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Neural correlates of emotion processing predict resilience in youth at familial risk for mood disorders

Published online by Cambridge University Press:  08 May 2019

Akua F. Nimarko ,
Amy S. Garrett ,
Gabrielle A. Carlson  and
Manpreet K. Singh
Akua F. Nimarko
Affiliation:
Stanford Neurosciences Graduate Program, Stanford University School of Medicine, Stanford, CA, USA
Amy S. Garrett
Affiliation:
Department of Psychiatry, University of Texas Health Science Center, San Antonio, TX, USA
Gabrielle A. Carlson
Affiliation:
Department of Psychiatry, Stonybrook University School of Medicine, Stony Brook, NY, USA
Manpreet K. Singh*
Affiliation:
Stanford Neurosciences Graduate Program, Stanford University School of Medicine, Stanford, CA, USA Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA
*
Address for Correspondence: Manpreet K. Singh, Department of Psychiatry and Behavioral Sciences, Stanford University, 401 Quarry Road, Stanford, CA, 94305; E-mail: mksingh@stanford.edu.
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Abstract

Aberrant face emotion processing has been demonstrated in youth with and at a familial risk for bipolar and major depressive disorders. However, the neurobiological factors related to emotion processing that underlie resilience from youth-onset mood disorders are not well understood. Functional magnetic resonance imaging data during an implicit emotion processing task were collected at baseline from a sample of 50 youth, ages 8–17, who were healthy but also familially at high risk for either bipolar disorder or major depressive disorder, and 24 healthy controls with no family history of psychopathology (HCL). Participants were reevaluated 3 years later and classified into three groups for analysis: high-risk youth who converted to a psychiatric diagnosis (CVT; N = 23), high-risk youth who were resilient from developing any psychopathology (RES; N = 27), and HCL youth (N = 24) who remained healthy at follow-up. For happy > calm faces, the CVT and RES groups had significantly lower activation in the left inferior parietal lobe (IPL), while the RES group had lower activation in the right supramarginal gyrus. For fear > calm faces, the RES group had lower activation in the right precuneus and inferior frontal gyrus (IFG) compared to the CVT group. Connectivity analyses revealed the RES group exhibited higher left IPL connectivity with visual cortical regions for happy > calm faces, and higher IFG connectivity with frontal, temporal, and limbic regions for fear > calm faces. These connectivities were correlated with improvements in prosocial behaviors and global functioning. Our findings suggest that differential activation and connectivity in the IPL, IFG, and precuneus in response to emotional stimuli may represent distinct resilience and risk markers for youth-onset mood disorders.

Keywords

bipolar disorderemotion processingfunctional connectivityfunctional magnetic resonance imagingmajor depressive disorderyouth
Type
Special Issue Articles
Information
Development and Psychopathology , Volume 31 , Special Issue 3: Emotion Dysregulation and Emerging Psychopathology , August 2019 , pp. 1037 - 1052
Copyright
Copyright © Cambridge University Press 2019 

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References

Ahmed, S. P., Bittencourt-Hewitt, A., & Sebastian, C. L. (2015). Neurocognitive bases of emotion regulation development in adolescence. Developmental Cognitive Neuroscience, 15, 11–25. doi:10.1016/J.DCN.2015.07.006Google Scholar
Alarcón, G., & Forbes, E. E. (2017). Prosocial behavior and depression: A case for developmental gender differences. Current Behavioral Neuroscience Reports, 4, 117–127. doi:10.1007/s40473-017-0113-xGoogle Scholar
Beauchaine, T. P. (2015). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875–896. doi:10.1080/15374416.2015.1038827Google Scholar
Breakspear, M., Roberts, G., Green, M. J., Nguyen, V. T., Frankland, A., Levy, F., … Mitchell, P. B. (2015). Network dysfunction of emotional and cognitive processes in those at genetic risk of bipolar disorder. Brain, 138, 3427–3439. doi:10.1093/brain/awv261Google Scholar
Brotman, M. A., Rich, B. A., Guyer, A. E., Lunsford, J. R., Horsey, S. E., Reising, M. M., … Leibenluft, E. (2010). Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder. American Journal of Psychiatry, 167, 61–69. doi:10.1176/appi.ajp.2009.09010043Google Scholar
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129, 564–583. doi:10.1093/brain/awl004Google Scholar
Chang, K., Garrett, A., Kelley, R., Howe, M., Sanders, E. M., Acquaye, T., … Reiss, A. (2017). Anomalous prefrontal-limbic activation and connectivity in youth at high-risk for bipolar disorder. Journal of Affective Disorders, 222, 7–13. doi:10.1016/J.JAD.2017.05.051Google Scholar
Chen, C.-H., Lennox, B., Jacob, R., Calder, A., Lupson, V., Bisbrown-Chippendale, R., … Bullmore, E. (2006). Explicit and implicit facial affect recognition in manic and depressed states of bipolar disorder: A functional magnetic resonance imaging study. Biological Psychiatry, 59, 31–39. doi:10.1016/J.BIOPSYCH.2005.06.008Google Scholar
Cicchetti, D., & Blender, J. A. (2006). A multiple-levels-of-analysis perspective on resilience: Implications for the developing brain, neural plasticity, and preventive interventions. Annals of the New York Academy of Sciences, 1094, 248–258. doi:10.1196/annals.1376.029Google Scholar
Cicchetti, D., & Rogosch, F. A. (1999). Psychopathology as risk for adolescent substance use disorders: A developmental psychopathology perspective. Journal of Clinical Child Psychology, 28, 355–365. doi:10.1207/S15374424jccp280308Google Scholar
Comasco, E., Åslund, C., Oreland, L., & Nilsson, K. W. (2013). Three-way interaction effect of 5-HTTLPR, BDNF Val66Met, and childhood adversity on depression: A replication study. European Neuropsychopharmacology, 23, 1300–1306. doi:10.1016/J.EURONEURO.2013.01.010Google Scholar
Daches, S., Vine, V., Layendecker, K. M., George, C. J., & Kovacs, M. (2018). Family functioning as perceived by parents and young offspring at high and low risk for depression. Journal of Affective Disorders, 226, 355–360. doi:10.1016/j.jad.2017.09.031Google Scholar
Dang, M. T. (2014). Social connectedness and self-esteem: Predictors of resilience in mental health among maltreated homeless youth. Issues in Mental Health Nursing, 35, 212–219. doi:10.3109/01612840.2013.860647Google Scholar
DelBello, M. P., & Geller, B. (2001). Review of studies of child and adolescent offspring of bipolar parents. Bipolar Disorders, 3, 325–334. doi:10.1034/j.1399-5618.2001.30607.xGoogle Scholar
Del Piero, L. B., Saxbe, D. E., & Margolin, G. (2016). Basic emotion processing and the adolescent brain: Task demands, analytic approaches, and trajectories of changes. Developmental Cognitive Neuroscience, 19, 174–189. doi:10.1016/j.dcn.2016.03.005Google Scholar
Doom, J. R., & Cicchetti, D. (2018). The developmental psychopathology of stress exposure in childhood. In Harkness, K. & Hayden, E. P. (Eds.), The Oxford handbook of stress and mental health. Oxford: Oxford University Press.Google Scholar
Duffy, A., Vandeleur, C., Heffer, N., & Preisig, M. (2017). The clinical trajectory of emerging bipolar disorder among the high-risk offspring of bipolar parents: Current understanding and future considerations. International Journal of Bipolar Disorders, 5, 37. doi:10.1186/s40345-017-0106-4Google Scholar
Eddy, C. M. (2016). The junction between self and other? Temporo-parietal dysfunction in neuropsychiatry. Neuropsychologia, 89, 465–477. doi:10.1016/J.NEUROPSYCHOLOGIA.2016.07.030Google Scholar
Fears, S. C., Service, S. K., Kremeyer, B., Araya, C., Araya, X., Bejarano, J., … Bearden, C. E. (2014). Multisystem component phenotypes of bipolar disorder for genetic investigations of extended pedigrees. JAMA Psychiatry, 71, 375–387. doi:10.1001/jamapsychiatry.2013.4100Google Scholar
Fischer, A. S., Camacho, M. C., Ho, T. C., Whitfield-Gabrieli, S., & Gotlib, I. H. (2018). Neural markers of resilience in adolescent females at familial risk for major depressive disorder. JAMA Psychiatry, 75, 493–502. doi:10.1001/jamapsychiatry.2017.4516Google Scholar
Forbes, E. E., Shaw, D. S., Silk, J. S., Feng, X., Cohn, J. F., Fox, N. A., & Kovacs, M. (2008). Children's affect expression and frontal EEG asymmetry: Transactional associations with mothers’ depressive symptoms. Journal of Abnormal Child Psychology, 36, 207–221. doi:10.1007/s10802-007-9171-yGoogle Scholar
Frangou, S. (2009). Risk and resilience in bipolar disorder: Rationale and design of the Vulnerability to Bipolar Disorders Study (VIBES). Biochemical Society Transactions, 37(Pt. 5), 1085–1089. doi:10.1042/BST0371085Google Scholar
Frangou, S. (2011). Brain structural and functional correlates of resilience to bipolar disorder. Frontiers in Human Neuroscience, 5, 184. doi:10.3389/fnhum.2011.00184Google Scholar
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., … Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience, 34, 418–432.Google Scholar
Garrett, A. S., Reiss, A. L., Howe, M. E., Kelley, R. G., Singh, M. K., Adleman, N. E., … Chang, K. D. (2012). Abnormal amygdala and prefrontal cortex activation to facial expressions in pediatric bipolar disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 821–831. doi:10.1016/j.jaac.2012.06.005Google Scholar
Geller, B., Zimerman, B., Williams, M., Bolhofner, K., Craney, J. L., DelBello, M. P., & Soutullo, C. (2001). Reliability of the Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia (WASH-U-KSADS) mania and rapid cycling sections. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 450–455. doi:10.1097/00004583-200104000-00014Google Scholar
Glover, G. H., & Law, C. S. (2001). Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magnetic Resonance in Medicine, 46, 515–522. doi:10.1002/mrm.1222Google Scholar
Goodman, R. (1997). The Strengths and Difficulties Questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38, 581–586. doi:10.1111/j.1469-7610.1997.tb01545.xGoogle Scholar
Goodman, S. H., & Gotlib, I. H. (1999). Risk for psychopathology in the children of depressed mothers: A developmental model for understanding mechanisms of transmission. Psychological Review, 106, 458–490. doi:10.1037/0033-295X.106.3.458Google Scholar
Gotlib, I. H., & Joormann, J. (2010). Cognition and depression: Current status and future directions. Annual Review of Clinical Psychology, 6, 285–312. doi:10.1146/annurev.clinpsy.121208.131305Google Scholar
Gröger, N., Matas, E., Gos, T., Lesse, A., Poeggel, G., Braun, K., & Bock, J. (2016). The transgenerational transmission of childhood adversity: Behavioral, cellular, and epigenetic correlates. Journal of Neural Transmission, 123, 1037–1052. doi:10.1007/s00702-016-1570-1Google Scholar
Hafeman, D. M., Bebko, G., Bertocci, M. A., Fournier, J. C., Bonar, L., Perlman, S. B., … Phillips, M. L. (2014). Abnormal deactivation of the inferior frontal gyrus during implicit emotion processing in youth with bipolar disorder: Attenuated by medication. Journal of Psychiatric Research, 58, 129–136. doi:10.1016/j.jpsychires.2014.07.023Google Scholar
Hall, L. M. J., Klimes-Dougan, B., Hunt, R. H., Thomas, K. M., Houri, A., Noack, E., … Cullen, K. R. (2014). An fMRI study of emotional face processing in adolescent major depression. Journal of Affective Disorders, 168, 44–50. doi:10.1016/j.jad.2014.06.037Google Scholar
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223–233. doi:10.1016/S1364-6613(00)01482-0Google Scholar
Ho, T. C., Connolly, C. G., Henje Blom, E., LeWinn, K. Z., Strigo, I. A., Paulus, M. P., … Yang, T. T. (2015). Emotion-dependent functional connectivity of the default mode network in adolescent depression. Biological Psychiatry, 78, 635–646. doi:10.1016/j.biopsych.2014.09.002Google Scholar
Horesh, N., Apter, A., & Zalsman, G. (2011). Timing, quantity and quality of stressful life events in childhood and preceding the first episode of bipolar disorder. Journal of Affective Disorders, 134, 434–437. doi:10.1016/J.JAD.2011.05.034Google Scholar
Igelström, K. M., & Graziano, M. S. A. (2017). The inferior parietal lobule and temporoparietal junction: A network perspective. Neuropsychologia, 105, 70–83. doi:10.1016/J.NEUROPSYCHOLOGIA.2017.01.001Google Scholar
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62, 782–790. doi:10.1016/J.NEUROIMAGE.2011.09.015Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., … Ryan, N. D. (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children—Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 980–988. doi:10.1097/00004583-199707000-00021Google Scholar
Kerestes, R., Davey, C. G., Stephanou, K., Whittle, S., & Harrison, B. J. (2014). Functional brain imaging studies of youth depression: A systematic review. NeuroImage. Clinical, 4, 209–231. doi:10.1016/j.nicl.2013.11.009Google Scholar
Kerestes, R., Segreti, A. M., Pan, L. A., Phillips, M. L., Birmaher, B., Brent, D. A., & Ladouceur, C. D. (2016). Altered neural function to happy faces in adolescents with and at risk for depression. Journal of Affective Disorders, 192, 143–152. doi:10.1016/j.jad.2015.12.013Google Scholar
Kopala-Sibley, D. C., Jelinek, C., Kessel, E. M., Frost, A., Allmann, A. E. S., & Klein, D. N. (2017). Parental depressive history, parenting styles, and child psychopathology over 6 years: The contribution of each parent's depressive history to the other's parenting styles. Development and Psychopathology, 29, 1469–1482. doi:10.1017/S0954579417000396Google Scholar
Ladouceur, C. D., Farchione, T., Diwadkar, V., Pruitt, P., Radwan, J., Axelson, D. A., … Phillips, M. L. (2011). Differential patterns of abnormal activity and connectivity in the amygdala-prefrontal circuitry in bipolar-I and bipolar-NOS youth. Journal of the American Academy of Child & Adolescent Psychiatry, 50, 1275–1289. doi:10.1016/j.jaac.2011.09.023Google Scholar
Lapalme, M., Hodgins, S., & LaRoche, C. (1997). Children of parents with bipolar disorder: A metaanalysis of risk for mental disorders. Canadian Journal of Psychiatry, 42, 623–631. doi:10.1177/070674379704200609Google Scholar
Leshin, J. C., & Lindquist, K. A. (2018). Neuroimaging of emotion dysregulation. In The Oxford handbook of emotion dysregulation. Oxford: Oxford University Press.Google Scholar
Liakakis, G., Nickel, J., & Seitz, R. J. (2011). Diversity of the inferior frontal gyrus—A meta-analysis of neuroimaging studies. Behavioural Brain Research, 225, 341–347. doi:10.1016/J.BBR.2011.06.022Google Scholar
Luthar, S. S., Cicchetti, D., & Becker, B. (2000). The construct of resilience: A critical evaluation and guidelines for future work. Child Development, 71, 543–562.Google Scholar
Manelis, A., Ladouceur, C. D., Graur, S., Monk, K., Bonar, L. K., Hickey, M. B., … Phillips, M. L. (2015). Altered amygdala-prefrontal response to facial emotion in offspring of parents with bipolar disorder. Brain, 138(Pt. 9), 2777–2790. doi:10.1093/brain/awv176Google Scholar
Martel, M. M. (2013). Sexual selection and sex differences in the prevalence of childhood externalizing and adolescent internalizing disorders. Psychological Bulletin, 139, 1221–1259. doi:10.1037/a0032247Google Scholar
Miklowitz, D. J., Schneck, C. D., Walshaw, P. D., Garrett, A. S., Singh, M. K., Sugar, C. A., & Chang, K. D. (2019). Early intervention for youth at high risk for bipolar disorder: A multisite randomized trial of family-focused treatment. Early Intervention in Psychiatry, 13, 208–216. doi:10.1111/eip.12463Google Scholar
Monk, C. S., Klein, R. G., Telzer, E. H., Schroth, E. A., Mannuzza, S., Moulton, J. L., … Ernst, M. (2008). Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. American Journal of Psychiatry, 165, 90–98. doi:10.1176/appi.ajp.2007.06111917Google Scholar
Olsavsky, A. K., Brotman, M. A., Rutenberg, J. G., Muhrer, E. J., Deveney, C. M., Fromm, S. J., … Leibenluft, E. (2012). Amygdala hyperactivation during face emotion processing in unaffected youth at risk for bipolar disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 294–303. doi:10.1016/j.jaac.2011.12.008Google Scholar
Oquendo, M. A., Ellis, S. P., Chesin, M. S., Birmaher, B., Zelazny, J., Tin, A., … Brent, D. A. (2013). Familial transmission of parental mood disorders: Unipolar and bipolar disorders in offspring. Bipolar Disorders, 15, 764–773. doi:10.1111/bdi.12107Google Scholar
Pagliaccio, D., Luby, J. L., Gaffrey, M. S., Belden, A. C., Botteron, K. N., Harms, M. P., & Barch, D. M. (2013). Functional brain activation to emotional and nonemotional faces in healthy children: Evidence for developmentally undifferentiated amygdala function during the school-age period. Cognitive, Affective and Behavioral Neuroscience, 13, 771–789. doi:10.3758/s13415-013-0167-5Google Scholar
Park, M.-H., Chang, K. D., Hallmayer, J., Howe, M. E., Kim, E., Hong, S. C., & Singh, M. K. (2015). Preliminary study of anxiety symptoms, family dysfunction, and the brain-derived neurotrophic factor (BDNF) Val66Met genotype in offspring of parents with bipolar disorder. Journal of Psychiatric Research, 61, 81–88. doi:10.1016/J.JPSYCHIRES.2014.11.013Google Scholar
Pavuluri, M. N., Passarotti, A. M., Harral, E. M., & Sweeney, J. A. (2009). An fMRI study of the neural correlates of incidental versus directed emotion processing in pediatric bipolar disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 308–319. doi:10.1097/CHI.0b013e3181948fc7Google Scholar
Peterson, B. S., Wang, Z., Horga, G., Warner, V., Rutherford, B., Klahr, K. W., … Weissman, M. M. (2014). Discriminating risk and resilience endophenotypes from lifetime illness effects in familial major depressive disorder. JAMA Psychiatry, 71, 136–148. doi:10.1001/jamapsychiatry.2013.4048Google Scholar
Phillips, M. L., & Swartz, H. A. (2014). A critical appraisal of neuroimaging studies of bipolar disorder: Toward a new conceptualization of underlying neural circuitry and a road map for future research. American Journal of Psychiatry, 171, 829–843. doi:10.1176/appi.ajp.2014.13081008Google Scholar
Phillips, O. R., Onopa, A. K., Hsu, V., Ollila, H. M., Hillary, R. P., Hallmayer, J., … Singh, M. K. (2018). Beyond a binary classification of sex: An examination of brain sex differentiation, psychopathology, and genotype. Journal of the American Academy of Child & Adolescent Psychiatry. Advance online publication. doi:10.1016/j.jaac.2018.09.425Google Scholar
Platt, B., Waters, A. M., Schulte-Koerne, G., Engelmann, L., & Salemink, E. (2017). A review of cognitive biases in youth depression: Attention, interpretation and memory. Cognition and Emotion, 31. doi:10.1080/02699931.2015.1127215Google Scholar
Poznanski, E. O., Grossman, J. A., Buchsbaum, Y., Banegas, M., Freeman, L., & Gibbons, R. (1984). Preliminary studies of the reliability and validity of the children's depression rating scale. Journal of the American Academy of Child Psychiatry, 23, 191–197.Google Scholar
Raouna, A., Osam, C. S., & MacBeth, A. (2018). Clinical staging model in offspring of parents with bipolar disorder: A systematic review. Bipolar Disorders, 20, 313–333. doi:10.1111/bdi.12604Google Scholar
Rich, B. A., Fromm, S. J., Berghorst, L. H., Dickstein, D. P., Brotman, M. A., Pine, D. S., & Leibenluft, E. (2008). Neural connectivity in children with bipolar disorder: Impairment in the face emotion processing circuit. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 49, 88–96. doi:10.1111/j.1469-7610.2007.01819.xGoogle Scholar
Roberts, G., Green, M. J., Breakspear, M., McCormack, C., Frankland, A., Wright, A., … Mitchell, P. B. (2013). Reduced inferior frontal gyrus activation during response inhibition to emotional stimuli in youth at high risk of bipolar disorder. Biological Psychiatry, 74, 55–61. doi:10.1016/J.BIOPSYCH.2012.11.004Google Scholar
Roberts, G., Lord, A., Frankland, A., Wright, A., Lau, P., Levy, F., … Breakspear, M. (2017). Functional dysconnection of the inferior frontal gyrus in young people with bipolar disorder or at genetic high risk. Biological Psychiatry, 81, 718–727. doi:10.1016/J.BIOPSYCH.2016.08.018Google Scholar
Shaffer, D., Gould, M. S., Brasic, J., Ambrosini, P., Fisher, P., Bird, H., & Aluwahlia, S. (1983). A Children's Global Assessment Scale (CGAS). Archives of General Psychiatry, 40, 1228–1231.Google Scholar
Sharma, A. N., Barron, E., Le Couteur, J., Close, A., Rushton, S., Grunze, H., … Le Couteur, A. S. (2017). Facial emotion labeling in unaffected offspring of adults with bipolar I disorder. Journal of Affective Disorders, 208, 198–204. doi:10.1016/J.JAD.2016.10.006Google Scholar
Silk, J. S., Vanderbilt-Adriance, E., Shaw, D. S., Forbes, E. E., Whalen, D. J., Ryan, N. D., & Dahl, R. E. (2007). Resilience among children and adolescents at risk for depression: Mediation and moderation across social and neurobiological contexts. Development and Psychopathology, 19, 841–865. doi:10.1017/S0954579407000417Google Scholar
Singh, M. K., Chang, K. D., Kelley, R. G., Saggar, M., Reiss, A. L., & Gotlib, I. H. (2014). Early signs of anomalous neural functional connectivity in healthy offspring of parents with bipolar disorder. Bipolar Disorders, 16, 678–689. doi:10.1111/bdi.12221Google Scholar
Singh, M. K., DelBello, M. P., Soutullo, C., Stanford, K. E., McDonough-Ryan, P., & Strakowski, S. M. (2007). Obstetrical complications in children at high risk for bipolar disorder. Journal of Psychiatric Research, 41, 680–685. doi:10.1016/J.JPSYCHIRES.2006.02.009Google Scholar
Singh, M. K., DelBello, M. P., Stanford, K. E., Soutullo, C., McDonough-Ryan, P., McElroy, S. L., & Strakowski, S. M. (2007). Psychopathology in children of bipolar parents. Journal of Affective Disorders, 102, 131–136. doi:10.1016/J.JAD.2007.01.004Google Scholar
Singh, M. K., Kelley, R. G., Howe, M. E., Reiss, A. L., Gotlib, I. H., & Chang, K. D. (2014). Reward processing in healthy offspring of parents with bipolar disorder. JAMA Psychiatry, 71, 1148. doi:10.1001/jamapsychiatry.2014.1031Google Scholar
Solé-Padullés, C., Castro-Fornieles, J., de la Serna, E., Calvo, R., Baeza, I., Moya, J., … Sugranyes, G. (2016). Intrinsic connectivity networks from childhood to late adolescence: Effects of age and sex. Developmental Cognitive Neuroscience, 17, 35–44. doi:10.1016/J.DCN.2015.11.004Google Scholar
Swales, D. A., Winiarski, D. A., Smith, A. K., Stowe, Z. N., Newport, D. J., & Brennan, P. A. (2018). Maternal depression and cortisol in pregnancy predict offspring emotional reactivity in the preschool period. Developmental Psychobiology, 60, 557–566. doi:10.1002/dev.21631Google Scholar
Townsend, J., & Altshuler, L. L. (2012). Emotion processing and regulation in bipolar disorder: A review. Bipolar Disorders, 14, 326–339. doi:10.1111/j.1399-5618.2012.01021.xGoogle Scholar
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_42Google Scholar
Wackerhagen, C., Wüstenberg, T., Mohnke, S., Erk, S., Veer, I. M., Kruschwitz, J. D., … Romanczuk-Seiferth, N. (2017). Influence of familial risk for depression on cortico-limbic connectivity during implicit emotional processing. Neuropsychopharmacology, 42, 1729–1738. doi:10.1038/npp.2017.59Google Scholar
Wang, C., Shen, M., Guillaume, B., Chong, Y.-S., Chen, H., Fortier, M. V, … Qiu, A. (2018). FKBP5 moderates the association between antenatal maternal depressive symptoms and neonatal brain morphology. Neuropsychopharmacology, 43, 564–570. doi:10.1038/npp.2017.232Google Scholar
Weschler. (1999). Weschler Abbreviated Scale of Intelligence (WASI). San Antonio, TX: Pearson.Google Scholar
Whalley, H. C., Sussmann, J. E., Romaniuk, L., Stewart, T., Kielty, S., Lawrie, S. M., … McIntosh, A. M. (2015). Dysfunction of emotional brain systems in individuals at high risk of mood disorder with depression and predictive features prior to illness. Psychological Medicine, 45, 1207–1218. doi:10.1017/S0033291714002256Google Scholar
Wiggins, J. L., Brotman, M. A., Adleman, N. E., Kim, P., Wambach, C. G., Reynolds, R. C., … Leibenluft, E. (2017). Neural markers in pediatric bipolar disorder and familial risk for bipolar disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 56, 67–78. doi:10.1016/j.jaac.2016.10.009Google Scholar
Wiggins, J. L., Mitchell, C., Hyde, L. W., & Monk, C. S. (2015). Identifying early pathways of risk and resilience: The codevelopment of internalizing and externalizing symptoms and the role of harsh parenting. Development and Psychopathology, 27(4, Pt 1), 1295–1312. doi:10.1017/S0954579414001412Google Scholar
Williams, J. B. W., Gibbon, M., First, M. B., Spitzer, R. L., Davies, M., Borus, J., … Wittchen, H.-U. (1992). The Structured Clinical Interview for DSM-III-R (SCID). Archives of General Psychiatry, 49, 630. doi:10.1001/archpsyc.1992.01820080038006Google Scholar
Worsley, K. J. (2001). Statistical analysis of activation images. In Jezzard, P., Matthews, P. M., & Smith, S. M. (Eds.), Functional MRI: An introduction to methods. Oxford: Oxford University Press.Google Scholar
Young, R. C., Biggs, J. T., Ziegler, V. E., & Meyer, D. A. (1978). A rating scale for mania: Reliability, validity and sensitivity. British Journal of Psychiatry, 133, 429–435.Google Scholar
Zhu, X., Wang, X., Xiao, J., Liao, J., Zhong, M., Wang, W., & Yao, S. (2012). Evidence of a dissociation pattern in resting-state default mode network connectivity in first-episode, treatment-naive major depression patients. Biological Psychiatry, 71, 611–617. doi:10.1016/j.biopsych.2011.10.035Google Scholar