Hostname: page-component-77c89778f8-5wvtr Total loading time: 0 Render date: 2024-07-18T05:04:42.298Z Has data issue: false hasContentIssue false

Alterations in facial expressions in individuals at risk for psychosis: a facial electromyography approach using emotionally evocative film clips

Published online by Cambridge University Press:  26 October 2022

Tina Gupta*
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
K. Juston Osborne
Affiliation:
Department of Psychology, Northwestern University, Evanston, IL, USA
Ajay Nadig
Affiliation:
Harvard/MIT MD-PhD Program, Harvard Medical School, Boston, MA, 02115
Claudia M. Haase
Affiliation:
Department of Psychology, Northwestern University, Evanston, IL, USA School of Education and Social Policy, Northwestern University, Evanston, IL, USA
Vijay A. Mittal
Affiliation:
Department of Psychology, Northwestern University, Evanston, IL, USA
*
Author for correspondence: Tina Gupta, E-mail: tinagupta2021@u.northwestern.edu

Abstract

Background

Negative symptoms such as blunted facial expressivity are characteristic of schizophrenia. However, it is not well-understood if and what abnormalities are present in individuals at clinical high-risk (CHR) for psychosis.

Methods

This experimental study employed facial electromyography (left zygomaticus major and left corrugator supercilia) in a sample of CHR individuals (N = 34) and healthy controls (N = 32) to detect alterations in facial expressions in response to emotionally evocative film clips and to determine links with symptoms.

Results

Findings revealed that the CHR group showed facial blunting manifested in reduced zygomatic activity in response to an excitement (but not amusement, fear, or sadness) film clip compared to controls. Reductions in zygomatic activity in the CHR group emerged in response to the emotionally evocative peak period of the excitement film clip. Lower zygomaticus activity during the excitement clip was related to anxiety while lower rates of change in zygomatic activity during the excitement video clip were related to higher psychosis risk conversion scores.

Conclusions

Together, these findings inform vulnerability/disease driving mechanisms and biomarker and treatment development.

Type
Original Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

*

Co-Senior Authors.

References

Andreasen, N. C. (1982). Negative symptoms in schizophrenia: Definition and reliability. Archives of General Psychiatry, 39, 784788.CrossRefGoogle ScholarPubMed
Andreasen, N. C. (1997). The evolving concept of schizophrenia: From Kraepelin to the present and future. Schizophrenia Research, 28(2–3), 105109. https://doi.org/10.1016/S0920-9964(97)00112-6.CrossRefGoogle Scholar
Berenbaum, H., & Oltmanns, T. F. (2012). Emotional experience and expression in schizophrenia and depression. What the Face Reveals: Basic and Applied Studies of Spontaneous Expression Using the Facial Action Coding System (FACS), 101(November 1988), 3744. https://doi.org/10.1093/acprof:oso/9780195179644.003.0021.Google Scholar
Burton, K. W., & Kaszniak, A. W. (2006). Emotional experience and facial expression in Alzheimer's disease. Aging, Neuropsychology, and Cognition, 13(3–4), 636651. https://doi.org/10.1080/13825580600735085.CrossRefGoogle ScholarPubMed
Cacioppo, J. T., Petty, R. E., & Morris, K. J. (1985). Semantic, evaluative, and self-referent processing: Memory, cognitive effort, and somatovisceral activity. Psychophysiology, 22, 371384.CrossRefGoogle ScholarPubMed
Cannon, T. D., Cadenhead, K., Cornblatt, B., Woods, S. W., Addington, J., Walker, E., … Heinssen, R. (2008). Prediction of psychosis in youth at high clinical risk: A multisite longitudinal study in North America. Archives of General Psychiatry, 65(1), 2837. https://doi.org/10.1001/archgenpsychiatry.2007.3.CrossRefGoogle ScholarPubMed
Chen, K.-H., Lwi, S. J., Hua, A. Y., Haase, C. M., Miller, B. L., & Levenson, R. W. (2017a). Increased subjective experience of non-target emotions in patients with frontotemporal dementia and Alzheimer's disease. Current Opinion in Behavioral Sciences, 15, 7784. https://doi.org/10.1016/j.cobeha.2017.05.017.CrossRefGoogle ScholarPubMed
Chen, K.-H., Wells, J. L., Otero, M. C., Lwi, S. J., Haase, C. M., & Levenson, R. W. (2017b). Greater experience of negative non-target emotions by patients with neurodegenerative diseases is related to lower emotional well-being in caregivers. Dementia and Geriatric Cognitive Disorders, 44(5–6), 245255. https://doi.org/10.1159/000481132.CrossRefGoogle ScholarPubMed
Cohen, A. S., Morrison, S. C., & Callaway, D. A. (2013). Computerized facial analysis for understanding constricted/blunted affect: Initial feasibility, reliability, and validity data. Schizophrenia Research, 148(1–3), 111116. https://doi.org/10.1016/j.schres.2013.05.003.CrossRefGoogle ScholarPubMed
Cowan, T., Masucci, M. D., Gupta, T., Haase, C. M., Strauss, G. P., & Cohen, A. S. (2022a). Computerized analysis of facial expressions in serious mental illness. Schizophrenia Research, 241, 4451. https://doi.org/10.1016/j.schres.2021.12.026.CrossRefGoogle ScholarPubMed
Cowan, T., Strauss, G. P., Raugh, I. M., Le, T. P., & Cohen, A. S. (2022b). How do social factors relate to blunted facial affect in schizophrenia? A digital phenotyping study using ambulatory video recordings. Journal of Psychiatric Research, 150, 96104. https://doi.org/10.1016/j.jpsychires.2022.03.024.CrossRefGoogle ScholarPubMed
Damme, K. S. F., Park, J. S., Vargas, T., Walther, S., Shankman, S. A., & Mittal, V. A. (2022). Motor abnormalities, depression risk, and clinical course in adolescence. Biological Psychiatry Global Open Science, 2(1), 6169. https://doi.org/10.1016/j.bpsgos.2021.06.011.CrossRefGoogle ScholarPubMed
Dimberg, U. (1982). Facial reactions to facial expressions. Psychophysiology, 19(6), 643647. https://doi.org/10.1111/j.1469-8986.1982.tb02516.x.CrossRefGoogle ScholarPubMed
Dowd, E. C., & Barch, D. M. (2010). Anhedonia and emotional experience in schizophrenia: Neural and behavioral indicators. Biological Psychiatry, 67(10), 902911. https://doi.org/10.1016/j.biopsych.2009.10.020.CrossRefGoogle ScholarPubMed
Dukes, D., Abrams, K., Adolphs, R., Ahmed, M. E., Beatty, A., Berridge, K. C., … Sander, D. (2021). The rise of affectivism. Nature Human Behaviour, 5(7), 816820. https://doi.org/10.1038/s41562-021-01130-8.CrossRefGoogle ScholarPubMed
Ekman, P., & Friesen, W. V. (1982). Felt, false, and miserable smiles. Journal of Nonverbal Behavior, 6(4), 238252. https://doi.org/10.1007/BF00987191.CrossRefGoogle Scholar
Ekman, P., Friesen, W. V., & Hager, J. C. (2002). Facial Action Coding System: The manual On CD ROM. Salt Lake City, UT: The Human Face.Google Scholar
First, M. B. (2014). Structured clinical interview for the DSM (SCID). R.L. Cautin & S.O. Lilienfeld (Eds.). The Encyclopedia of Clinical Psychology, 16. https://doi.org/10.1002/9781118625392.wbecp351Google Scholar
Foussias, G., Agid, O., Fervaha, G., & Remington, G. (2014). Negative symptoms of schizophrenia: Clinical features, relevance to real world functioning and specificity versus other CNS disorders. European Neuropsychopharmacology, 24(5), 693709. https://doi.org/10.1016/j.euroneuro.2013.10.017.CrossRefGoogle ScholarPubMed
Fridlund, A. J., & Cacioppo, J. T. (1986). Guidelines for human electromyographic research. Psychophysiology, 23(5), 567589.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Borgwardt, S., Bechdolf, A., Addington, J., Riecher-Rössler, A., Schultze-Lutter, F., … Yung, A. (2013). The psychosis high-risk state. JAMA Psychiatry, 70(1), 107120. https://doi.org/10.1001/jamapsychiatry.2013.269.CrossRefGoogle ScholarPubMed
Gray, H. M., Ishii, K., & Ambady, N. (2011). Misery loves company: When sadness increases the desire for social connectedness. Personality and Social Psychology Bulletin, 37(11), 14381448.CrossRefGoogle ScholarPubMed
Greden, J. F., Price, H. L., Genero, N., Feinberg, M., & Levine, S. (1984). Facial EMG activity levels predict treatment outcome in depression. Psychiatry Research, 13(4), 345352. https://doi.org/10.1016/0165-1781(84)90082-9.CrossRefGoogle ScholarPubMed
Gross, J. J., & Levenson, R. W. (1995). Emotion elicitation using films. Cognition & Emotion, 9(1), 87108. https://doi.org/10.1080/02699939508408966.CrossRefGoogle Scholar
Gruber, J., Oveis, C., Keltner, D., & Johnson, S. L. (2008). Risk for mania and positive emotional responding: Too much of a good thing? Emotion (Washington, D.C.), 8(1), 2333. https://doi.org/10.1037/1528-3542.8.1.23.CrossRefGoogle ScholarPubMed
Gruber, J., Strauss, G. P., Dombrecht, L., & Mittal, V. A. (2018). Neuroleptic-free youth at ultrahigh risk for psychosis evidence diminished emotion reactivity that is predicted by depression and anxiety. Schizophrenia Research, 193, 428434. https://doi.org/10.1016/j.schres.2017.08.013.CrossRefGoogle ScholarPubMed
Gupta, T., Haase, C. M., Strauss, G. P., Cohen, A. S., & Mittal, V. A. (2019). Alterations in facial expressivity in youth at clinical high-risk for psychosis. Journal of Abnormal Psychology, 128(4), 341351. https://doi.org/10.1037/abn0000413.CrossRefGoogle ScholarPubMed
Gupta, T., Haase, C. M., Strauss, G. P., Cohen, A. S., Ricard, J. R., & Mittal, V. A. (2022). Alterations in facial expressions of emotion: Determining the promise of ultrathin slicing approaches and comparing human and automated coding methods in psychosis risk. Emotion, 22(4), 714.CrossRefGoogle ScholarPubMed
Gur, R. E., Kohler, C. G., Ragland, J. D., Siegel, S. J., Lesko, K., Bilker, W. B., & Gur, R. C. (2006). Flat affect in schizophrenia: Relation to emotion processing and neurocognitive measures. Schizophrenia Bulletin, 32(2), 279287. https://doi.org/10.1093/schbul/sbj041.CrossRefGoogle ScholarPubMed
James, W. (1948). II. – What is an emotion? Mind, Os-IX(34), 188205. https://doi.org/10.1093/mind/os-IX.34.188.Google Scholar
Johnson, S. L., Haase, C. M., Beermann, U., Sanchez, A. H., Tharp, J. A., Lwi, S. J., … Nguyen, N. K. (2017). Positive urgency and emotional reactivity: Evidence for altered responding to positive stimuli. Emotion (Washington, D.C.), 17(3), 442449. https://doi.org/10.1037/emo0000240.CrossRefGoogle ScholarPubMed
Keltner, D., & Bonanno, G. A. (n.d.). A Study of Laughter and Dissociation: Distinct Correlates of Laughter and Smiling During Bereavement. 16.Google Scholar
Keltner, D., & Gross, J. J. (1999). Functional accounts of emotions. Cognition and Emotion, 13(5), 467480. https://doi.org/10.1080/026999399379140.CrossRefGoogle Scholar
Keltner, D., Kring, A. M., & Bonanno, G. A. (1999). Fleeting signs of the course of life: Facial expression and personal adjustment. Current Directions in Psychological Science, 8(1), 1822. https://doi.org/10.1111/1467-8721.00005.CrossRefGoogle Scholar
Kirkpatrick, B., Fenton, W. S., Carpenter, W. T., & Marder, S. R. (2006). The NIMH-MATRICS consensus statement on negative symptoms. Schizophrenia Bulletin, 32(2), 214219. https://doi.org/10.1093/schbul/sbj053.CrossRefGoogle ScholarPubMed
Kring, A. M., & Elis, O. (2013). Emotion deficits in people with schizophrenia. Annual Review of Clinical Psychology, 9(1), 409433. https://doi.org/10.1146/annurev-clinpsy-050212-185538.CrossRefGoogle ScholarPubMed
Kring, A. M., Kerr, S. L., & Earnst, K. S. (1999). Schizophrenic patients show facial reactions to emotional facial expressions. Psychophysiology, 36(2), 186192. https://doi.org/10.1111/1469-8986.3620186.CrossRefGoogle ScholarPubMed
Kring, A. M., Kerr, S. L., Smith, D. A., & Neale, J. M. (1993). Flat affect in schizophrenia does not reflect diminished subjective experience of emotion. Journal of Abnormal Psychology, 102(4), 507517. https://doi.org/10.1037/0021-843X.102.4.507.CrossRefGoogle Scholar
Lang, P. J., Greenwald, M. K., Bradley, M. M., & Hamm, A. O. (1993). Looking at pictures: Affective, facial, visceral, and behavioral reactions. Psychophysiology, 30(3), 261273. https://doi.org/10.1111/j.1469-8986.1993.tb03352.x.CrossRefGoogle ScholarPubMed
Lee, J. S., Chun, J. W., Yoon, S. Y., Park, H. J., & Kim, J. J. (2014). Involvement of the mirror neuron system in blunted affect in schizophrenia. Schizophrenia Research, 152(1), 268274. https://doi.org/10.1016/j.schres.2013.10.043.CrossRefGoogle ScholarPubMed
Levenson, R. W. (2014). The autonomic nervous system and emotion. Emotion Review, 6(2), 100112. https://doi.org/10.1177/1754073913512003.CrossRefGoogle Scholar
McGlashan, T. H., Miller, T. J., Woods, S. W., Rosen, J. L., Hoffman, R. E., & Davidson, L. (2001). Structured interview for prodromal syndromes. New Haven, CT: PRIME Research Clinic, Yale School of Medicine.Google Scholar
Miller, T. J., McGlashan, T. H., Rosen, J. L., Cadenhead, K., Ventura, J., McFarlane, W., … Woods, S. W. (2003). Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: Predictive validity, interrater reliability, and training to reliability. Schizophrenia Bulletin, 29(4), 703715. https://doi.org/10.1093/oxfordjournals.schbul.a007040.CrossRefGoogle ScholarPubMed
Mittal, V. A., & Walker, E. F. (2007). Movement abnormalities predict conversion to Axis I psychosis among prodromal adolescents. Journal of Abnormal Psychology, 116(4), 796803. (2007-17062-012). https://doi.org/10.1037/0021-843X.116.4.796.CrossRefGoogle ScholarPubMed
Noah, T., Schul, Y., & Mayo, R. (2018). When both the original study and its failed replication are correct: Feeling observed eliminates the facial-feedback effect. Journal of Personality and Social Psychology, 114(5), 657664. https://doi.org/10.1037/pspa0000121.CrossRefGoogle ScholarPubMed
Osborne, K. J., Damme, K. S. F., Gupta, T., Dean, D. J., Bernard, J. A., & Mittal, V. A. (2021). Timing dysfunction and cerebellar resting state functional connectivity abnormalities in youth at clinical high-risk for psychosis. Psychological Medicine, 51(8), 12891298. https://doi.org/10.1017/S0033291719004161.CrossRefGoogle ScholarPubMed
Osborne, K. J., & Mittal, V. A. (2019). External validation and extension of the NAPLS-2 and SIPS-RC personalized risk calculators in an independent clinical high-risk sample. Psychiatry Research, 279, 914. https://doi.org/10.1016/j.psychres.2019.06.034.CrossRefGoogle Scholar
Osborne, K. J., & Mittal, V. A. (2022). Postural sway and neurocognition in individuals meeting criteria for a clinical high-risk syndrome. European Archives of Psychiatry and Clinical Neuroscience, 272(1), 155160. https://doi.org/10.1007/s00406-021-01234-2.CrossRefGoogle ScholarPubMed
Papa, A., & Bonanno, G. A. (2008). Smiling in the face of adversity: The interpersonal and intrapersonal functions of smiling. Emotion, 8(1), 1.CrossRefGoogle ScholarPubMed
Piskulic, D., Addington, J., Cadenhead, K. S., Cannon, T. D., Cornblatt, B. A., Heinssen, R., … McGlashan, T. H. (2012). Negative symptoms in individuals at clinical high risk of psychosis. Psychiatry Research, 196(2), 220224. https://doi.org/10.1016/j.psychres.2012.02.018.CrossRefGoogle ScholarPubMed
Ricard, J. R., Gupta, T., Vargas, T., Haase, C. M., & Mittal, V. A. (2022). Genuine and non-genuine smiles in individuals meeting criteria for a clinical high-risk syndrome. Early Intervention in Psychiatry, 16(8), 875882.CrossRefGoogle ScholarPubMed
Rompilla, D. B. Jr., Hittner, E. F., Stephens, J. E., Mauss, I., & Haase, C. M. (2021). Emotion regulation in the face of loss: How detachment, positive reappraisal, and acceptance shape experiences, physiology, and perceptions in late life. Emotion, 22(7), 14171434. https://doi.org/10.1037/emo0000932.CrossRefGoogle ScholarPubMed
Ruch, W., & McGhee, P. E. (2014). Humor intervention programs. In A.C. Parks & S.M. Schueller (Eds.). The Wiley Blackwell handbook of positive psychological interventions (pp. 179193). Wiley Blackwell. https://doi.org/10.1002/9781118315927.ch10.CrossRefGoogle Scholar
Schiffman, J. (2017). Motor issues in the clinical high risk phase of psychosis. Schizophrenia Bulletin, 43(5), 937938. https://doi.org/10.1093/schbul/sbx086.CrossRefGoogle ScholarPubMed
Sestito, M., Umilta’, M. A., De Paola, G., Fortunati, R., Raballo, A., Leuci, E., … Gallese, V. (2013). Facial reactions in response to dynamic emotional stimuli in different modalities in patients suffering from schizophrenia: A behavioral and EMG study. Frontiers in Human Neuroscience, 7, 368. https://doi.org/10.3389/fnhum.2013.00368.CrossRefGoogle ScholarPubMed
Shiota, M. N., & Levenson, R. W. (2009). Effects of aging on experimentally instructed detached reappraisal, positive reappraisal, and emotional behavior suppression. Psychology and Aging, 24(4), 890900. https://doi.org/10.1037/a0017896.CrossRefGoogle ScholarPubMed
Soto, J. A., Levenson, R. W., & Ebling, R. (2005). Cultures of moderation and expression: Emotional experience, behavior, and physiology in Chinese Americans and Mexican Americans. Emotion (Washington, D.C.), 5(2), 154165. https://doi.org/10.1037/1528-3542.5.2.154.CrossRefGoogle ScholarPubMed
Strauss, G. P., Horan, W. P., Kirkpatrick, B., Fischer, B. A., Keller, W. R., Miski, P., … Carpenter, W. T. (2013). Deconstructing negative symptoms of schizophrenia: Avolition–apathy and diminished expression clusters predict clinical presentation and functional outcome. Journal of Psychiatric Research, 47(6), 783790. https://doi.org/10.1016/j.jpsychires.2013.01.015.CrossRefGoogle ScholarPubMed
Strauss, G. P., Pelletier-Baldelli, A., Visser, K. F., Walker, E. F., & Mittal, V. A. (2020). A review of negative symptom assessment strategies in youth at clinical high-risk for psychosis. Schizophrenia Research, 222, 104112. https://doi.org/10.1016/j.schres.2020.04.019.CrossRefGoogle ScholarPubMed
Trémeau, F. (2006). A review of emotion deficits in schizophrenia. Dialogues in Clinical Neuroscience, 8(1), 5970.CrossRefGoogle ScholarPubMed
Trémeau, F., Malaspina, D., Duval, F., Corrêa, H., Hager-Budny, M., Coin-Bariou, L., … Gorman, J. M. (2005). Facial expressiveness in patients with schizophrenia compared to depressed patients and nonpatient comparison subjects. American Journal of Psychiatry, 162(1), 92101. https://doi.org/10.1176/appi.ajp.162.1.92.CrossRefGoogle ScholarPubMed
Tron, T., Peled, A., Grinsphoon, A., & Weinshall, D. (2016). Automated facial expressions analysis in schizophrenia: A continuous dynamic approach. In Serino, S., Matic, A., Giakoumis, D., Lopez, G., & Cipresso, P. (Eds.), Pervasive computing paradigms for mental health (pp. 7281). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-32270-4_8.CrossRefGoogle Scholar
Varcin, K. J., Bailey, P. E., & Henry, J. D. (2010). Empathic deficits in schizophrenia: The potential role of rapid facial mimicry. Journal of the International Neuropsychological Society, 16(4), 621629. https://doi.org/10.1017/S1355617710000329.CrossRefGoogle ScholarPubMed
Volz, M., Hamm, A. O., Kirsch, P., & Rey, E.-R. (2003). Temporal course of emotional startle modulation in schizophrenia patients. International Journal of Psychophysiology, 49(2), 123137. https://doi.org/10.1016/S0167-8760(03)00100-4.CrossRefGoogle ScholarPubMed
Walker, E., Lewis, N., Loewy, R., & Palyo, S. (1999). Motor dysfunction and risk for schizophrenia. Development and Psychopathology, 11(3), 509523. https://doi.org/10.1017/S0954579499002187.CrossRefGoogle ScholarPubMed
Walker, E. F., Grimes, K. E., Davis, D. M., & Smith, A. J. (1993). Childhood precursors of schizophrenia: Facial expressions of emotion. The American Journal of Psychiatry, 150(11), 16541660. https://doi.org/10.1176/ajp.150.11.1654.Google ScholarPubMed
Werner, K. H., Roberts, N. A., Rosen, H. J., Dean, D. L., Kramer, J. H., Weiner, M. W., … Levenson, R. W. (2007). Emotional reactivity and emotion recognition in frontotemporal lobar degeneration. Neurology, 69(2), 148155. https://doi.org/10.1212/01.wnl.0000265589.32060.d3.CrossRefGoogle ScholarPubMed
Wolf, K., Mass, R., Kiefer, F., Wiedemann, K., & Naber, D. (2006). Characterization of the facial expression of emotions in schizophrenia patients: Preliminary findings with a new electromyography method. The Canadian Journal of Psychiatry, 51(6), 335341. https://doi.org/10.1177/070674370605100601.CrossRefGoogle ScholarPubMed
Zec, R. F. (1995). Neuropsychology of schizophrenia according to Kraepelin: Disorders of volition and executive functioning. European Archives of Psychiatry and Clinical Neuroscience, 245(4–5), 216223. https://doi.org/10.1007/BF02191800.CrossRefGoogle ScholarPubMed
Zhang, T., Li, H., Tang, Y., Niznikiewicz, M. A., Shenton, M. E., Keshavan, M. S., … Wang, J. (2018). Validating the predictive accuracy of the NAPLS-2 psychosis risk calculator in a clinical high-risk sample from the SHARP (Shanghai At Risk for Psychosis) program. American Journal of Psychiatry, 175(9), 906908. https://doi.org/10.1176/appi.ajp.2018.18010036.CrossRefGoogle Scholar
Zhang, T., Xu, L., Tang, Y., Li, H., Tang, X., Cui, H.Wang, J. (2019). Prediction of psychosis in prodrome: development and validation of a simple, personalized risk calculator. Psychological Medicine, 49(12), 19901998.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gupta et al. supplementary material

Gupta et al. supplementary material

Download Gupta et al. supplementary material(File)
File 23.7 KB