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Neurobehavioral correlates of impaired emotion recognition in pediatric PTSD

Published online by Cambridge University Press:  25 January 2021

Sara A. Heyn*
Affiliation:
Neuroscience and Public Policy Program, University of Wisconsin-Madison, Madison, WI, USA Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
Collin Schmit
Affiliation:
Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA
Taylor J. Keding
Affiliation:
Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
Richard Wolf
Affiliation:
Neuroscience Training Program, University of Wisconsin-Madison, Madison, WI, USA
Ryan J. Herringa
Affiliation:
Department of Psychiatry, University of Wisconsin-Madison School of Medicine and Public Health, Madison, WI, USA
*
Author for Correspondence: Sara Heyn, Department of Psychiatry, University of Wisconsin-Madison, 6001 Research Park Blvd. Rm 1329, Madison, WI53719; E-mail: [email protected]

Abstract

Despite broad evidence suggesting that adversity-exposed youth experience an impaired ability to recognize emotion in others, the underlying biological mechanisms remains elusive. This study uses a multimethod approach to target the neurological substrates of this phenomenon in a well-phenotyped sample of youth meeting diagnostic criteria for posttraumatic stress disorder (PTSD). Twenty-one PTSD-afflicted youth and 23 typically developing (TD) controls completed clinical interview schedules, an emotion recognition task with eye-tracking, and an implicit emotion processing task during functional magnetic resonance imaging )fMRI). PTSD was associated with decreased accuracy in identification of angry, disgust, and neutral faces as compared to TD youth. Of note, these impairments occurred despite the normal deployment of visual attention in youth with PTSD relative to TD youth. Correlation with a related fMRI task revealed a group by accuracy interaction for amygdala–hippocampus functional connectivity (FC) for angry expressions, where TD youth showed a positive relationship between anger accuracy and amygdala–hippocampus FC; this relationship was reversed in youth with PTSD. These findings are a novel characterization of impaired threat recognition within a well-phenotyped population of severe pediatric PTSD. Further, the differential amygdala–hippocampus FC identified in youth with PTSD may imply aberrant efficiency of emotional contextualization circuits.

Type
Regular Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Abhang, P. A., Gawali, B. W., & Mehrotra, S. C. (2016). Chapter 5 – Emotion recognition. In Abhang, P. A., Gawali, B. W. & Mehrotra, S. C. (Eds.), Introduction to EEG- and speech-based emotion recognition (pp. 97112). Academic Press. doi:10.1016/B978-0-12-804490-2.00005-1CrossRefGoogle Scholar
Aboyoun, D. C., & Dabbs, J. M. (1998). The Hess pupil dilation findings: Sex or novelty? Social Behavior and Personality: An International Journal, 26, 415419. doi:10.2224/sbp.1998.26.4.415CrossRefGoogle Scholar
Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12, 169177. doi:10.1016/S0959-4388(02)00301-XCrossRefGoogle ScholarPubMed
Adolphs, R., Gosselin, F., Buchanan, T. W., Tranel, D., Schyns, P., & Damasio, A. R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 68. doi:10.1038/nature03086CrossRefGoogle ScholarPubMed
Adolphs, R., Tranel, D., & Damasio, H. (2001). Emotion recognition from faces and prosody following temporal lobectomy. Neuropsychology, 15, 396404. doi:10.1037/0894-4105.15.3.396CrossRefGoogle ScholarPubMed
Adolphs, R., Tranel, D., Hamann, S., Young, A. W., Calder, A. J., Phelps, E. A., … Damasio, A. R. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37, 11111117. doi:10.1016/S0028-3932(99)00039-1CrossRefGoogle ScholarPubMed
Anderson, M., & Miller, K. L. (1998). Modularity, mental retardation and speed of processing. Developmental Science, 1, 239245. doi:10.1111/1467-7687.00037CrossRefGoogle Scholar
Anderson, A. K., Spencer, D. D., Fulbright, R. K., & Phelps, E. A. (2000). Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology, 14, 526536. doi:10.1037/0894-4105.14.4.526CrossRefGoogle Scholar
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289300. doi:10.2307/2346101CrossRefGoogle Scholar
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. (1997). The screen for child anxiety related emotional disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 545553. doi:10.1097/00004583-199704000-00018CrossRefGoogle ScholarPubMed
Black, M. H., Chen, N. T. M., Iyer, K. K., Lipp, O. V., Bölte, S., Falkmer, M., … Girdler, S. (2017). Mechanisms of facial emotion recognition in autism spectrum disorders: Insights from eye tracking and electroencephalography. Neuroscience & Biobehavioral Reviews, 80, 488515. doi:10.1016/j.neubiorev.2017.06.016CrossRefGoogle ScholarPubMed
Blechert, J., Michael, T., Vriends, N., Margraf, J., & Wilhelm, F. H. (2007). Fear conditioning in posttraumatic stress disorder: Evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behaviour Research and Therapy, 45, 20192033. doi:10.1016/j.brat.2007.02.012CrossRefGoogle ScholarPubMed
Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45, 602607. doi:10.1111/j.1469-8986.2008.00654.xCrossRefGoogle ScholarPubMed
Brady, K. T. (1997). Posttraumatic stress disorder and comorbidity: Recognizing the many faces of PTSD. The Journal of Clinical Psychiatry, 58, 1215.Google ScholarPubMed
Broks, P., Young, A. W., Maratos, E. J., Coffey, P. J., Calder, A. J., Isaac, C. L., … Hadley, D. (1998). Face processing impairments after encephalitis: Amygdala damage and recognition of fear. Neuropsychologia, 36, 5970. doi:10.1016/S0028-3932(97)00105-XCrossRefGoogle Scholar
Calder, A. J. (1996). Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear. Cognitive Neuropsychology, 13, 699745. doi:10.1080/026432996381890CrossRefGoogle Scholar
Calder, A. J., Lawrence, A. D., & Young, A. W. (2001). Neuropsychology of fear and loathing. Nature Reviews Neuroscience, 2, 352. doi:10.1038/35072584CrossRefGoogle ScholarPubMed
Cisler, J. M., Scott Steele, J., Smitherman, S., Lenow, J. K., & Kilts, C. D. (2013). Neural processing correlates of assaultive violence exposure and PTSD symptoms during implicit threat processing: A network-level analysis among adolescent girls. Psychiatry Research, 214, 238246. doi:10.1016/j.pscychresns.2013.06.003CrossRefGoogle ScholarPubMed
Costello, E. J., & Angold, A. (1988). Scales to assess child and adolescent depression: Checklists, screens, and nets. Journal of the American Academy of Child and Adolescent Psychiatry, 27, 726737. doi:10.1097/00004583-198811000-00011CrossRefGoogle ScholarPubMed
da Silva Ferreira, G. C., Crippa, J. A. S., & de Lima Osório, F. (2014). Facial emotion processing and recognition among maltreated children: A systematic literature review. Frontiers in Psychology, 5. doi:10.3389/fpsyg.2014.01460CrossRefGoogle ScholarPubMed
Demers, L. A., McKenzie, K. J., Hunt, R. H., Cicchetti, D., Cowell, R. A., Rogosch, F. A., … Thomas, K. M. (2018). Separable effects of childhood maltreatment and adult adaptive functioning on amygdala connectivity during emotion processing. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3, 116124. doi:10.1016/j.bpsc.2017.08.010Google ScholarPubMed
de Voogd, L. D., Fernández, G., & Hermans, E. J. (2016). Awake reactivation of emotional memory traces through hippocampal–neocortical interactions. NeuroImage, 134, 563572. doi:10.1016/j.neuroimage.2016.04.026CrossRefGoogle ScholarPubMed
Donnelly, C. L., & Amaya-Jackson, L. (2002). Post-traumatic stress disorder in children and adolescents: Epidemiology. Diagnosis and Treatment Options. Pediatric Drugs, 4, 159170. doi:10.2165/00148581-200204030-00003Google ScholarPubMed
Ehlers, A., Suendermann, O., Boellinghaus, I., Vossbeck-Elsebusch, A., Gamer, M., Briddon, E., … Glucksman, E. (2010). Heart rate responses to standardized trauma-related pictures in acute posttraumatic stress disorder. International Journal of Psychophysiology, 78, 2734. doi:10.1016/j.ijpsycho.2010.04.009CrossRefGoogle ScholarPubMed
Eisenbarth, H., & Alpers, G. W. (2011). Happy mouth and sad eyes: Scanning emotional facial expressions. Emotion, 11, 860865. https://doi.org/10.1037/a0022758CrossRefGoogle ScholarPubMed
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry, 164, 14761488. doi:10.1176/appi.ajp.2007.07030504CrossRefGoogle ScholarPubMed
Famularo, R., Fenton, T., Kinscherff, R., & Augustyn, M. (1996). Psychiatric comorbidity in childhood post traumatic stress disorder. Child Abuse & Neglect, 20, 953961.CrossRefGoogle ScholarPubMed
Garrett, A. S., Carrion, V., Kletter, H., Karchemskiy, A., Weems, C. F., & Reiss, A. (2012). Brain activation to facial expressions in youth with PTSD symptoms. Depression and Anxiety, 29, 449459. doi:10.1002/da.21892CrossRefGoogle ScholarPubMed
Harms, M. B., Martin, A., & Wallace, G. L. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review, 20, 290322. doi:10.1007/s11065-010-9138-6CrossRefGoogle ScholarPubMed
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4, 223233. doi:10.1016/S1364-6613(00)01482-0CrossRefGoogle ScholarPubMed
Hayes, J. P., Hayes, S. M., & Mikedis, A. M. (2012). Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biology of Mood & Anxiety Disorders, 2, 9. doi:10.1186/2045-5380-2-9CrossRefGoogle ScholarPubMed
Hein, T. C., & Monk, C. S. (2017). Research review: Neural response to threat in children, adolescents, and adults after child maltreatment – a quantitative meta-analysis. Journal of Child Psychology and Psychiatry, 58, 222230. doi:10.1111/jcpp.12651CrossRefGoogle ScholarPubMed
Henigsberg, N., Kalember, P., Petrović, Z. K., & Šečić, A. (2019). Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 90, 3742. doi:10.1016/j.pnpbp.2018.11.003CrossRefGoogle ScholarPubMed
Herba, C., & Phillips, M. (2004). Annotation: Development of facial expression recognition from childhood to adolescence: Behavioural and neurological perspectives. Journal of Child Psychology and Psychiatry, 45, 11851198. doi:10.1111/j.1469-7610.2004.00316.xCrossRefGoogle ScholarPubMed
Hermans, E. J., Kanen, J. W., Tambini, A., Fernández, G., Davachi, L., & Phelps, E. A. (2017). Persistence of amygdala–hippocampal connectivity and multi-voxel correlation structures during awake rest after fear learning predicts long-term expression of fear. Cerebral Cortex (New York, N.Y.: 1991), 27, 30283041. doi:10.1093/cercor/bhw145Google Scholar
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008). Switching on and off fear by distinct neuronal circuits. Nature, 454, 600606. doi:10.1038/nature07166CrossRefGoogle ScholarPubMed
Hess, E. H., & Polt, J. M. (1960). Pupil size as related to interest value of visual stimuli. Science, 132, 349350. doi:10.1126/science.132.3423.349CrossRefGoogle ScholarPubMed
Heyn, S. A., Keding, T. J., Ross, M. C., Cisler, J. M., Mumford, J. A., & Herringa, R. J. (2019). Abnormal prefrontal development in pediatric posttraumatic stress disorder: A longitudinal structural and functional magnetic resonance imaging study. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4, 171179. doi:10.1016/j.bpsc.2018.07.013Google ScholarPubMed
Iffland, B., & Neuner, F. (2020). Varying cognitive scars – differential associations between types of childhood maltreatment and facial emotion processing. Frontiers in Psychology, 11. doi:10.3389/fpsyg.2020.00732CrossRefGoogle ScholarPubMed
Izard, C., Fine, S., Schultz, D., Mostow, A., Ackerman, B., & Youngstrom, E. (2001). Emotion knowledge as a predictor of social behavior and academic competence in children at risk. Psychological Science, 12, 1823. doi:10.1111/1467-9280.00304CrossRefGoogle ScholarPubMed
Javdani, S., Sadeh, N., Donenberg, G. R., Emerson, E. M., Houck, C., & Brown, L. K. (2017). Affect recognition among adolescents in therapeutic schools: Relationships with posttraumatic stress disorder and conduct disorder symptoms. Child and Adolescent Mental Health, 22, 4248. doi:10.1111/camh.12198CrossRefGoogle ScholarPubMed
Jones, C. R. G., Pickles, A., Falcaro, M., Marsden, A. J. S., Happé, F., Scott, S. K., … Charman, T. (2011). A multimodal approach to emotion recognition ability in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 52, 275285. doi:10.1111/j.1469-7610.2010.02328.xCrossRefGoogle ScholarPubMed
Kaiser, D., Jacob, G. A., van Zutphen, L., Siep, N., Sprenger, A., Tuschen-Caffier, B., … Domes, G. (2019). Biased attention to facial expressions of ambiguous emotions in borderline personality disorder: An eye-tracking study. Journal of Personality Disorders, 128. doi:10.1521/pedi_2019_33_363Google Scholar
Karsh, R. B., & Breitenbach, F. W.. (1983). Looking at looking: The amorphous fixation measure (pp. 5364). Hillsdale, NJ: Erlbaum.Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., … Ryan, N. (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 and Adolescent Psychiatry, 36, 980988. doi:10.1097/00004583-199707000-00021CrossRefGoogle ScholarPubMed
Keding, T. J., & Herringa, R. J. (2015). Abnormal structure of fear circuitry in pediatric post-traumatic stress disorder. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 40, 537545. doi:10.1038/npp.2014.239CrossRefGoogle ScholarPubMed
Keding, T. J., & Herringa, R. J. (2016). Paradoxical prefrontal-amygdala recruitment to angry and happy expressions in pediatric posttraumatic stress disorder. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 41, 29032912. doi:10.1038/npp.2016.104CrossRefGoogle ScholarPubMed
Kessler, R. C., Sonnega, A., Bromet, E., Hughes, M., & Nelson, C. B. (1995). Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry, 52, 10481060.CrossRefGoogle ScholarPubMed
Lakshman, M., Murphy, L., Mekawi, Y., Carter, S., Briscione, M., Bradley, B., … Powers, A. (2020). Attention bias towards threat in African American children exposed to early life trauma. Behavioural Brain Research, 383, 112513. doi:10.1016/j.bbr.2020.112513CrossRefGoogle ScholarPubMed
Lamberg, L. (2001). Psychiatrists explore legacy of traumatic stress in early life. JAMA, 286, 523526. doi:10.1001/jama.286.5.523-JMN0801-2-1CrossRefGoogle ScholarPubMed
Lambert, R. H., Monty, R. A., & Hall, R. J. (1974). High-speed data processing and unobtrusive monitoring of eye movements. Behavior Research Methods & Instrumentation, 6, 525530. doi:10.3758/BF03201340CrossRefGoogle Scholar
Libby, W. L., Lacey, B. C., & Lacey, J. I. (1973). Pupillary and cardiac activity during visual attention. Psychophysiology, 10, 270294. doi:10.1111/j.1469-8986.1973.tb00526.xCrossRefGoogle ScholarPubMed
Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska Directed Emotional Faces—KDEF [CD ROM]. Stockholm, Sweden: Department of Clinical Neuroscience, Psychology section, Karolinska Institutet.Google Scholar
Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291303.CrossRefGoogle ScholarPubMed
Marshall, W. A., & Tanner, J. M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 1323. doi:10.1136/adc.45.239.13CrossRefGoogle ScholarPubMed
Masten, C. L., Guyer, A. E., Hodgdon, H. B., McClure, E. B., Charney, D. S., Ernst, M., … Monk, C. S. (2008). Recognition of facial emotions among maltreated children with high rates of post-traumatic stress disorder. Child Abuse & Neglect, 32, 139153. doi:10.1016/j.chiabu.2007.09.006CrossRefGoogle ScholarPubMed
Mattavelli, G., Sormaz, M., Flack, T., Asghar, A. U. R., Fan, S., Frey, J., … Andrews, T. J. (2014). Neural responses to facial expressions support the role of the amygdala in processing threat. Social Cognitive and Affective Neuroscience, 9, 16841689. doi:10.1093/scan/nst162CrossRefGoogle ScholarPubMed
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 and Adolescent Psychiatry, 52, 815830.e14. doi:10.1016/j.jaac.2013.05.011CrossRefGoogle Scholar
Miché, M., Hofer, P. D., Voss, C., Meyer, A. H., Gloster, A. T., Beesdo-Baum, K., & Lieb, R. (2018). Mental disorders and the risk for the subsequent first suicide attempt: Results of a community study on adolescents and young adults. European Child & Adolescent Psychiatry, 27, 839848. doi:10.1007/s00787-017-1060-5CrossRefGoogle Scholar
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008). Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. Journal of Psychiatric Research, 42, 515520. doi:10.1016/j.jpsychires.2008.01.017CrossRefGoogle ScholarPubMed
Patel, R., Spreng, R. N., Shin, L. M., & Girard, T. A. (2012). Neurocircuitry models of posttraumatic stress disorder and beyond: A meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 36, 21302142. doi:10.1016/j.neubiorev.2012.06.003CrossRefGoogle ScholarPubMed
Phelps, E. A. (2004). Human emotion and memory: Interactions of the amygdala and hippocampal complex. Current Opinion in Neurobiology, 14, 198202. doi:10.1016/j.conb.2004.03.015CrossRefGoogle ScholarPubMed
Philippot, P., & Feldman, R. S. (1990). Age and social competence in preschoolers’ decoding of facial expression. British Journal of Social Psychology, 29, 4354. doi:10.1111/j.2044-8309.1990.tb00885.xCrossRefGoogle ScholarPubMed
Picci, G., & Scherf, K. S. (2016). From caregivers to peers: Puberty shapes human face perception. Psychological Science, 27, 14611473. doi:10.1177/0956797616663142CrossRefGoogle ScholarPubMed
Pine, D. S., Mogg, K., Bradley, B. P., Montgomery, L., Monk, C. S., McClure, E., … Kaufman, J. (2005). Attention bias to threat in maltreated children: Implications for vulnerability to stress-related psychopathology. The American Journal of Psychiatry, 162, 291296. doi:10.1176/appi.ajp.162.2.291CrossRefGoogle ScholarPubMed
Pitkänen, A., Pikkarainen, M., Nurminen, N., & Ylinen, A. (2000). Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat: A review. Annals of the New York Academy of Sciences, 911, 369391. doi:10.1111/j.1749-6632.2000.tb06738.xCrossRefGoogle ScholarPubMed
Pole, N., Neylan, T. C., Otte, C., Henn-Hasse, C., Metzler, T. J., & Marmar, C. R. (2009). Prospective prediction of posttraumatic stress disorder symptoms using fear potentiated auditory startle responses. Biological Psychiatry, 65, 235240. doi:10.1016/j.biopsych.2008.07.015CrossRefGoogle ScholarPubMed
Pollak, S. D. (2008). Mechanisms linking early experience and the emergence of emotions: Illustrations from the study of maltreated children. Current Directions in Psychological Science, 17, 370375. doi:10.1111/j.1467-8721.2008.00608.xCrossRefGoogle Scholar
Pollak, S. D., Messner, M., Kistler, D. J., & Cohn, J. F. (2009). Development of perceptual expertise in emotion recognition. Cognition, 110, 242247. doi:10.1016/j.cognition.2008.10.010CrossRefGoogle ScholarPubMed
Pollak, S. D., & Sinha, P. (2002). Effects of early experience on children's recognition of facial displays of emotion. Developmental Psychology, 38, 784791. https://doi.org/10.1037/0012-1649.38.5.784CrossRefGoogle ScholarPubMed
R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.orgGoogle Scholar
RSTudio Team. (2012). RStudio: Integrated development for R. Boston, MA: RStudio, Inc.Google Scholar
Schmolck, H., & Squire, L. R. (2001). Impaired perception of facial emotions following bilateral damage to the anterior temporal lobe. Neuropsychology, 15, 3038. https://doi.org/10.1037/0894-4105.15.1.30CrossRefGoogle Scholar
Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., … Lüthi, A. (2014). Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron, 81, 428437. doi:10.1016/j.neuron.2013.11.006CrossRefGoogle ScholarPubMed
Shin, L. M., & Handwerger, K. (2009). Is posttraumatic stress disorder a stress-induced fear circuitry disorder? Journal of Traumatic Stress, 22, 409415. doi:10.1002/jts.20442CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Stevens, J. S., & Jovanovic, T. (2019). Role of social cognition in post-traumatic stress disorder: A review and meta-analysis. Genes, Brain, and Behavior, 18, e12518. doi:10.1111/gbb.12518CrossRefGoogle ScholarPubMed
Tottenham, N., Hare, T. A., & Casey, B. J. (2011). Behavioral assessment of emotion discrimination, emotion regulation, and cognitive control in childhood, adolescence, and adulthood. Frontiers in Psychology, 2. doi:10.3389/fpsyg.2011.00039CrossRefGoogle Scholar
Tovote, P., Fadok, J. P., & Lüthi, A. (2015). Neuronal circuits for fear and anxiety. Nature Reviews Neuroscience, 16, 317331. doi:10.1038/nrn3945CrossRefGoogle ScholarPubMed
Vetter, N. C., Drauschke, M., Thieme, J., & Altgassen, M. (2018). Adolescent basic facial emotion recognition is not influenced by puberty or own-age bias. Frontiers in Psychology, 9. doi:10.3389/fpsyg.2018.00956CrossRefGoogle ScholarPubMed
Weathers, F. W., Keane, T. M., & Davidson, J. R. (2001). Clinician-administered PTSD scale: A review of the first ten years of research. Depression and Anxiety, 13, 132156.CrossRefGoogle ScholarPubMed
Wechsler, D. (2011). Wechsler abbreviated scale of intelligence – Second edition manual. Bloomington, MN: Pearson.Google Scholar
Williamson, D. E., Birmaher, B., Ryan, N. D., Shiffrin, T. P., Lusky, J. A., Protopapa, J., … Brent, D. A. (2003). The stressful life events schedule for children and adolescents: Development and validation. Psychiatry Research, 119, 225241.CrossRefGoogle ScholarPubMed
Wolf, R. C. (2016). A role for ventromedial prefrontal cortex in facial emotion recognition (Ph.D., The University of Wisconsin – Madison). Madison, WI, USA: The University of Wisconsin. Retrieved from https://search.proquest.com/docview/1811945642/abstract/6DB38A4EE27F4A48PQ/1Google Scholar
Wolf, R. C., & Herringa, R. J. (2016). Prefrontal-amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 41, 822831. doi:10.1038/npp.2015.209CrossRefGoogle ScholarPubMed
Wolf, R. C., Philippi, C. L., Motzkin, J. C., Baskaya, M. K., & Koenigs, M. (2014). Ventromedial prefrontal cortex mediates visual attention during facial emotion recognition. Brain: A Journal of Neurology, 137, 17721780. doi:10.1093/brain/awu063CrossRefGoogle ScholarPubMed
Wright, B., Clarke, N., Jordan, J., Young, A. W., Clarke, P., Miles, J., … Williams, C. (2008). Emotion recognition in faces and the use of visual context Vo in young people with high-functioning autism spectrum disorders. Autism, 12, 607626. doi:10.1177/1362361308097118CrossRefGoogle Scholar
Young, J. C., & Widom, C. S. (2014). Long-term effects of child abuse and neglect on emotion processing in adulthood. Child Abuse & Neglect, 38, 13691381. doi:10.1016/j.chiabu.2014.03.008CrossRefGoogle ScholarPubMed
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