Skip to main content Accessibility help
×
Home

Violence exposure and neural systems underlying working memory for emotional stimuli in youth

  • Jessica L. Jenness (a1), Maya L. Rosen (a1), Kelly A. Sambrook (a1), Meg J. Dennison (a2), Hilary K. Lambert (a1), Margaret A. Sheridan (a3) and Katie A. McLaughlin (a1)...

Abstract

Violence exposure during childhood is common and associated with poor cognitive and academic functioning. However, little is known about how violence exposure influences cognitive processes that might contribute to these disparities, such as working memory, or their neural underpinnings, particularly for cognitive processes that occur in emotionally salient contexts. We address this gap in a sample of 54 participants aged 8 to 19 years (50% female), half with exposure to interpersonal violence. Participants completed a delayed match to sample task for emotional faces while undergoing functional magnetic resonance imaging scanning. Violence-exposed youth performed worse than controls on happy and neutral, but not angry, trials. In whole-brain analysis, violence-exposed youth had reduced activation in the left middle frontal gyrus and right intraparietal sulcus during encoding and the left superior temporal sulcus and temporal–parietal junction during retrieval compared to control youth. Reduced activation in the left middle frontal gyrus during encoding and the left superior temporal sulcus during retrieval mediated the association between violence exposure and task performance. Violence exposure influences the frontoparietal network that supports working memory as well as regions involved in facial processing during working memory for emotional stimuli. Reduced neural recruitment in these regions may explain atypical patterns of cognitive processing seen among violence-exposed youth, particularly within emotional contexts.

Copyright

Corresponding author

Address correspondence and reprint requests to: Katie McLaughlin, Department of Psychology, University of Washington, Box 351525, Seattle, WA 98195; E-mail: mclaughk@uw.edu.

Footnotes

Hide All

This research was supported by National Institute of Child Health and Human Development Grant T32-HD057822 and National Institute of Mental Health Grants K01-MH092526, R01-MH103291, and R01-MH106482.

Footnotes

References

Hide All
Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5). Washington, DC: Author.
Askren, M. K., McAllister-Day, T. K., Koh, N., Mestre, Z., Dines, J. N., Korman, B. A., … Madhyastha, T. M. (2016). Using make for reproducible and parallel neuroimaging workflow and quality-assurance. Frontiers in Neuroinformatics. Advance online publication.
Augusti, E.-M., & Melinder, A. (2013). Maltreatment is associated with specific impairments in executive functions: A pilot study: Executive functions in maltreated children. Journal of Traumatic Stress, 26, 780783. doi:10.1002/jts.21860
Avants, B. B., Tustison, N. J., Song, G., Cook, P. A., Klein, A., & Gee, J. C. (2011). A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage, 54, 20332044.
Barrett, L. F., Tugade, M. M., & Engle, R. W. (2004). Individual differences in working memory capacity and dual-process theories of the mind. Psychological Bulletin, 130, 553.
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37, 90101.
Bernstein, D. P., Ahluvalia, T., Pogge, D., & Handelsman, L. (1997). Validity of the Childhood Trauma Questionnaire in an adolescent psychiatric population. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 340348.
Bifulco, A., Brown, G. W., Lillie, A., & Jarvis, J. (1997). Memories of childhood neglect and abuse: Corroboration in a series of sisters. Journal of Child Psychology and Psychiatry, 38, 365374.
Braunlich, K., Gomez-Lavin, J., & Seger, C. A. (2015). Frontoparietal networks involved in categorization and item working memory. NeuroImage, 107, 146162.
Cicchetti, D., Rogosch, F. A., Maughan, A., Toth, S. L., & Bruce, J. (2003). False belief understanding in maltreated children. Development and Psychopathology, 15, 10671091.
Cromheeke, S., Herpoel, L.-A., & Mueller, S. C. (2014). Childhood abuse is related to working memory impairment for positive emotion in female university students. Child Maltreatment, 19, 3848. doi:10.1177/1077559513511522
Curtis, C. E., & D'Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences, 7, 415423.
Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage, 9, 179194.
Deen, B., Koldewyn, K., Kanwisher, N., & Saxe, R. (2015). Functional organization of social perception and cognition in the superior temporal sulcus. Cerebral Cortex, 25, 45964609.
Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15, 331. doi:10.1017/S1355617709090481
DePrince, A. P., Weinzierl, K. M., & Combs, M. D. (2009). Executive function performance and trauma exposure in a community sample of children. Child Abuse and Neglect, 33, 353361.
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences. Advance online publication.
Finkelhor, D., Ormrod, R. K., & Turner, H. A. (2009). The developmental epidemiology of childhood victimization. Journal of Interpersonal Violence, 24, 711731.
Finn, A. S., Minas, J. E., Leonard, J. A., Mackey, A. P., Salvatore, J., Goetz, C., … Gabrieli, J. D. (2016). Functional brain organization of working memory in adolescents varies in relation to family income and academic achievement. Developmental Science. Advance online publication. doi:10.1111/desc.12450/full
Geier, C. F., Garver, K., Terwilliger, R., & Luna, B. (2009). Development of working memory maintenance. Journal of Neurophysiology, 101, 8499.
Ghosh, S. S., Kakunoori, S., Augustinack, J., Nieto-Castanon, A., Kovelman, I., Gaab, N., … Fischl, B. (2010). Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11 years of age. NeuroImage, 53, 8593.
Gold, A. L., Sheridan, M. A., Peverill, M., Busso, D. S., Lambert, H. K., Alves, S., … McLaughlin, K. A. (2016). Childhood abuse and reduced cortical thickness in brain regions involved in emotional processing. Journal of Child Psychology and Psychiatry, 57, 11541164.
Gould, F., Clarke, J., Heim, C., Harvey, P. D., Majer, M., & Nemeroff, C. B. (2012). The effects of child abuse and neglect on cognitive functioning in adulthood. Journal of Psychiatric Research, 46, 500506.
Hanson, J. L., Chung, M. K., Avants, B. B., Shirtcliff, E. A., Gee, J. C., Davidson, R. J., & Pollak, S. D. (2010). Early stress is associated with alterations in the orbitofrontal cortex: A tensor-based morphometry investigation of brain structure and behavioral risk. Journal of Neuroscience, 30, 74667472.
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223233.
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2002). Human neural systems for face recognition and social communication. Biological Psychiatry, 51, 5967.
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.
Hein, G., & Knight, R. T. (2008). Superior temporal sulcus—It's my area: Or is it? Journal of Cognitive Neuroscience, 20, 21252136.
Holt, M. K., Finkelhor, D., & Kantor, G. K. (2007). Multiple victimization experiences of urban elementary school students: Associations with psychosocial functioning and academic performance. Child Abuse and Neglect, 31, 503515.
Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S. M. (2012). NeuroImage, 62, 782790.
Lambert, H. K., Sheridan, M. A., Sambrook, K. A., Rosen, M. L., Askren, M. K., & McLaughlin, K. A. (2017). Hippocampal contribution to context encoding across development is disrupted following early-life adversity. Journal of Neuroscience, 37, 19251934.
Lipina, S., Segretin, S., Hermida, J., Prats, L., Fracchia, C., Camelo, J. L., & Colombo, J. (2013). Linking childhood poverty and cognition: Environmental mediators of non-verbal executive control in an Argentine sample. Developmental Science, 16, 697707.
LoPresti, M. L., Schon, K., Tricarico, M. D., Swisher, J. D., Celone, K. A., & Stern, C. E. (2008). Working memory for social cues recruits orbitofrontal cortex and amygdala: A functional magnetic resonance imaging study of delayed matching to sample for emotional expressions. Journal of Neuroscience, 28, 37183728.
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the life span on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434445.
Mackey, A. P., Finn, A. S., Leonard, J. A., Jacoby-Senghor, D. S., West, M. R., Gabrieli, C. F., & Gabrieli, J. D. (2015). Neuroanatomical correlates of the income-achievement gap. Psychological Science, 26, 925933.
Marcus, D. S., Harms, M. P., Snyder, A. Z., Jenkinson, M., Wilson, J. A., Glasser, M. F., … others. (2013). Human Connectome Project informatics: Quality control, database services, and data visualization. NeuroImage, 80, 202219.
Marusak, H. A., Zundel, C. G., Brown, S., Rabinak, C. A., & Thomason, M. E. (2016). Convergent behavioral and corticolimbic connectivity evidence of a negativity bias in children and adolescents. Social Cognitive and Affective Neuroscience. Advance online publication.
McLaughlin, K. A. (2016). Future directions in childhood adversity and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 45, 361382.
McLaughlin, K. A., Busso, D. S., Duys, A., Green, J. G., Alves, S., Way, M., & Sheridan, M. A. (2014). Amygdala response to negative stimuli predicts PTSD symptom onset following a terrorist attack. Depression and Anxiety, 31, 834842. doi:10.1002/da.22284
McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2012). Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Archives of General Psychiatry, 69, 11511160.
McLaughlin, K. A., Koenen, K. C., Hill, E. D., Petukhova, M., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2013). Trauma exposure and posttraumatic stress disorder in a national sample of adolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 52, 815830.
McLaughlin, K. A., & Lambert, H. K. (2016). Child trauma exposure and psychopathology: Mechanisms of risk and resilience. Current Opinion in Psychology, 14, 2934.
McLaughlin, K. A., Peverill, M., Gold, A. L., Alves, S., & Sheridan, M. A. (2015). Child maltreatment and neural systems underlying emotion regulation. Journal of the American Academy of Child & Adolescent Psychiatry, 54, 753762.
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience & Biobehavioral Reviews, 47, 578591.
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.
Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110, 40.
Miyake, A., & Friedman, N. P. (2012). The nature and organization of individual differences in executive functions four general conclusions. Current Directions in Psychological Science, 21, 814.
Noble, K. G., Houston, S. M., Brito, N. H., Bartsch, H., Kan, E., Kuperman, J. M., … Sowell, E. R. (2015). Family income, parental education and brain structure in children and adolescents. Nature Neuroscience, 18, 773778.
Nolte, T., Bolling, D. Z., Hudac, C. M., Fonagy, P., Mayes, L., & Pelphrey, K. A. (2013). Brain mechanisms underlying the impact of attachment-related stress on social cognition. Frontiers in Human Neuroscience, 7. doi:10.3389/fnhum.2013.00816
Pollak, S. D., Cicchetti, D., Hornung, K., & Reed, A. (2000). Recognizing emotion in faces: Developmental effects of child abuse and neglect. Developmental Psychology, 36, 679688. doi:10.1037/0012-1649.36.5.679
Pollak, S. D., & Tolley-Schell, S. A. (2003). Selective attention to facial emotion in physically abused children. Journal of Abnormal Psychology, 112, 323.
Raschle, N., Zuk, J., Ortiz-Mantilla, S., Sliva, D. D., Franceschi, A., Grant, P. E., … Gaab, N. (2012). Pediatric neuroimaging in early childhood and infancy: Challenges and practical guidelines. Annals of the New York Academy of Sciences, 1252, 4350.
Roche, A. (2011). A four-dimensional registration algorithm with application to joint correction of motion and slice timing in fMRI. IEEE Transactions on Medical Imaging, 30, 15461554.
Sarsour, K., Sheridan, M., Jutte, D., Nuru-Jeter, A., Hinshaw, S., & Boyce, W. T. (2011). Family socioeconomic status and child executive functions: The roles of language, home environment, and single parenthood. Journal of the International Neuropsychological Society, 17, 120132.
Scherf, K. S., Sweeney, J. A., & Luna, B. (2006). Brain basis of developmental change in visuospatial working memory. Journal of Cognitive Neuroscience, 18, 10451058. doi:10.1162/jocn.2006.18.7.1045
Shackman, J. E., Shackman, A. J., & Pollak, S. D. (2007). Physical abuse amplifies attention to threat and increases anxiety in children. Emotion, 7, 838.
Sheridan, M. A., & McLaughlin, K. A. (2014). Dimensions of early experience and neural development: Deprivation and threat. Trends in Cognitive Sciences, 18, 580585.
Sheridan, M. A., Peverill, M. A., Finn, A. S., & McLaughlin, K. A. (2017). Dimensions of childhood adversity have distinct associations with neural systems underlying executive functioning. Development and Psychopathology. Advance online publication.
Shonk, S. M., & Cicchetti, D. (2001). Maltreatment, competency deficits, and risk for academic and behavioral maladjustment. Developmental Psychology, 37, 3.
Soto, D., Rotshtein, P., & Kanai, R. (2014). Parietal structure and function explain human variation in working memory biases of visual attention. NeuroImage, 89, 289296.
Steinberg, A. M., Brymer, M. J., Decker, K. B., & Pynoos, R. S. (2004). The University of California at Los Angeles Post-Traumatic Stress Disorder Reaction Index. Current Psychiatry Reports, 6, 96100.
Swartz, J. R., Graham-Bermann, S. A., Mogg, K., Bradley, B. P., & Monk, C. S. (2011). Attention bias to emotional faces in young children exposed to intimate partner violence. Journal of Child and Adolescent Trauma, 4, 109122. doi:10.1080/19361521.2011.573525
Thomas, K. M., Drevets, W. C., Whalen, P. J., Eccard, C. H., Dahl, R. E., Ryan, N. D., & Casey, B. J. (2001). Amygdala response to facial expressions in children and adults. Biological Psychiatry, 49, 309316.
Tibu, F., Sheridan, M. A., McLaughlin, K. A., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2016). Disruptions of working memory and inhibition mediate the association between exposure to institutionalization and symptoms of attention deficit hyperactivity disorder. Psychological Medicine, 46, 529541.
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242249.
Twamley, E. W., Hami, S., & Stein, M. B. (2004). Neuropsychological function in college students with and without posttraumatic stress disorder. Psychiatry Research, 126, 265274. doi:10.1016/j.psychres.2004.01.008
Vasilevski, V., & Tucker, A. (2016). Wide-ranging cognitive deficits in adolescents following early life maltreatment. Neuropsychology, 30, 239246. doi:10.1037/neu0000215
Vul, E., Harris, C., Winkielman, P., & Pashler, H. (2009). Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspectives on Psychological Science, 4, 274290.
Walker, E. A., Unutzer, J., Rutter, C., Gelfand, A., Saunders, K., VonKorff, M., … Katon, W. (1999). Costs of health care use by women HMO members with a history of childhood abuse and neglect. Archives of General Psychiatry, 56, 609613.
Woolrich, M. (2008). Robust group analysis using outlier inference. NeuroImage, 41, 286301.
Type Description Title
WORD
Supplementary materials

Jenness et al supplementary material
Jenness et al supplementary material 1

 Word (24 KB)
24 KB
UNKNOWN
Supplementary materials

Jenness et al supplementary material
Jenness et al supplementary material 2

 Unknown (132 KB)
132 KB
WORD
Supplementary materials

Jenness et al supplementary material
Jenness et al supplementary material 3

 Word (21 KB)
21 KB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed