Skip to main content
Log in

Angry but not neutral faces facilitate response inhibition in schizophrenia patients

  • Original Paper
  • Published:
European Archives of Psychiatry and Clinical Neuroscience Aims and scope Submit manuscript

Abstract

Schizophrenia is a very heterogeneous disorder with extensive impairments in cognitive as well as emotional abilities. One critical domain is response inhibition, and previous studies in schizophrenia patients have mostly observed impairments, i.e., slower inhibition. Moreover, response inhibition to socially salient stimuli has not been investigated in schizophrenia so far. Therefore, to elucidate emotion–cognition interactions by examining potential emotional effects on inhibition processes and further investigate the association of cognition with inhibition we used an emotional stop signal task in 27 schizophrenia patients and 27 gender- and age-matched controls. Task irrelevant emotional faces (angry and neutral) were used as stimuli in a stop signal reaction time task. Regarding accuracy, patients showed significantly worse performance in neutral trials, while their performance in anger trials (stop and go) was similar to controls. Angry faces elicited faster response inhibition in both groups, underlining an emotional facilitation effect. Neurocognitive functions significantly correlated with accuracy in the stop signal task in schizophrenia patients, thus further strengthening the notion of the strong link between cognitive abilities and inhibition processes. Inhibitory control impairments are of high clinical interest due to their association with substance abuse, impulsive behavior and suicide. Based on our data, neutral faces significantly affect response inhibition in schizophrenia while an emotional facilitation effect was apparent for angry faces even in schizophrenia patients. Thus, our data further support the notion that neutral face processing is critically impaired in schizophrenia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Derntl B, Habel U (2011) Deficits in social cognition: a marker for psychiatric disorders? Eur Arch Psychiatry Clin Neurosci 261:145–149

    Article  Google Scholar 

  2. Green MF, Horan WP, Lee J (2015) Social cognition in schizophrenia. Nat Rev Neurosci 16:620–631

    Article  CAS  PubMed  Google Scholar 

  3. Fett AK, Viechtbauer W, Dominguez MD, Penn DL, van Os J, Krabbendam L (2011) The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neurosci Biobehav Rev 35:573–588

    Article  PubMed  Google Scholar 

  4. Bowers L, Jeffery D, Bilgin H, Jarrett M, Simpson A, Jones J (2008) Psychiatric intensive care units: a literature review. Int J Soc Psychiatry 54:56–68

    Article  PubMed  Google Scholar 

  5. Gut-Fayand A, Dervaux A, Olie JP, Loo H, Poirier MF, Krebs MO (2001) Substance abuse and suicidality in schizophrenia: a common risk factor linked to impulsivity. Psychiatry Res 102:65–72

    Article  CAS  PubMed  Google Scholar 

  6. Volavka J, Citrome L (2008) Heterogeneity of violence in schizophrenia and implications for long-term treatment. Int J Clin Pract 62:1237–1245

    Article  CAS  PubMed  Google Scholar 

  7. Bellgrove MA, Chambers CD, Vance A, Hall N, Karamitsios M, Bradshaw JL (2006) Lateralized deficit of response inhibition in early-onset schizophrenia. Psychol Med 36:495–505

    Article  PubMed  Google Scholar 

  8. Hughes ME, Fulham WR, Johnston PJ, Michie PT (2012) Stop-signal response inhibition in schizophrenia: behavioral, event-related potential and functional neuroimaging data. Biol Psychol 89:220–231

    Article  PubMed  Google Scholar 

  9. Nolan KA, D’Angelo D, Hoptman MJ (2011) Self-report and laboratory measures of impulsivity in patients with schizophrenia or schizoaffective disorder and healthy controls. Psychiatry Res 187:301–303

    Article  PubMed  Google Scholar 

  10. Lipszyc J, Schachar R (2010) Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsychol Soc 16:1064–1076

    Article  PubMed  Google Scholar 

  11. Badcock JC, Michie PT, Johnson L, Combrinck J (2002) Acts of control in schizophrenia: dissociating the components of inhibition. Psychol Med 32:287–297

    Article  CAS  PubMed  Google Scholar 

  12. Ethridge LE, Soilleux M, Nakonezny PA, Reilly JL, Hill SK, Keefe RSE, Gershon ES, Pearlson GD, Tamminga CA, Keshavan MS, Sweeney JA (2014) Behavioral response inhibition in psychotic disorders: diagnostic specificity, familiality and relation to generalized cognitive deficit. Schizophr Res 159:491–498

    Article  PubMed  PubMed Central  Google Scholar 

  13. Park IH, Park HJ, Chun JW, Kim EY, Kim JJ (2008) Dysfunctional modulation of emotional interference in the medial prefrontal cortex in patients with schizophrenia. Neurosci Lett 440:119–124

    Article  CAS  PubMed  Google Scholar 

  14. Egashira K, Matsuo K, Nakashima M, Watanuki T, Harada K, Nakano M, Matsubara T, Takahashi K, Watanabe Y (2015) Blunted brain activation in patients with schizophrenia in response to emotional cognitive inhibition: a functional near-infrared spectroscopy study. Schizophr Res 162:196–204

    Article  PubMed  Google Scholar 

  15. Vercammen A, Morris R, Green MJ, Lenroot R, Kulkarni J, Carr VJ, Weickert CS, Weickert TW (2012) Reduced neural activity of the prefrontal cognitive control circuitry during response inhibition to negative words in people with schizophrenia. J Psychiatry Neurosci 37:379–388

    Article  PubMed  PubMed Central  Google Scholar 

  16. Adolphs R (2001) The neurobiology of social cognition. Curr Opin Neurobiol 11:231–239

    Article  CAS  PubMed  Google Scholar 

  17. Horstmann G (2003) What do facial expressions convey: feeling states, behavioral intentions, or action requests? Emotion 3:150–166

    Article  PubMed  Google Scholar 

  18. Seidel EM, Habel U, Kirschner M, Gur RC, Derntl B (2010) The impact of facial emotional expressions on behavioral tendencies in women and men. J Exp Psychol Hum Percept Perform 36:500–507

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kohler CG, Walker JB, Martin EA, Healey KM, Moberg PJ (2010) Facial emotion perception in schizophrenia: a meta-analytic review. Schizophr Bull 36:1009–1019

    Article  PubMed  Google Scholar 

  20. Abram SV, Karpouzian TM, Reilly JL, Derntl B, Habel U, Smith MJ (2014) Accurate perception of negative emotions predicts functional capacity in schizophrenia. Psychiatry Res 216:6–11

    Article  PubMed  Google Scholar 

  21. Pawliczek CM, Derntl B, Kellermann T, Kohn N, Gur RC, Habel U (2013) Inhibitory control and trait aggression: neural and behavioral insights using the emotional stop signal task. Neuroimage 79:264–274

    Article  PubMed  Google Scholar 

  22. Pessoa L, Padmala S, Kenzer A, Bauer A (2012) Interactions between cognition and emotion during response inhibition. Emotion 12:192–197

    Article  PubMed  Google Scholar 

  23. Kring AM, Moran EK (2008) Emotional response deficits in schizophrenia: insights from affective science. Schizophr Bull 34:819–834

    Article  PubMed  PubMed Central  Google Scholar 

  24. Habel U, Chechko N, Pauly K, Koch K, Backes V, Seiferth N, Shah NJ, Stöcker T, Schneider F (2010) Neural correlates of emotion recognition in schizophrenia. Schizophr Res 122:113–123

    Article  PubMed  Google Scholar 

  25. Derntl B, Kryspin-Exner I, Fernbach E, Moser E, Habel U (2008) Emotion recognition accuracy in healthy young females is associated with cycle phase. Horm Behav 53:90–95

    Article  PubMed  Google Scholar 

  26. Wittchen H, Zaudig M, Fydrich T (1997) Strukturiertes Klinisches Interview für DSM-IV. Hogrefe, Göttingen

    Google Scholar 

  27. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276

    Article  CAS  PubMed  Google Scholar 

  28. Andreasen NC, Pressler M, Nopoulos P, Miller D, Ho B-C (2010) Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biol Psychiatry 67:255–262

    Article  CAS  PubMed  Google Scholar 

  29. Naber D, Lambert M (2004) Kompendium der psychiatrischen Pharmakotherapie. Georg Thieme Verlag, Stuttgart

    Google Scholar 

  30. Radke S, Pfersmann V, Derntl B (2015) The impact of emotional faces on social motivation in schizophrenia. Eur Arch Psychiatry Clin Neurosci 265:613–622

    Article  PubMed  Google Scholar 

  31. Gur RC, Sara R, Hagendoorn M, Marom O, Hughett P, Macy L, Turner T, Bajcsy R, Posner A, Gur RE (2002) A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J Neurosci Methods 115:137–143

    Article  PubMed  Google Scholar 

  32. Li C, Huang C, Constable T, Sinha R (2006) Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. J Neurosci 26:186–192

    Article  CAS  PubMed  Google Scholar 

  33. Li C, Yan P, Sinha R, Lee T (2008) Sub-cortical processes of motor response inhibition during a stop signal task. Neuroimage 41:1352–1363

    Article  PubMed  PubMed Central  Google Scholar 

  34. Li C, Zhang S, Duann J, Yan P, Sinha R, Mazure C (2009) Gender differences in cognitive control: an extended investigation of the stop signal task. Brain Imaging Behav 3:262–276

    Article  PubMed  PubMed Central  Google Scholar 

  35. Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt Impulsiveness scale. J Clin Psychol 51:768–774

    Article  CAS  PubMed  Google Scholar 

  36. Preuss U, Rujescu D, Giegling I, Watzke S, Kollger G, Zetzsche T, Meisenzahl E, Soyka M, Möller H (2008) Psychometrische Evaluation der deutschsprachigen Version der Barratt-Impulsiveness-Skala. Nervenarzt 3:305–319

    Article  Google Scholar 

  37. Reitan R (1956) Trail making test: manual for administration, scoring and interpretation. Indiana University Press, Indianapolis

    Google Scholar 

  38. Lehrl S, Triebig G, Fischer B (1995) Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 91:335–345

    Article  CAS  PubMed  Google Scholar 

  39. Hautzinger M, Keller F, Kühner C (2006) BDI-II. Beck Depressions-Inventar Revision. Harcourt Test Services, Frankfurt am Main

    Google Scholar 

  40. Stuss DT, Murphy KJ, Binns MA, Alexander MP (2003) Staying on the job: the frontal lobes control individual performance variability. Brain 126:2363–2380

    Article  PubMed  Google Scholar 

  41. Pinkham AE, Brensinger C, Kohler C, Gur RE, Gur RC (2011) Actively paranoid patients with schizophrenia over attribute anger to neutral faces. Schizophr Res 125:174–178

    Article  PubMed  Google Scholar 

  42. Seiferth NY, Pauly K, Kellermann T, Shah NJ, Ott G, Herpertz-Dahlmann B, Schneider F, Kircher T, Habel U (2009) Neuronal correlates of facial emotion discrimination in early onset schizophrenia. Neuropsychopharmacology 34:477–487

    Article  PubMed  Google Scholar 

  43. Phillips LK, Seidman LJ (2008) Emotion processing in persons at risk for schizophrenia. Schizophr Bull 34:888–903

    Article  PubMed  PubMed Central  Google Scholar 

  44. Thakkar KN, Congdon E, Poldrack RA, Sabb FW, London ED, Cannon TD, Bilder RM (2014) Women are more sensitive than men to prior trial events on the stop-signal task. Br J Psychol 105:254–272

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Nina Trojan and Pia Hoffmann, Dr. Vera Pfersmann, Dr. Werner Brosch, Mag. Manfred Kornberger, Dr. Maria Doppelbauer-Dragschitz, Dr. Eleonore Miller-Reiter and Dr. Friedrich Schmidl for their assistance and support of data collection and patient recruitment. BD and UH were supported by the Austrian Science Fund (P23533-B13), German Research Foundation (DFG, IRTG 1318 and 2150) and JARA BRAIN. Funding agencies had no role regarding data analyses, preparation or submission of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Birgit Derntl.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Derntl, B., Habel, U. Angry but not neutral faces facilitate response inhibition in schizophrenia patients. Eur Arch Psychiatry Clin Neurosci 267, 621–627 (2017). https://doi.org/10.1007/s00406-016-0748-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00406-016-0748-8

Keywords

Navigation