Skip to main content
SpringerLink
Log in

Restricted attention to social cues in schizophrenia patients

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

Abstract

Deficits of psychosocial functioning are a robust finding in schizophrenia. Research on social cognition may open a new avenue for the development of effective interventions. As a correlate of social perceptive information processing deficits, schizophrenia patients (SZP) show deviant gaze behavior (GB) while viewing emotional faces. As understanding of a social environment requires gathering complex social information, our study aimed at investigating the gaze behavior of SZP related to social interactions and its impact on the level of social and role functioning. GB of 32 SZP and 37 healthy control individuals (HCI) was investigated with a high-resolution eye tracker during an unguided viewing of 12 complex pictures of social interaction scenes. Regarding whole pictures, SZP showed a shorter scanpath length, fewer fixations and a shorter mean distance between fixations. Furthermore, SZP exhibited fewer and shorter fixations on faces, but not on the socially informative bodies nor on the background, suggesting a cue-specific abnormality. Logistic regression with bootstrapping yielded a model including two GB parameters; a subsequent ROC curve analysis indicated an excellent ability of group discrimination (AUC .85). Face-related GB aberrations correlated with lower social and role functioning and with delusional thinking, but not with negative symptoms. Training of spontaneous integration of face-related social information seems promising to enable a holistic perception of social information, which may in turn improve social and role functioning. The observed ability to discriminate SZP from HCI warrants further research on the predictive validity of GB in psychosis risk prediction.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Bellack AS et al (1990) An analysis of social competence in schizophrenia. Br J Psychiatry 156:809–818

    Article  CAS  PubMed  Google Scholar 

  2. Bellack AS et al (2007) Assessment of community functioning in people with schizophrenia and other severe mental illnesses: a white paper based on an NIMH-sponsored workshop. Schizophr Bull 33(3):805–822

    Article  PubMed  Google Scholar 

  3. Penn DL et al (1997) Social cognition in schizophrenia. Psychol Bull 121(1):114–132

    Article  CAS  PubMed  Google Scholar 

  4. Green MF et al (2008) Social cognition in schizophrenia: an NIMH workshop on definitions, assessment, and research opportunities. Schizophr Bull 34(6):1211–1220

    Article  PubMed  PubMed Central  Google Scholar 

  5. Green MF et al (2005) Social cognition in schizophrenia: recommendations from the measurement and treatment research to improve cognition in schizophrenia new approaches conference. Schizophr Bull 31(4):882–887

    Article  PubMed  Google Scholar 

  6. Green MF, Horan WP, Lee J (2015) Social cognition in schizophrenia. Nat Rev Neurosci 16(10):620–631

    Article  CAS  PubMed  Google Scholar 

  7. Horan WP et al (2012) Social cognition in schizophrenia, Part 2: 12-month stability and prediction of functional outcome in first-episode patients. Schizophr Bull 38(4):865–872

    Article  PubMed  Google Scholar 

  8. Roberts DL et al (2014) A randomized, controlled trial of social cognition and interaction training (SCIT) for outpatients with schizophrenia spectrum disorders. Br J Clin Psychol 53(3):281–298

    Article  PubMed  Google Scholar 

  9. Couture SM, Penn DL, Roberts DL (2006) The functional significance of social cognition in schizophrenia: a review. Schizophr Bull 32(Suppl 1):S44–S63

    Article  PubMed  PubMed Central  Google Scholar 

  10. Fett AK et al (2011) The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neurosci Biobehav Rev 35(3):573–588

    Article  PubMed  Google Scholar 

  11. Schmidt SJ, Mueller DR, Roder V (2011) Social cognition as a mediator variable between neurocognition and functional outcome in schizophrenia: empirical review and new results by structural equation modeling. Schizophr Bull 37(Suppl 2):S41–S54

    Article  PubMed  PubMed Central  Google Scholar 

  12. Penn DL et al (2009) The effects of antipsychotic medications on emotion perception in patients with chronic schizophrenia in the CATIE trial. Schizophr Res 115(1):17–23

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kee KS et al (1998) Risperidone versus haloperidol for perception of emotion in treatment-resistant schizophrenia: preliminary findings. Schizophr Res 31(2–3):159–165

    Article  CAS  PubMed  Google Scholar 

  14. van der Gaag M et al (2013) Preventing a first episode of psychosis: meta-analysis of randomized controlled prevention trials of 12 month and longer-term follow-ups. Schizophr Res 149(1–3):56–62

    Article  PubMed  Google Scholar 

  15. Schmidt SJ et al (2015) EPA guidance on the early intervention in clinical high risk states of psychoses. Eur Psychiatry 30:388–404

    Article  CAS  PubMed  Google Scholar 

  16. Kohler CG et al (2010) Facial emotion perception in schizophrenia: a meta-analytic review. Schizophr Bull 36(5):1009–1019

    Article  PubMed  Google Scholar 

  17. Yalcin-Siedentopf N et al (2014) Facial affect recognition in symptomatically remitted patients with schizophrenia and bipolar disorder. Schizophr Res 152(2–3):440–445

    Article  PubMed  Google Scholar 

  18. Kurtz MM, Richardson CL (2012) Social cognitive training for schizophrenia: a meta-analytic investigation of controlled research. Schizophr Bull 38(5):1092–1104

    Article  PubMed  Google Scholar 

  19. Marsh PJ et al (2012) Effects of facial emotion recognition remediation on visual scanning of novel face stimuli. Schizophr Res 141(2–3):234–240

    Article  PubMed  Google Scholar 

  20. Wölwer W, Frommann N (2011) Social-cognitive remediation in schizophrenia: generalization of effects of the training of affect recognition (TAR). Schizophr Bull 37(Suppl 2):S63–S70

    Article  PubMed  PubMed Central  Google Scholar 

  21. Russell TA, Chu E, Phillips ML (2006) A pilot study to investigate the effectiveness of emotion recognition remediation in schizophrenia using the micro-expression training tool. Br J Clin Psychol 45(Pt 4):579–583

    Article  PubMed  Google Scholar 

  22. Statucka M, Walder DJ (2013) Efficacy of social cognition remediation programs targeting facial affect recognition deficits in schizophrenia: a review and consideration of high-risk samples and sex differences. Psychiatry Res 206(2–3):125–139

    Article  PubMed  Google Scholar 

  23. Barkl SJ et al (2014) Facial emotion identification in early-onset psychosis. Schizophr Res 160(1–3):150–156

    Article  PubMed  Google Scholar 

  24. Ventura J et al (2013) Neurocognition and symptoms identify links between facial recognition and emotion processing in schizophrenia: meta-analytic findings. Schizophr Res 151(1–3):78–84

    Article  PubMed  PubMed Central  Google Scholar 

  25. Loughland CM, Williams L, Gordon E (2002) Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample. Schizophr Res 55(1–2):159–170

    Article  PubMed  Google Scholar 

  26. Loughland CM, Williams L, Gordon E (2002) Schizophrenia and affective disorder show different visual scanning behavior for faces: a trait versus state-based distinction? Biol Psychiatry 52(4):338–348

    Article  PubMed  Google Scholar 

  27. Loughland CM, Williams L, Harris AW (2004) Visual scanpath dysfunction in first-degree relatives of schizophrenia probands: evidence for a vulnerability marker? Schizophr Res 67(1):11–21

    Article  PubMed  Google Scholar 

  28. McCabe K et al (2007) Remediation of facial affect decoding and visual scanpath deficits in schizophrenia. Schizophr Bull 33(2):531–532

    Google Scholar 

  29. Morris RW, Weickert CS, Loughland CM (2009) Emotional face processing in schizophrenia. Curr Opin Psychiatry 22(2):140–146

    Article  PubMed  Google Scholar 

  30. Williams L et al (2003) Emotion perception in schizophrenia: an eye movement study comparing the effectiveness of risperidone vs. haloperdiol. Psychiatry Res 120(1):13–27

    Article  CAS  PubMed  Google Scholar 

  31. Williams LM et al (1999) Visual scanpaths in schizophrenia: is there a deficit in face recognition? Schizophr Res 40(3):189–199

    Article  CAS  PubMed  Google Scholar 

  32. Bestelmeyer PEG et al (2006) Global visual scanning abnormalities in schizophrenia and bipolar disorder. Schizophr Res 87(1–3):212–222

    Article  PubMed  Google Scholar 

  33. Phillips ML, David AS (1994) Understanding the symptoms of schizophrenia using visual scan paths. Br J Psychiatry 165(5):673–675

    Article  CAS  PubMed  Google Scholar 

  34. Phillips ML, Senior C, David AS (2000) Perception of threat in schizophrenics with persecutory delusions: an investigation using visual scan paths. Psychol Med 30:157–167

    Article  CAS  PubMed  Google Scholar 

  35. Phillips ML et al (1999) A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics. Psychiatry Res-Neuroimaging 92(1):11–31

    Article  CAS  Google Scholar 

  36. Noton D, Stark L (1971) Scanpaths in saccadic eye movements while viewing and recognizing patterns. Vis Res 11(9):929–942

    Article  CAS  PubMed  Google Scholar 

  37. Noton D, Stark L (1971) Eye movements and visual perception. Sci Am 224(6):35–43

    CAS  PubMed  Google Scholar 

  38. Noton D, Stark L (1971) Scanpaths in eye movements during pattern perception. Science 171(968):308–311

    Article  CAS  PubMed  Google Scholar 

  39. Toh WL, Rossell SL, Castle DJ (2011) Current visual scanpath research: a review of investigations into the psychotic, anxiety, and mood disorders. Compr Psychiatry 52(6):567–579

    Article  PubMed  Google Scholar 

  40. Buttner U, Buttner-Ennever JA (2006) Present concepts of oculomotor organization. Prog Brain Res 151:1–42

    Article  CAS  PubMed  Google Scholar 

  41. Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218–228

    Article  CAS  PubMed  Google Scholar 

  42. Gasper K, Clore GL (2002) Attending to the big picture: mood and global versus local processing of visual information. Psychol Sci 13(1):34–40

    Article  PubMed  Google Scholar 

  43. Granger GW (1953) Personality and visual perception: a review. J Ment Sci 99(414):8–43

    CAS  PubMed  Google Scholar 

  44. Just MA, Carpenter PA (1976) Role of eye-fixation research in cognitive psychology. Behav Res Methods Instrum 8(2):139–143

    Article  Google Scholar 

  45. Just MA, Carpenter PA (1976) Eye fixations and cognitive-processes. Cogn Psychol 8(4):441–480

    Article  Google Scholar 

  46. Henderson JM (1992) Visual attention and eye movement control during reading and picture viewing. In: Rayner K (ed) Eye movements and visual cognition: scene perception and reading. Springer, New York, pp 260–283

    Chapter  Google Scholar 

  47. Meso AI (2012) Eye tracking: a comprehensive guide to methods and measures. Perception 41(10):1286–1287

    Article  Google Scholar 

  48. Beedie SA, Benson PJ, St Clair DM (2011) Atypical scanpaths in schizophrenia: evidence of a trait- or state-dependent phenomenon? J Psychiatry Neurosci 36(3):150–164

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yarbus AL (1961) Eye movements during the examination of complicated objects. Biofizika 6(2):52–56

    PubMed  Google Scholar 

  50. Smilek D et al (2006) Cognitive Ethology and exploring attention in real-world scenes. Brain Res 1080(1):101–119

    Article  CAS  PubMed  Google Scholar 

  51. Smilek D, Dixon MJ, Merikle PM (2006) Revisiting the category effect: the influence of meaning and search strategy on the efficiency of visual search. Brain Res 1080(1):73–90

    Article  CAS  PubMed  Google Scholar 

  52. Birmingham E, Bischof WF, Kingstone A (2008) Gaze selection in complex social scenes. Vis Cognit 16(2–3):341–355

    Article  Google Scholar 

  53. Gordon E et al (1992) Eye-movement response to a facial stimulus in schizophrenia. Biol Psychiatry 31(6):626–629

    Article  CAS  PubMed  Google Scholar 

  54. Sprenger A et al (2013) Advanced analysis of free visual exploration patterns in schizophrenia. Front Psychol 4:737

    Article  PubMed  PubMed Central  Google Scholar 

  55. Freeman D, Garety PA, Phillips ML (2000) An examination of hypervigilance for external threat in individuals with generalized anxiety disorder and individuals with persecutory delusions using visual scan paths. Q J Exp Psychol A 53(2):549–567

    Article  CAS  PubMed  Google Scholar 

  56. Green MJ, Williams LM, Davidson D (2003) Visual scanpaths to threat-related faces in deluded schizophrenia. Psychiatry Res 119(3):271–285

    Article  PubMed  Google Scholar 

  57. Green MJ et al (2008) Visual processing of social context during mental state perception in schizophrenia. J Psychiatry Neurosci 33(1):34–42

    PubMed  PubMed Central  Google Scholar 

  58. Benson PJ et al (2007) Visual scan paths in first-episode schizophrenia and cannabis-induced psychosis. J Psychiatry Neurosci 32(4):267–274

    PubMed  PubMed Central  Google Scholar 

  59. Sasson N et al (2007) Orienting to social stimuli differentiates social cognitive impairment in autism and schizophrenia. Neuropsychologia 45(11):2580–2588

    Article  PubMed  PubMed Central  Google Scholar 

  60. Green MF, Leitman DI (2008) Social cognition in schizophrenia. Schizophr Bull 34(4):670–672

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13(2):261–276

    Article  CAS  PubMed  Google Scholar 

  62. Hall RC (1995) Global assessment of functioning. A modified scale. Psychosomatics 36(3):267–275

    Article  CAS  PubMed  Google Scholar 

  63. Cornblatt BA et al (2007) Preliminary findings for two new measures of social and role functioning in the prodromal phase of schizophrenia. Schizophr Bull 33(3):688–702

    Article  PubMed  PubMed Central  Google Scholar 

  64. APA (2000) Diagnostic and statistical manual of mental disorders: text revision, 4th edn. American Psychiatric Publishing, Arlington

    Google Scholar 

  65. Sheehan D et al (2006) Mini international neuropsychiatric interview (M.I.N.I. PLUS). English version 5.0.0. University of South Florida, Tampa

    Google Scholar 

  66. Lecrubier Y et al (1999) Mini international neuropsychiatric interview (M.I.N.I.) 5.0.0 German version DSM-IV. University of South Florida, Tampa

    Google Scholar 

  67. Cornblatt BA et al (1988) The continuous performance-test, identical pairs version (Cpt-Ip).1. New findings about sustained attention in normal-families. Psychiatry Res 26(2):223–238

    Article  CAS  PubMed  Google Scholar 

  68. Roder V, Brenner HD, Kienzle N (2002) Integriertes psychologisches therapieprogramm für schizophrene patienten. Weinheim, Beltz

    Google Scholar 

  69. Roder V et al (2006) Integrated psychological therapy (IPT) for schizophrenia: is it effective? Schizophr Bull 32(Suppl 1):S81–S93

    Article  PubMed  PubMed Central  Google Scholar 

  70. Mueller DR, Schmidt SJ, Roder V (2015) One-year randomized controlled trial and follow-up of integrated neurocognitive therapy for schizophrenia outpatients. Schizophr Bull 41(3):604–616

    Article  PubMed  PubMed Central  Google Scholar 

  71. Roder V, Mueller DR, Schmidt SJ (2011) Effectiveness of integrated psychological therapy (IPT) for schizophrenia patients: a research update. Schizophr Bull 37(Suppl 2):S71–S79

    Article  PubMed  PubMed Central  Google Scholar 

  72. Manor BR et al (1999) Eye movements reflect impaired face processing in patients with schizophrenia. Biol Psychiatry 46(7):963–969

    Article  CAS  PubMed  Google Scholar 

  73. Loughin TM (1998) On the bootstrap and monotone likelihood in the cox proportional hazards regression model. Lifetime Data Anal 4(4):393–403

    Article  CAS  PubMed  Google Scholar 

  74. Tropsha A, Gramatica P, Gombar VK (2003) The importance of being earnest: validation is the absolute essential for successful application and interpretation of QSPR models. QSAR Comb Sci 22(1):69–77

    Article  CAS  Google Scholar 

  75. Hosmer W, Lemeshow S (eds) (2000) Applied logistic regression, 2nd edn. New York, Wiley

    Google Scholar 

  76. Sheskin DJ (2011) Handbook of parametric and nonparametric statistical procedures, 5th edn. Taylor and Francis Group, New York

    Google Scholar 

  77. Jeffery L, Rhodes G (2011) Insights into the development of face recognition mechanisms revealed by face aftereffects. Br J Psychol 102(4):799–815

    Article  PubMed  Google Scholar 

  78. Pegna AJ et al (2004) Visual recognition of faces, objects, and words using degraded stimuli: where and when it occurs. Hum Brain Mapp 22(4):300–311

    Article  PubMed  Google Scholar 

  79. Bortolon C, Capdevielle D, Raffard S (2015) Face recognition in schizophrenia disorder: a comprehensive review of behavioral, neuroimaging and neurophysiological studies. Neurosci Biobehav Rev 53:79–107

    Article  PubMed  Google Scholar 

  80. Liu L, Ioannides AA (2010) Emotion separation is completed early and it depends on visual field presentation. PLoS One 5(3):e9790

    Article  PubMed  PubMed Central  Google Scholar 

  81. Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Earlbaum, Hillsdale

    Google Scholar 

  82. Birchwood M, Smith J, Cochrane R (1992) Specific and non-specific effects of educational intervention for families living with schizophrenia. A comparison of three methods. Br J Psychiatry 160:806–814

    Article  CAS  PubMed  Google Scholar 

  83. Sergi MJ, Green MF (2003) Social perception and early visual processing in schizophrenia. Schizophr Res 59(2–3):233–241

    Article  PubMed  Google Scholar 

  84. Sergi MJ et al (2007) Social cognition in schizophrenia: relationships with neurocognition and negative symptoms. Schizophr Res 90(1–3):316–324

    Article  PubMed  Google Scholar 

  85. Sergi MJ et al (2006) Social perception as a mediator of the influence of early visual processing on functional status in schizophrenia. Am J Psychiatry 163(3):448–454

    Article  PubMed  Google Scholar 

  86. Kojima T et al (1990) Eye movements in acute, chronic, and remitted schizophrenics. Biol Psychiatry 27(9):975–989

    Article  CAS  PubMed  Google Scholar 

  87. Minassian A et al (2005) Visual scanning deficits in schizophrenia and their relationship to executive functioning impairment. Schizophr Res 74(1):69–79

    Article  PubMed  Google Scholar 

  88. Ryu H et al (2001) Abnormal exploratory eye movements in schizophrenic patients vs healthy subjects. Acta Neurol Scand 104(6):369–376

    Article  CAS  PubMed  Google Scholar 

  89. Gaebel W, Ulrich G, Frick K (1987) Visuomotor performance of schizophrenic patients and normal controls in a picture viewing task. Biol Psychiatry 22(10):1227–1237

    Article  CAS  PubMed  Google Scholar 

  90. Ventura J, Wood RC, Hellemann GS (2013) Symptom domains and neurocognitive functioning can help differentiate social cognitive processes in schizophrenia: a meta-analysis. Schizophr Bull 39(1):102–111

    Article  PubMed  Google Scholar 

  91. Pelphrey KA et al (2002) Visual scanning of faces in autism. J Autism Dev Disord 32(4):249–261

    Article  PubMed  Google Scholar 

  92. Pinkham AE et al (2008) Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders. Schizophr Res 99(1–3):164–175

    Article  PubMed  Google Scholar 

  93. Minnebusch DA, Daum I (2009) Neuropsychological mechanisms of visual face and body perception. Neurosci Biobehav Rev 33(7):1133–1144

    Article  PubMed  Google Scholar 

  94. Taylor JC, Downing PE (2011) Division of labor between lateral and ventral extrastriate representations of faces, bodies, and objects. J Cogn Neurosci 23(12):4122–4137

    Article  PubMed  Google Scholar 

  95. Quintana J et al (2003) Prefrontal-posterior parietal networks in schizophrenia: primary dysfunctions and secondary compensations. Biol Psychiatry 53(1):12–24

    Article  PubMed  Google Scholar 

  96. Seiferth NY et al (2008) Increased neural response related to neutral faces in individuals at risk for psychosis. Neuroimage 40(1):289–297

    Article  PubMed  Google Scholar 

  97. Marwick K, Hall J (2008) Social cognition in schizophrenia: a review of face processing. Br Med Bull 88(1):43–58

    Article  PubMed  Google Scholar 

  98. Hosmer DW et al (1997) A comparison of goodness-of-fit tests for the logistic regression model. Stat Med 16(9):965–980

    Article  CAS  PubMed  Google Scholar 

  99. Sweeney JA et al (1997) Adverse effects of risperidone on eye movement activity: a comparison of risperidone and haloperidol in antipsychotic-naive schizophrenic patients. Neuropsychopharmacology 16(3):217–228

    Article  CAS  PubMed  Google Scholar 

  100. Ruhrmann S et al (2014) Prediction and prevention of psychosis: current progress and future tasks. Eur Arch Psychiatry Clin Neurosci 264(Suppl 1):S9–S16

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by the Deutsche Forschungsgemeinschaft (DFG) (S.R., J.K.; grant number RU859/2-1). We thank all of the study participants and the clinical staff who contributed to this project, Prof. Roder (Bern, Switzerland) and his team for providing us with the IPT stimulus material and Dr. Michael Edmond (Munich, Germany) for language editing.

Author information

Authors and Affiliations

  1. Department of Psychiatry and Psychotherapy, University of Cologne, Kerpener Strasse 62, 50924, Cologne, Germany

    Alexandra Nikolaides, Susanne Miess, Isabella Auvera, Ralf Müller, Joachim Klosterkötter & Stephan Ruhrmann

Authors
  1. Alexandra Nikolaides
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susanne Miess
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabella Auvera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ralf Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joachim Klosterkötter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephan Ruhrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephan Ruhrmann.

Ethics declarations

Conflict of interest

None.

Ethical standards

The study was approved by the ethics committee of the Medical Faculty of the University of Cologne and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 52 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nikolaides, A., Miess, S., Auvera, I. et al. Restricted attention to social cues in schizophrenia patients. Eur Arch Psychiatry Clin Neurosci 266, 649–661 (2016). https://doi.org/10.1007/s00406-016-0705-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00406-016-0705-6

Keywords

Search

Navigation