Top

European Archives of Psychiatry and Clinical Neuroscience

Published in:

01-10-2016 | Original Paper

Restricted attention to social cues in schizophrenia patients

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

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 7/2016

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.

Available only for authorised users

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

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):805–822PubMedCrossRef

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

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

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):882–887PubMedCrossRef

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

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):865–872PubMedCrossRef

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):281–298PubMedCrossRef

Couture SM, Penn DL, Roberts DL (2006) The functional significance of social cognition in schizophrenia: a review. Schizophr Bull 32(Suppl 1):S44–S63PubMedPubMedCentralCrossRef

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):573–588PubMedCrossRef

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–S54PubMedPubMedCentralCrossRef

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):17–23PubMedPubMedCentralCrossRef

13.

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

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):56–62PubMedCrossRef

15.

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

16.

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

17.

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

18.

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

19.

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

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–S70PubMedPubMedCentralCrossRef

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):579–583PubMedCrossRef

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):125–139PubMedCrossRef

23.

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

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):78–84PubMedPubMedCentralCrossRef

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):159–170PubMedCrossRef

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):338–348PubMedCrossRef

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):11–21PubMedCrossRef

28.

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

29.

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

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):13–27PubMedCrossRef

31.

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

32.

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

33.

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

34.

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

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):11–31CrossRef

36.

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

37.

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

38.

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

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):567–579PubMedCrossRef

40.

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

41.

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

42.

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

43.

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

44.

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

45.

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

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 260–283CrossRef

47.

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

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):150–164PubMedPubMedCentralCrossRef

49.

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

50.

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

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):73–90PubMedCrossRef

52.

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

53.

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

54.

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

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):549–567PubMedCrossRef

56.

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

57.

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

58.

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

59.

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

60.

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

61.

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

62.

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

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):688–702PubMedPubMedCentralCrossRef

64.

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

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

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

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):223–238PubMedCrossRef

68.

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

69.

Roder V et al (2006) Integrated psychological therapy (IPT) for schizophrenia: is it effective? Schizophr Bull 32(Suppl 1):S81–S93PubMedPubMedCentralCrossRef

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):604–616PubMedPubMedCentralCrossRef

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–S79PubMedPubMedCentralCrossRef

72.

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

73.

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

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):69–77CrossRef

75.

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

76.

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

77.

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

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):300–311PubMedCrossRef

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 53:79–107PubMedCrossRef

80.

Liu L, Ioannides AA (2010) Emotion separation is completed early and it depends on visual field presentation. PLoS One 5(3):e9790PubMedPubMedCentralCrossRef

81.

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

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 160:806–814PubMedCrossRef

83.

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

84.

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

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):448–454PubMedCrossRef

86.

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

87.

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

88.

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

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):1227–1237PubMedCrossRef

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):102–111PubMedCrossRef

91.

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

92.

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

93.

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

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):4122–4137PubMedCrossRef

95.

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

96.

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

97.

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

98.

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

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):217–228PubMedCrossRef

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–S16PubMedCrossRef

Title: Restricted attention to social cues in schizophrenia patients
Authors: Alexandra Nikolaides
Susanne Miess
Isabella Auvera
Ralf Müller
Joachim Klosterkötter
Stephan Ruhrmann
Publication date: 01-10-2016
Publisher: Springer Berlin Heidelberg
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 7/2016
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-016-0705-6

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Restricted attention to social cues in schizophrenia patients

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2016

Inverse effect of the APOE epsilon4 allele in late- and early-onset Alzheimer’s disease

Searching biomarkers for mental disorders—lessons from Alzheimer’s disease

Diagnosis and neurocognitive profiles in first-episode non-affective psychosis patients

Minocycline exacerbates apoptotic neurodegeneration induced by the NMDA receptor antagonist MK-801 in the early postnatal mouse brain

Lithium activates brain phospholipase A2 and improves memory in rats: implications for Alzheimer’s disease

Using the cognitive assessment interview to screen cognitive impairment in psychosis