.1016/j.neuroimage.2017.01.015CrossRefGoogle ScholarPubMed
Ouellet-Morin, I, Odgers, C. L., Danese, A., Bowes, L., Shakoor, S., Papadopoulos, A, ... Arseneault, L. (2011). Blunted cortisol responses to stress signal social and behavioral problems among maltreated/bullied 12-year-old children. Biological Psychiatry, 70(11), 1015–1023.CrossRefGoogle ScholarPubMed
Palanca, B. J., Mitra, A., Larson-Prior, L., Snyder, A. Z., Avidan, M. S., & Raichle, M. E. (2015). Resting-state functional magnetic resonance imaging correlates of sevoflurane-induced unconsciousness. Anesthesiology, 123, 346–356. doi:10.1097/aln.0000000000000731CrossRefGoogle ScholarPubMed
Parr, L. A., Murphy, L., Feczko, E., Brooks, J., Collantes, M., & Heitz, T. R. (2016). Experience-dependent changes in the development of face preferences in infant rhesus monkeys. Developmental Psychobiology, 58, 1002–1018. doi:10.1002/dev.21434CrossRefGoogle ScholarPubMed
Paxinos, G, Huang, X.-F., & Toga, A. W. (2000). The Rhesus Monkey Brain in Sterotaxic Coordinates. San Diego, CA: Academic Press.Google Scholar
Petrullo, L. A., Mandalaywala, T. M., Parker, K. J., Maestripieri, D., & Higham, J. P. (2016). Effects of early life adversity on cortisol/salivary alpha-amylase symmetry in free-ranging juvenile rhesus macaques. Hormones and Behavior, 86, 78–84. doi:10.1016/j.yhbeh.2016.05.004CrossRefGoogle ScholarPubMed
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59, 2142–2154. doi:10.1016/j.neuroimage.2011.10.018CrossRefGoogle ScholarPubMed
Power, J. D., Laumann, T. O., Plitt, M., Martin, A., & Petersen, S. E. (2017). On global fMRI signals and simulations. Trends in Cognitive Sciences, 21, 911–913. doi:10.1016/j.tics.2017.09.002CrossRefGoogle ScholarPubMed
Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage, 84, 320–341. doi:10.1016/j.neuroimage.2013.08.048CrossRefGoogle ScholarPubMed
Qin, S., Young, C. B., Supekar, K., Uddin, L. Q., & Menon, V. (2012). Immature integration and segregation of emotion-related brain circuitry in young children. Proceedings of the National Academy of Sciences USA, 109, 7941–7946. doi:10.1073/pnas.1120408109CrossRefGoogle ScholarPubMed
Rasmussen, K., Morilak, D. A., & Jacobs, B. L. (1986). Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli. Brain Research, 371, 324–334.CrossRefGoogle ScholarPubMed
Reding, K. M., Grayson, D. S., Miranda-Dominguez, O., Ray, S., Wilson, M. E., Toufexis, D., ... Sanchez, M. M. (2019). Effects of social subordination and estradiol on resting-state amygdala functional connectivity in adult female rhesus monkeys. Journal of Neuroendocrinology, e12822. doi:10.1111/jne.12822.Google Scholar
Reding, K. M., Grayson, D. S., Miranda-Dominguez, O., Ray, S., Wilson, M. E., Toufexis, D., … Sanchez, M. M. (2020). Effects of social subordination and oestradiol on resting-state amygdala functional connectivity in adult female rhesus monkeys. Journal of Neuroendocrinology, 32, e12822. doi:10.1111/jne.12822CrossRefGoogle ScholarPubMed
Rockstroh, B., & Elbert, T. (2010). Traces of fear in the neural web–magnetoencephalographic responding to arousing pictorial stimuli. International Journal of Psychophysiology, 78, 14–19. doi:10.1016/j.ijpsycho.2010.01.012CrossRefGoogle ScholarPubMed
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10, 423–433. doi:10.1038/nrn2651CrossRefGoogle ScholarPubMed
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Gotimer, K., … Milham, M. P. (2009). Functional connectivity of the human amygdala using resting state fMRI. Neuroimage, 45, 614–626. doi:10.1016/j.neuroimage.2008.11.030CrossRefGoogle ScholarPubMed
Russchen, F. T., Bakst, I., Amaral, D. G., & Price, J. L. (1985). The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Research, 329, 241–257.CrossRefGoogle ScholarPubMed
Rutter, M., Andersen-Wood, L., Beckett, C., Bredenkamp, D., Castle, J., Groothues, C., … O'Connor, T. G. (1999). Quasi-autistic patterns following severe early global privation. English and Romanian Adoptees (ERA) Study Team. Journal of Child Psychology and Psychiatry, 40, 537–549.CrossRefGoogle ScholarPubMed
Sallet, J., Mars, R. B., Noonan, M. P., Andersson, J. L., O'Reilly, J. X., Jbabdi, S., … Rushworth, M. F. (2011). Social network size affects neural circuits in macaques. Science, 334, 697–700. doi:10.1126/science.1210027CrossRefGoogle ScholarPubMed
Sanchez, M. M. (2006). The impact of early adverse care on HPA axis development: Nonhuman primate models. Hormones and Behavior, 50, 623–631. doi:10.1016/j.yhbeh.2006.06.012CrossRefGoogle ScholarPubMed
Sanchez, M. M., Alagbe, O., Felger, J. C., Zhang, J., Graff, A. E., Grand, A. P., … Miller, A. H. (2007). Activated p38 MAPK is associated with decreased CSF 5-HIAA and increased maternal rejection during infancy in rhesus monkeys. Molecular Psychiatry, 12, 895–897. doi:10.1038/sj.mp.4002025CrossRefGoogle ScholarPubMed
Sanchez, M. M., Hearn, E. F., Do, D., Rilling, J. K., & Herndon, J. G. (1998). Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Research, 812, 38–49.CrossRefGoogle ScholarPubMed
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. Developmental Psychopathology, 13, 419–449.CrossRefGoogle ScholarPubMed
Sanchez, M. M., McCormack, K., Grand, A. P., Fulks, R., Graff, A., & Maestripieri, D. (2010). Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys. Developmental Psychopathology, 22, 45–53. doi:10.1017/s0954579409990253CrossRefGoogle Scholar
Sanchez, M. M., McCormack, K. M., & Howell, B. R. (2015). Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits. Social Neuroscience, 10, 512–526. doi:10.1080/17470919.2015.1087426CrossRefGoogle ScholarPubMed
Sanchez, M. D., Milanes, M. V., Pazos, A., Diaz, A., & Laorden, M. L. (2000a). Autoradiographic evidence of delta-opioid receptor downregulation after prenatal stress in offspring rat brain. Pharmacology, 60, 13–18. doi:10.1159/000028341CrossRefGoogle Scholar
Sanchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000b). Distribution of corticosteroid receptors in the rhesus brain: Relative absence of glucocorticoid receptors in the hippocampal formation. Journal of Neuroscience, 20, 4657–4668.CrossRefGoogle Scholar
Schmahmann, J. D., Pandya, D. N. (2006). Fiber pathways of the brain. Oxford: Oxford University Press.CrossRefGoogle Scholar
Shi, Y., Budin, F., Yapuncich, E., Rumple, A., Young, J., Payne, C., ... Styner, M. A. (2017). UNC-Emory infant atlases for macaque brain image analysis: Postnatal brain development through 12 months. Frontiers in Neuroscience, 10, 617.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23, S208–219. doi:10.1016/j.neuroimage.2004.07.051CrossRefGoogle ScholarPubMed
Spinazzola, J., Hodgdon, H., Liang, L., Ford, J. D., Layne, C. M., Pynoos, R., … Kisiel, C. (2014). Unseen wounds: The contribution of psychological maltreatment to child and adolescent mental health and risk outcomes. Psychological Trauma: Theory, Research, Practice, and Policy, 6, S18–S28.CrossRefGoogle Scholar
Steinberg, A., Pynoos, R., Briggs, E. C., Gerrity, E. T., Layne, C. M., Vivrette, R. L., … Fairbank, J. A. (2014). The national child traumatic stress network core data set: Emerging findings, future directions, and implications for theory, research, practice, and policy. Psychological Trauma: Theory, Research, Practice, and Policy, 6, S50–S57.CrossRefGoogle Scholar
Styner, M., Knickmeyer, R., Joshi, S., Coe, C., Short, S. J., & Gilmore, J.. (2007). Automatic brain segmentation in rhesus monkeys. P Soc Photo-Opt Ins, 6512, L5122.Google Scholar
Sugita, Y. (2008). Face perception in monkeys reared with no exposure to faces. Proceedings of the National Academy of Sciences USA, 105, 394–398. doi:10.1073/pnas.0706079105CrossRefGoogle ScholarPubMed
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000). Good memories of bad events in infancy. Nature, 407, 38–39. doi:10.1038/35024156CrossRefGoogle ScholarPubMed
Tang, C. Y., & Ramani, R. (2016). fMRI and anesthesia. International Anesthesiology Clinics, 54(1), 129–142. doi:10.1097/AIA.0000000000000081CrossRefGoogle ScholarPubMed
Tarullo, A. R., & Gunnar, M. R. (2006). Child maltreatment and the developing HPA axis. Hormones and Behavior, 50, 632–639. doi:10.1016/j.yhbeh.2006.06.010CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17, 652–666. doi:10.1038/nrn.2016.111CrossRefGoogle ScholarPubMed
Thomason, M. E., Marusak, H. A., Tocco, M. A., Vila, A. M., McGarragle, O., & Rosenberg, D. R. (2015). Altered amygdala connectivity in urban youth exposed to trauma. Social Cognitive and Affective Neuroscience, 10, 1460–1468. doi:10.1093/scan/nsv030CrossRefGoogle ScholarPubMed
Thomason, M. E., & Thompson, P. M. (2011). Diffusion imaging, white matter, and psychopathology. Annual Reviews of Clinical Psychology, 7, 63–85. doi:10.1146/annurev-clinpsy-032210-104507CrossRefGoogle ScholarPubMed
Tottenham, N. (2015). Social scaffolding of human amygdala-mPFCcircuit development. Social Neuroscience, 10, 489–499. doi:10.1080/17470919.2015.1087424CrossRefGoogle ScholarPubMed
Trickett, P. K., Gordis, E., Peckins, M. K., & Susman, E. J. (2014). Stress reactivity in maltreated and comparison male and female young adolescents. Child Maltreatment, 19(1), 27–37.CrossRefGoogle ScholarPubMed
Troisi, A., & D'Amato, F. R. (1984). Ambivalence in monkey mothering. Infant abuse combined with maternal possessiveness. The Journal or Nervous and Mental Disease, 172, 105–108.CrossRefGoogle ScholarPubMed
Van Bockstaele, E. J., Bajic, D., Proudfit, H., & Valentino, R. J. (2001). Topographic architecture of stress-related pathways targeting the noradrenergic locus coeruleus. Physiology & Behavior, 73, 273–283.CrossRefGoogle ScholarPubMed
VanTieghem, M. R., & Tottenham, N. (2018). Neurobiological programming of early life stress: Functional development of amygdala-prefrontal circuitry and vulnerability for stress-related psychopathology. Current Topics in Behavioral Neurosciences, 38, 117–136. doi:10.1007/7854_2016_42CrossRefGoogle ScholarPubMed
Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., … Raichle, M. E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447, 83–86. doi:10.1038/nature05758CrossRefGoogle ScholarPubMed
Vohr, B. R., Wright, L. L., Dusick, A. M., Mele, L., Verter, J., Steichen, J. J., … Kaplan, M. D. (2000). Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993-1994. Pediatrics, 105, 1216–1226.CrossRefGoogle Scholar
Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience, 22, 6810–6818. doi:20026655.CrossRefGoogle ScholarPubMed
Weber, D. L. (2008). Information processing bias in post-traumatic stress disorder. Open Neuroimaging Journal, 2, 29–51. doi:10.2174/1874440000802010029CrossRefGoogle ScholarPubMed
Webster, M. J., Ungerleider, L. G., & Bachevalier, J. (1991a). Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. Journal of Neuroscience, 11, 1095–1116.CrossRefGoogle Scholar
Webster, M. J., Ungerleider, L. G., & Bachevalier, J. (1991b). Lesions of inferior temporal area TE in infant monkeys alter cortico-amygdalar projections. Neuroreport, 2, 769–772.CrossRefGoogle Scholar
Woolrich, M. W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., … Smith, S. M. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage, 45, S173–186. doi:10.1016/j.neuroimage.2008.10.055CrossRefGoogle ScholarPubMed
Yan, C. G., Cheung, B., Kelly, C., Colcombe, S., Craddock, R. C., Di Martino, A., … Milham, M. P. (2013). A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage, 76, 183–201. doi:10.1016/j.neuroimage.2013.03.004CrossRefGoogle ScholarPubMed
Zatorre, R. J., Fields, R. D., & Johansen-Berg, H. (2012). Plasticity in gray and white: Neuroimaging changes in brain structure during learning. Nature Neuroscience, 15, 528–536. doi:10.1038/nn.3045CrossRefGoogle ScholarPubMed
Zhang, W., Jiang, X., Zhang, S., Howell, B. R., Zhao, Y., Zhang, T., … Liu, T. (2017). Connectome-scale functional intrinsic connectivity networks in macaques. Neuroscience, 364, 1–14. doi:10.1016/j.neuroscience.2017.08.022CrossRefGoogle ScholarPubMed