Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-19T06:51:52.075Z Has data issue: false hasContentIssue false

Altered ventral striatal–medial prefrontal cortex resting-state connectivity mediates adolescent social problems after early institutional care

Published online by Cambridge University Press:  22 November 2017

Dominic S. Fareri*
Affiliation:
Adelphi University
Laurel Gabard-Durnam
Affiliation:
Boston Children's Hospital
Bonnie Goff
Affiliation:
University of California–Los Angeles
Jessica Flannery
Affiliation:
University of Oregon
Dylan G. Gee
Affiliation:
Yale University
Daniel S. Lumian
Affiliation:
University of Denver
Christina Caldera
Affiliation:
University of California–Los Angeles
Nim Tottenham
Affiliation:
Columbia University
*
Address correspondence and reprint requests to: Dominic Fareri, Gordon F. Derner School of Psychology, Adelphi University, 212B Blodgett Hall, Garden City, NY 11530; E-mail: dfareri@adelphi.edu.

Abstract

Early caregiving adversity is associated with increased risk for social difficulties. The ventral striatum and associated corticostriatal circuitry, which have demonstrated vulnerability to early exposures to adversity, are implicated in many aspects of social behavior, including social play, aggression, and valuation of social stimuli across development. Here, we used resting-state functional magnetic resonance imaging to assess the degree to which early caregiving adversity was associated with altered coritocostriatal resting connectivity in previously institutionalized youth (n = 41) relative to youth who were raised with their biological families from birth (n = 47), and the degree to which this connectivity was associated with parent-reported social problems. Using a seed-based approach, we observed increased positive coupling between the ventral striatum and anterior regions of medial prefrontal cortex (mPFC) in previously institutionalized youth. Stronger ventral striatum–mPFC coupling was associated with parent reports of social problems. A moderated-mediation analysis showed that ventral striatal–mPFC connectivity mediated group differences in social problems, and more so with increasing age. These findings show that early institutional care is associated with differences in resting-state connectivity between the ventral striatum and the mPFC, and this connectivity seems to play an increasingly important role in social behaviors as youth enter adolescence.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

This work was supported by National Institute of Mental Health Grant R01MH091864 (to N.T.) and the Dana Foundation.

References

Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7, 268277. doi:10.1038/nrn1884 Google Scholar
Báez-Mendoza, R., Harris, C. J., & Schultz, W. (2013). Activity of striatal neurons reflects social action and own reward. Proceedings of the National Academy of Sciences, 110, 2013. doi:10.1073/pnas.1211342110 Google Scholar
Báez-Mendoza, R., & Schultz, W. (2013). The role of the striatum in social behavior. Frontiers in Neuroscience, 7, 233. doi:10.3389/fnins.2013.00233 Google Scholar
Bartra, O., McGuire, J. T., & Kable, J. W. (2013). The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. NeuroImage, 76, 412427. doi:10.1016/j.neuroimage.2013.02.063 Google Scholar
Bos, K., Zeanah, C. H., Fox, N. A., Drury, S. S., McLaughlin, K. A., & Nelson, C. A. (2011). Psychiatric outcomes in young children with a history of institutionalization. Harvard Review of Psychiatry, 19, 1524. doi:10.3109/10673229.2011.549773 CrossRefGoogle ScholarPubMed
Burgund, E. D., Kang, H. C., Kelly, J. E., Buckner, R. L., Snyder, A. Z., Petersen, S. E., & Schlaggar, B. L. (2002). The feasibility of a common stereotactic space for children and adults in fMRI studies of development. NeuroImage, 17, 184200. doi:10.1006/nimg.2002.1174 Google Scholar
Burnett, S., Sebastian, C., Kadosh, K. C., & Blakemore, S.-J. (2011). The social brain in adolescence: Evidence from functional magnetic resonance imaging and behavioural studies. Neuroscience & Biobehavioral Reviews, 35, 16541664. doi:10.1016/j.neubiorev.2010.10.011 CrossRefGoogle ScholarPubMed
Callaghan, B. L., & Richardson, R. (2011). Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behavioral Neuroscience, 125, 2028. doi:10.1037/a0022008 CrossRefGoogle ScholarPubMed
Callaghan, B. L., & Tottenham, N. (2015). The neuro-environmental loop of plasticity: A cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving. Neuropsychopharmacology, 41, 163176. doi:10.1038/npp.2015.204 Google Scholar
Casey, B. J. (2015). Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annual Review of Psychology, 66, 295319. doi:10.1146/annurev-psych-010814-015156 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, 749760. doi:10.1016/j.neuron.2010.08.033 Google Scholar
Chen, G., Chen, G., Xie, C., Ward, B. D., Li, W., Antuono, P., & Li, S.-J. (2012). A method to determine the necessity for global signal regression in resting-state fMRI studies. Magnetic Resonance in Medicine, 68, 18281835. doi:10.1002/mrm.24201 CrossRefGoogle ScholarPubMed
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magentic resonance neuroimages. Computers and Biomedical Research, 29, 162173.Google Scholar
Crone, E. A., & Dahl, R. E. (2012). Understanding adolescence as a period of social–affective engagement and goal flexibility. Nature Reviews Neuroscience, 13, 636650. doi:10.1038/nrn3313 CrossRefGoogle ScholarPubMed
Delgado, M. R., Frank, R., & Phelps, E. A. (2005). Perceptions of moral character modulate the neural systmes of reward during the trust game. Nature Neuroscience, 8, 16111618. doi:10.1038/nn1575 Google Scholar
Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D., & Fiez, J. A. (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology, 84, 30723077.Google Scholar
Di Martino, A., Kelly, C., Grzadzinski, R., Zuo, X.-N., Mennes, M., Mairena, M. A., … Milham, M. P. (2011). Aberrant striatal functional connectivity in children with autism. Biological Psychiatry, 69, 847856. doi:10.1016/j.biopsych.2010.10.029 Google Scholar
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Shehzad, Z., … Milham, M. P. (2008). Functional connectivity of human striatum: A resting state fMRI study. Cerebral Cortex, 18, 27352747. doi:10.1093/cercor/bhn041 Google Scholar
Efron, B. (1987). Better bootstrap confidence intervals. Journal of the American Statistical Association, 82, 171185. doi:10.1080/01621459.1987.10478410 Google Scholar
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Correction for Eklund et al., Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences, 113, E4929. doi:10.1073/pnas.1612033113 Google Scholar
Ernst, M., Nelson, E. E., Jazbec, S., McClure, E. B., Monk, C. S., Leibenluft, E., … Pine, D. S. (2005). Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. NeuroImage, 25, 12791291. doi:10.1016/j.neuroimage.2004.12.038 Google Scholar
Fareri, D. S., Chang, L. J., & Delgado, M. R. (2012). Effects of direct social experience on trust decisions and neural reward circuitry. Frontiers in Neuroscience, 6, 148. doi:10.3389/fnins.2012.00148 CrossRefGoogle ScholarPubMed
Fareri, D. S., Chang, L. J., & Delgado, M. R. (2015). Computational substrates of social value in interpersonal collaboration. Journal of Neuroscience, 35, 81708180. doi:10.1523/jneurosci.4775-14.2015 Google Scholar
Fareri, D. S., & Delgado, M. R. (2014). The importance of social rewards and social networks in the human brain. Neuroscientist, 20, 387402. doi:10.1177/1073858414521869 Google Scholar
Fareri, D. S., Gabard-Durnam, L., Goff, B., Flannery, J., Gee, D. G., Lumian, D. S., … Tottenham, N. (2015). Normative development of ventral striatal resting state connectivity in humans. NeuroImage, 118, 422437. doi:10.1016/j.neuroimage.2015.06.022 Google Scholar
Fareri, D. S., Martin, L. N., & Delgado, M. R. (2008). Reward-related processing in the human brain: Developmental considerations. Development and Psychopathology, 20, 11911211. doi:10.1017/S0954579408000576 CrossRefGoogle ScholarPubMed
Fareri, D. S., Niznikiewicz, M. A., Lee, V. K., & Delgado, M. R. (2012). Social network modulation of reward-related signals. Journal of Neuroscience, 32, 90459052. doi:10.1523/jneuroscI.0610-12.2012 Google Scholar
Fareri, D. S., & Tottenham, N. (2016). Effects of early life stress on amygdala and striatal development. Developmental Cognitive Neuroscience, 19, 233247. doi:10.1016/j.dcn.2016.04.005 Google Scholar
Frith, C. D., & Frith, U. (2006). The neural basis of mentalizing. Neuron, 50, 531534. doi:10.1016/j.neuron.2006.05.001 Google 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, 193207. doi:10.1016/j.neuroimage.2014.03.038 CrossRefGoogle ScholarPubMed
Gabard-Durnam, L. J., Gee, D. G., Goff, B., Flannery, J., Telzer, E., Humphreys, K. L., … Tottenham, N. (2016). Stimulus elicited connectivity influences resting-state connectivity years later in human development: A prospective study. Journal of Neuroscience, 36, 47714784. doi:10.1523/JNEUROSCI.0598-16.2016 Google Scholar
Galván, A. (2010). Adolescent development of the reward system. Frontiers in Human Neuroscience, 4, 6. doi:10.3389/neuro.09.006.2010 Google ScholarPubMed
Galván, A. (2013). Neural systems underlying reward and approach behaviors in childhood and adolescence. Current Topics in Behavioral Neurosciences, 16, 167188. doi:10.1007/7854_2013_240 Google Scholar
Galván, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., & Casey, B. J. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience, 26, 68856892. doi:10.1523/jneurosci.1062-06.2006 Google Scholar
Galván, A., & McGlennen, K. M. (2012). Enhanced striatal sensitivity to aversive reinforcement in adolescents versus adults. Journal of Cognitive Neuroscience, 25, 284296. doi:10.1162/jocn_a_00326 Google Scholar
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, 110, 1563815643. doi:10.1073/pnas.1307893110 CrossRefGoogle ScholarPubMed
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., … Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33, 45844593. doi:10.1523/jneurosci.3446-12.2013 Google Scholar
Gleason, M. M., Fox, N. A., Drury, S. S., Smyke, A. T., Nelson, C. A., & Zeanah, C. H. (2014). Indiscriminate behaviors in previously institutionalized young children. Pediatrics, 133, e657e665. doi:10.1542/peds.2013-0212 Google Scholar
Goff, B., Gee, D. G., Telzer, E. H., Humphreys, K. L., Gabard-Durnam, L., Flannery, J., & Tottenham, N. (2013). Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience, 249, 129138. doi:10.1016/j.neuroscience.2012.12.010 Google Scholar
Groenewegen, H. J., Wright, C. I., Beijer, A. V. J., & Voorn, P. (1999). Convergence and segregation of ventral striatal inputs and outputs. Annals of the New York Academy of Sciences, 877, 4963. doi:10.1111/j.1749-6632.1999.tb09260.x CrossRefGoogle ScholarPubMed
Gunnar, M., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145173. doi:10.1146/annurev.psych.58.110405.085605 Google Scholar
Haber, S. N. (2003). The primate basal ganglia: Parallel and integrative networks. Journal of Chemical Neuroanatomy, 26, 317330.Google Scholar
Haber, S. N., Kim, K.-S., Mailly, P., & Calzavara, R. (2006). Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. Journal of Neuroscience, 26, 83688376. doi:10.1523/jneurosci.0271-06.2006 Google Scholar
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 426. doi:10.1038/npp.2009.129 Google Scholar
Haber, S. N., & McFarland, N. R. (1999). The concept of the ventral striatum in nonhuman primates. Annals of the New York Academy of Sciences, 877, 3348. doi:10.1111/j.1749-6632.1999.tb09259.x Google Scholar
Hallquist, M. N., Hwang, K., & Luna, B. (2013). The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage, 82C, 208225. doi:10.1016/j.neuroimage.2013.05.116 Google Scholar
Hampson, M., Driesen, N., Roth, J. K., Gore, J. C., & Constable, R. T. (2010). Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. Magnetic Resonance Imaging, 28, 10511057. doi:10.1016/j.mri.2010.03.021.Google Scholar
Hampton, A. N., Bossaerts, P., & O'Doherty, J. P. (2008). Neural correlates of mentalizing-related computations during strategic interactions in humans. Proceedings of the National Academy of Sciences, 105, 67416746. doi:10.1073/pnas.0711099105 CrossRefGoogle ScholarPubMed
Hanson, J. L., Hariri, A. R., & Williamson, D. E. (2015). Archival Report. Biological Psychiatry, 78, 598605. doi:10.1016/j.biopsych.2015.05.010 CrossRefGoogle Scholar
Härfstrand, A., Fuxe, K., Cintra, A., Agnati, L. F., Zini, I., Wikström, A. C., … Steinbusch, H. (1986). Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proceedings of the National Academy of Sciences, 83, 97799783.Google Scholar
Hayes, A. F. (2012). PROCESS: A versatile computational tool for observed variable mediation, moderation and conditional process modeling [White paper]. Retrieved July 28, 2014, from http://www.afhayes.com/public/process2012pdf Google Scholar
Hayes, A. F., & Scharkow, M. (2013). The relative trustworthiness of inferential tests of the indirect effect in statistical mediation analysis: Does method really matter? Psychological Science, 24, 19181927. doi:10.1177/0956797613480187 Google Scholar
Hodges, J., & Tizard, B. (1989). Social and family relationships of ex-institutional adolescents. Journal of Child Psychology and Psychiatry, 30, 7797.Google Scholar
Humphreys, K. L., Lee, S. S., Telzer, E. H., Gabard-Durnam, L. J., Goff, B., Flannery, J., & Tottenham, N. (2015). Exploration-exploitation strategy is dependent on early experience. Developmental Psychobiology, 57, 313321. doi:10.1002/dev.21293 Google Scholar
Izuma, K., Saito, D. N., & Sadato, N. (2008). Processing of social and monetary rewards in the human striatum. Neuron, 58, 284294. doi:10.1016/j.neuron.2008.03.020 Google Scholar
Izuma, K., Saito, D. N., & Sadato, N. (2010). Processing of the incentive for social approval in the ventral striatum during charitable donation. Journal of Cognitive Neuroscience, 22, 621631. doi:10.1162/jocn.2009.21228 Google Scholar
Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Powers, A., Mehta, N., … Casey, B. J. (2014). Adolescent-specific patterns of behavior and neural activity during social reinforcement learning. Cognitive, Affective, and Behavioral Neuroscience, 14, 683697. doi:10.3758/s13415-014-0257-z Google Scholar
Kang, H. C., Burgund, E. D., Lugar, H. M., Petersen, S. E., & Schlaggar, B. L. (2003). Comparison of functional activation foci in children and adults using a common stereotactic space. NeuroImage, 19, 1628. doi:10.1016/S1053-8119(03)00038-7 Google Scholar
Knutson, B., Adams, C., Fong, G., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21, RC159. doi:20015472 Google Scholar
Knutson, B., Taylor, J., Kaufman, M., Peterson, R., & Glover, G. (2005). Distributed neural representation of expected value. Journal of Neuroscience, 25, 48064812. doi:10.1523/jneurosci.0642-05.2005 Google Scholar
Kohls, G., Perino, M. T., Taylor, J. M., Madva, E. N., & Cayless, S. J. (2013). The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment. Neuropsychologia, 51, 20622069. doi:10.1016/j.neuropsychologia.2013.07.020 Google Scholar
Krienen, F. M., Tu, P. C., & Buckner, R. L. (2010). Clan mentality: Evidence that the medial prefrontal cortex responds to close others. Journal of Neuroscience, 30, 1390613915. doi:10.1523/jneurosci.2180-10.2010 Google Scholar
Li, J., Schiller, D., Schoenbaum, G., Phelps, E. A., & Daw, N. D. (2011). Differential roles of human striatum and amygdala in associative learning. Nature Neuroscience, 14, 12501252. doi:10.1038/nn.2904 CrossRefGoogle ScholarPubMed
Loman, M. M., Johnson, A. E., Quevedo, K., Lafavor, T. L., & Gunnar, M. R. (2014). Risk-taking and sensation-seeking propensity in postinstitutionalized early adolescents. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 55, 11451152. doi:10.1111/jcpp.12208 Google Scholar
Lovallo, W. R., Farag, N. H., Sorocco, K. H., Acheson, A., Cohoon, A. J., & Vincent, A. S. (2012). Early life adversity contributes to impaired cognition and impulsive behavior: Studies from the Oklahoma Family Health Patterns Project. Alcoholism, Clinical and Experimental Research, 37, 616623. doi:10.1111/acer.12016 Google Scholar
Matthews, K., Dalley, J. W., Matthews, C., Tsai, T. H., & Robbins, T. W. (2001). Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse, 40, 110. doi:10.1002/1098-2396(200104)40:1 Google Scholar
Matthews, K., & Robbins, T. W. (2003). Early experience as a determinant of adult behavioural responses to reward: The effects of repeated maternal separation in the rat. Neuroscience & Biobehavioral Reviews, 27, 4555. doi:10.1016/S0149-7634(03)00008-3 Google Scholar
Matthews, K., Wilkinson, L. S., & Robbins, T. W. (1996). Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiology and Behavior, 59, 99107.Google Scholar
McLaughlin, K. A., Sheridan, M. A., Winter, W., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2014). Widespread reductions in cortical thickness following severe early-life deprivation: A neurodevelopmental pathway to attention-deficit/hyperactivity disorder. Biological Psychiatry, 76, 629638. doi:10.1016/j.biopsych.2013.08.016 Google Scholar
Mehta, M. A., Gore-Langton, E., Golembo, N., Colvert, E., Williams, S. C. R., & Sonuga-Barke, E. (2010). Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. Journal of Cognitive Neuroscience, 22, 23162325. doi:10.1162/jocn.2009.21394 Google Scholar
Meyer-Lindenberg, A., & Tost, H. (2012). Neural mechanisms of social risk for psychiatric disorders. Nature Neuroscience, 15, 663668. doi:10.1038/nn.3083 Google Scholar
Miranda-Dominguez, O., Mills, B. D., Grayson, D., Woodall, A., Grant, K. A., Kroenke, C. D., & Fair, D. A. (2014). 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, 55525563. doi:10.1523/jneurosci.4229-13.2014 CrossRefGoogle Scholar
Mitchell, J. P., Banaji, M. R., & Macrae, C. N. (2005). The link between social cognition and self-referential thought in the medial prefrontal cortex. Journal of Cognitive Neuroscience, 17, 13061315. doi:10.1162/0898929055002418 Google Scholar
Olsavsky, A. K., Telzer, E. H., Shapiro, M., Humphreys, K. L., Flannery, J., Goff, B., & Tottenham, N. (2013). Indiscriminate amygdala response to mothers and strangers after early maternal deprivation. Biological Psychiatry, 74, 853860. doi:10.1016/j.biopsych.2013.05.025 Google Scholar
Overton, P. G., Tong, Z. Y., Brain, P. F., & Clark, D. (1996). Preferential occupation of mineralocorticoid receptors by corticosterone enhances glutamate-induced burst firing in rat midbrain dopaminergic neurons. Brain Research, 737, 146154.Google Scholar
Pfeifer, J. H., Kahn, L. E., Merchant, J. S., Peake, S. J., Veroude, K., Masten, C. L., … Dapetto, M. (2013). Longitudinal change in the neural bases of adolescent social self-evaluations: Effects of age and pubertal development. Journal of Neuroscience, 33, 74157419. doi:10.1523/jneurosci.4074-12.2013 Google Scholar
Pfeifer, J. H., Masten, C. L., Moore, W. E. III, Oswald, T. M., Mazziotta, J. C., Iacoboni, M., & Dapretto, M. (2011). Entering adolescence: Resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron, 69, 10291036. doi:10.1016/j.neuron.2011.02.019 CrossRefGoogle ScholarPubMed
Phan, K. L., Sripada, C. S., Angstadt, M., & McCabe, K. (2010). Reputation for reciprocity engages the brain reward center. Proceedings of the National Academy of Sciences, 107, 1039913104. doi:10.1073/pnas.1008137107 Google Scholar
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, 21422154. doi:10.1016/j.neuroimage.2011.10.018 Google Scholar
Power, J. D., Schlaggar, B. L., & Petersen, S. E. (2015). Recent progress and outstanding issues in motion correction in resting state fMRI. NeuroImage, 105, 536551. doi:10.1016/j.neuroimage.2014.10.044 Google Scholar
Puetz, V. B., Kohn, N., Dahmen, B., Zvyagintsev, M., Schüppen, A., Schultz, R. T., … Konrad, K. (2014). Neural response to social rejection in children with early separation experiences. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 13281337. doi:10.1016/j.jaac.2014.09.004 Google Scholar
Rilling, J., Gutman, D., Zeh, T., Pagnoni, G., Berns, G., & Kilts, C. (2002). A neural basis for social cooperation. Neuron, 35, 395405. doi:10.1016/S0896-6273(02)00755-9 Google Scholar
Robbins, T. W., Cador, M., Taylor, J. R., & Everitt, B. J. (1989). Limbic-striatal interactions in reward-related processes. Current Opinion in Neurobiology, 13, 155162.Google Scholar
Roy, P., Rutter, M., & Pickles, A. (2004). Institutional care: Associations between overactivity and lack of selectivity in social relationships. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 45, 866873. doi:10.1111/j.1469-7610.2004.00278.x Google Scholar
Rutledge, R. B., Dean, M., Caplin, A., & Glimcher, P. W. (2010). Testing the reward prediction error hypothesis with an axiomatic model. Journal of Neuroscience, 30, 1352513536. doi:10.1523/jneurosci.1747-10.2010 Google Scholar
Saad, Z., Reynolds, R. C., Jo, H. J., Gotts, S. J., Chen, G., Martin, A., & Cox, R. (2013). Correcting brain-wide correlation differences in resting-state FMRI. Brain Connectivity, 3, 339352. doi:10.1089/brain.2013.0156 Google Scholar
Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., … Wolf, D. H. (2013). An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage, 64, 240256. doi:10.1016/j.neuroimage.2012.08.052 Google Scholar
Satterthwaite, T. D., Wolf, D. H., Loughead, J., Ruparel, K., Elliott, M. A., Hakonarson, H., … Gur, R. E. (2012). Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth. NeuroImage, 60, 623632. doi:10.1016/j.neuroimage.2011.12.063 Google Scholar
Schonberg, T., Daw, N., Joel, D., & O'Doherty, J. (2007). Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. Journal of Neurocscience, 27, 1286012867. doi:27/47/12860 Google Scholar
Silvers, J. A., Insel, C., Powers, A., Franz, P., Weber, J., Mischel, W., … Ochshner, K. N. (2014). Curbing craving: Behavioral and brain evidence that children regulate craving when instructed to do so but have higher baseline craving than adults. Psychological Science, 25, 19321942. doi:10.1177/0956797614546001 Google Scholar
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L., Gee, D. G., Goff, B., Fareri, D. S., … Tottenham, N. (2016). Previous institutionalization is followed by broader amygdala-hippocampal-PFC network connectivity during aversive learning in human development. Journal of Neuroscience, 36, 64206430. doi:10.1523/jneurosci.0038-16.2016 CrossRefGoogle ScholarPubMed
Smith, D. V., Clithero, J. A., Boltuck, S. E., & Huettel, S. A. (2014). Functional connectivity with ventromedial prefrontal cortex reflects subjective value for social rewards. Social Cognitive and Affective Neuroscience, 9, 20172025. doi:10.1093/scan/nsu005 Google Scholar
Smith, D. V., Hayden, B. Y., Truong, T.-K., Song, A. W., Platt, M. L., & Huettel, S. A. (2010). Distinct value signals in anterior and posterior ventromedial prefrontal cortex. Journal of Neuroscience, 30, 24902495. doi:10.1523/JNEUROSCI.3319-09.2010 Google Scholar
Somerville, L. H., Hare, T., & Casey, B. J. (2011). Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. Journal of Cognitive Neuroscience, 23, 21232134. doi:10.1162/jocn.2010.21572 CrossRefGoogle ScholarPubMed
Somerville, L. H., Heatherton, T. F., & Kelley, W. M. (2006). Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nature Neuroscience, 9, 10071008. doi:10.1038/nn1728 Google Scholar
Somerville, L. H., Jones, R. M., & Casey, B. J. (2010). A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition, 72, 124133. doi:10.1016/j.bandc.2009.07.003 Google Scholar
Supekar, K., Musen, M., & Menon, V. (2009). Development of large-scale functional brain networks in children. PLOS Biology, 7, e1000157. doi:10.1371/journal.pbio.1000157 Google Scholar
Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: George Thieme.Google Scholar
Tops, M., Koole, S. L., Ijzerman, H., & Buisman-Pijlman, F. T. A. (2014). Why social attachment and oxytocin protect against addiction and stress: Insights from the dynamics between ventral and dorsal corticostriatal systems. Pharmacology Biochemistry and Behavior, 119, 3948. doi:10.1016/j.pbb.2013.07.015 CrossRefGoogle ScholarPubMed
Tottenham, N., & Galván, A. (2016). Stress and the adolescent brain: Amygdala-prefrontal cortex circuitry and ventral striatum as developmental targets. Neuroscience & Biobehavioral Reviews, 70, 217227. doi:10.1016/j.neubiorev.2016.07.030 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, 190204. doi:10.1111/j.1467-7687.2010.00971.x Google Scholar
Tziortzi, A. C., Searle, G. E., Tzimopoulou, S., Salinas, C., Beaver, J. D., Jenkinson, M., … Gunn, R. L. (2011). Imaging dopamine receptors in humans with [11C]-(+)-PHNO: Dissection of D3 signal and anatomy. NeuroImage, 54, 264277. doi:10.1016/j.neuroimage.2010.06.044 Google Scholar
Van Dijk, K. R. A., Hedden, T., Venkataraman, A., Evans, K. C., Lazar, S. W., & Buckner, R. L. (2010). Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. Journal of Neurophysiology, 103, 297321. doi:10.1152/jn.00783.2009 Google Scholar
Van Dijk, K. R. A., Sabuncu, M. R., & Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. NeuroImage, 59, 431438. doi:10.1016/j.neuroimage.2011.07.044 Google Scholar
Vrtička, P., & Vuilleumier, P. (2012). Neuroscience of human social interactions and adult attachment style. Frontiers in Human Neuroscience, 6, 212. doi:10.3389/fnhum.2012.00212 Google Scholar
Wang, K. S., Smith, D. V., & Delgado, M. R. (2016). Using fMRI to study reward processing in humans: Past, present, and future. Journal of Neurophysiology, 115, 16641678. doi:10.1152/jn.00333.2015 Google Scholar
Weschsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. New York: Psychological Corporation.Google Scholar