Assessing early processing of eye gaze in schizophrenia: measuring the cone of direct gaze and reflexive orienting of attention

ABSTRACT Introduction: The accurate discrimination of another person’s eye-gaze direction is vital as it provides a cue to the gazer’s focus of attention, which in turn supports joint attention. Patients with schizophrenia have shown a “direct gaze bias” when judging gaze direction. However, current tasks do not dissociate an early perceptual bias from high-level top-down effects. We investigated early stages of gaze processing in schizophrenia by measuring perceptual sensitivity to fine deviations in gaze direction (i.e., the cone of direct gaze: CoDG) and ability to reflexively orient to locations cued by the same deviations. Methods: Twenty-four patients and 26 controls completed a CoDG discrimination task that used realistic direct-face images with six fine degrees of deviation (i.e., 3, 6 or 9 pixels to the left and right) and direct gaze, and a gaze cueing task that assessed reflexive orienting to the same fine-grained deviations. Results: Our data showed patients exhibited no impairment in gaze discrimination, nor did we observe a reduced orienting response. Conclusions: These results suggest that while patients may suffer deficits associated with interpreting another person’s gaze, the earliest processes concerned with detecting averted gaze and reflexively orienting to the gazed-at location are intact.

[1]  Nancy C. Andreasen,et al.  Scale for the Assessment of Positive Symptoms , 2018 .

[2]  P. Ward,et al.  Automatic attentional orienting to other people's gaze in schizophrenia , 2017, Quarterly journal of experimental psychology.

[3]  G. Rhodes,et al.  Intact unconscious processing of eye contact in schizophrenia , 2015, Schizophrenia Research: Cognition.

[4]  Michael F. Green,et al.  Social cognition in schizophrenia , 2015, Nature Reviews Neuroscience.

[5]  Andrew N Meltzoff,et al.  Connecting the dots from infancy to childhood: a longitudinal study connecting gaze following, language, and explicit theory of mind. , 2015, Journal of experimental child psychology.

[6]  B. Gallhofer,et al.  Hemodynamic Response Pattern of Spatial Cueing is Different for Social and Symbolic Cues , 2014, Front. Hum. Neurosci..

[7]  N. Andreasen Scale for the Assessment of Negative Symptoms , 2014 .

[8]  T. Kircher,et al.  Superior temporal sulcus disconnectivity during processing of metaphoric gestures in schizophrenia. , 2014, Schizophrenia bulletin.

[9]  Dirk Kerzel,et al.  Lack of automatic attentional orienting by gaze cues following a bilateral loss of visual cortex , 2014, Neuropsychologia.

[10]  Katharine N. Thakkar,et al.  Altered brain activation during action imitation and observation in schizophrenia: a translational approach to investigating social dysfunction in schizophrenia. , 2014, The American journal of psychiatry.

[11]  Giovanni Galfano,et al.  Is social attention impaired in schizophrenia? Gaze, but not pointing gestures, is associated with spatial attention deficits. , 2013, Neuropsychology.

[12]  Johan D. Carlin,et al.  The neural basis of eye gaze processing , 2013, Current Opinion in Neurobiology.

[13]  Isabelle Mareschal,et al.  Humans Have an Expectation That Gaze Is Directed Toward Them , 2013, Current Biology.

[14]  Jennifer A. Walsh,et al.  The Influences of Face Inversion and Facial Expression on Sensitivity to Eye Contact in High-Functioning Adults with Autism Spectrum Disorders , 2013, Journal of autism and developmental disorders.

[15]  G. Rhodes,et al.  Facial Expressions of Threat Influence Perceived Gaze Direction in 8 Year-Olds , 2012, PloS one.

[16]  G. Galfano,et al.  Social status gates social attention in humans , 2012, Biology Letters.

[17]  J. Lagopoulos,et al.  Mentalizing impairment in schizophrenia: A functional MRI study , 2012, Schizophrenia Research.

[18]  Matthew Finkbeiner,et al.  Effective processing of masked eye gaze requires volitional control , 2012, Experimental Brain Research.

[19]  P. Deldin,et al.  Eye-contact perception in schizophrenia: relationship with symptoms and socioemotional functioning. , 2012, Journal of abnormal psychology.

[20]  Johan D. Carlin,et al.  A Head View-Invariant Representation of Gaze Direction in Anterior Superior Temporal Sulcus , 2011, Current Biology.

[21]  Giovanni Galfano,et al.  Racial Group Membership Is Associated to Gaze-Mediated Orienting in Italy , 2011, PloS one.

[22]  Claire K. Naughtin,et al.  A direct link between gaze perception and social attention. , 2011, Journal of experimental psychology. Human perception and performance.

[23]  Randolph Blake,et al.  Perception of Biological Motion in Schizophrenia and Healthy Individuals: A Behavioral and fMRI Study , 2011, PloS one.

[24]  R. Kahn,et al.  More prolonged brain activity related to gaze cueing in schizophrenia , 2011, Clinical Neurophysiology.

[25]  A. Calder,et al.  “You Talkin’ to Me?” , 2010, Psychological science.

[26]  Andrew D. Engell,et al.  Differential activation of frontoparietal attention networks by social and symbolic spatial cues , 2010, Social cognitive and affective neuroscience.

[27]  A. Calder,et al.  Why are you angry with me? Facial expressions of threat influence perception of gaze direction. , 2009, Journal of vision.

[28]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[29]  Ulrich Schall,et al.  Australian Schizophrenia Research Bank: A Database of Comprehensive Clinical, Endophenotypic and Genetic Data for Aetiological Studies of Schizophrenia , 2009, The Australian and New Zealand journal of psychiatry.

[30]  R. Badgaiyan Theory of mind and schizophrenia , 2009, Consciousness and Cognition.

[31]  A. Kingstone Taking a real look at social attention , 2009, Current Opinion in Neurobiology.

[32]  H. Kashima,et al.  Gaze-triggered orienting is reduced in chronic schizophrenia , 2008, Psychiatry Research.

[33]  Wataru Sato,et al.  Attentional shift by gaze is triggered without awareness , 2007, Experimental Brain Research.

[34]  S. Tipper,et al.  Gaze cueing of attention: visual attention, social cognition, and individual differences. , 2007, Psychological bulletin.

[35]  R. Dolan,et al.  Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule , 2007, Current Biology.

[36]  M. Coltheart,et al.  Attentional orienting triggered by gaze in schizophrenia , 2006, Neuropsychologia.

[37]  Riitta Parkkola,et al.  Automatic attention orienting by social and symbolic cues activates different neural networks: An fMRI study , 2006, NeuroImage.

[38]  A. David,et al.  Are semantic deficits in schizophrenia due to problems with access or storage? , 2006, Schizophrenia Research.

[39]  Sohee Park,et al.  You must be looking at me: The nature of gaze perception in schizophrenia patients , 2005, Cognitive neuropsychiatry.

[40]  G. Valuri,et al.  The diagnostic interview for psychoses (DIP): development, reliability and applications , 2005, Psychological Medicine.

[41]  Andrew P Bayliss,et al.  Orienting of attention via observed eye gaze is head-centred , 2004, Cognition.

[42]  Alan Kingstone,et al.  The eyes have it!: An fMRI investigation , 2004, Brain and Cognition.

[43]  Melissa J. Green,et al.  Social threat perception and the evolution of paranoia , 2004, Neuroscience & Biobehavioral Reviews.

[44]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[45]  A. Kingstone,et al.  Are eyes special? It depends on how you look at it , 2002, Psychonomic bulletin & review.

[46]  G. Tiberghien,et al.  Gaze direction determination in schizophrenia , 2002, Schizophrenia Research.

[47]  M J Brammer,et al.  Exploring the social brain in schizophrenia: left prefrontal underactivation during mental state attribution. , 2000, The American journal of psychiatry.

[48]  L. Jones,et al.  Impaired eye expression recognition in schizophrenia. , 2000, Journal of psychiatric research.

[49]  J. Hietanen Does your gaze direction and head orientation shift my visual attention? , 1999, Neuroreport.

[50]  S. Baron-Cohen,et al.  Gaze Perception Triggers Reflexive Visuospatial Orienting , 1999 .

[51]  F. Michèl,et al.  Gaze discrimination is unimpaired in schizophrenia , 1998, Psychiatry Research.

[52]  A. Kingstone,et al.  The eyes have it! Reflexive orienting is triggered by nonpredictive gaze , 1998 .

[53]  Jon Driver,et al.  Adult's Eyes Trigger Shifts of Visual Attention in Human Infants , 1998 .

[54]  M. Phillips,et al.  Visual scan paths are abnormal in deluded schizophrenics , 1997, Neuropsychologia.

[55]  P. Mundy,et al.  Joint Attention and Early Social Communication: Implications for Research on Intervention with Autism , 1997, Journal of Autism and Developmental Disorders.

[56]  D. Povinelli,et al.  Mindblindness. An Essay on Autism and Theory of Mind Simon Baron-Cohen 1995 , 1996, Trends in Neurosciences.

[57]  M. Argyle,et al.  Gaze and Mutual Gaze , 1994, British Journal of Psychiatry.

[58]  R. Wyatt,et al.  Gaze discrimination in patients with schizophrenia: preliminary report. , 1994, The American journal of psychiatry.

[59]  N. Andreasen The Scale for the Assessment of Negative Symptoms (SANS): Conceptual and Theoretical Foundations , 1989, British Journal of Psychiatry.

[60]  A. J. Mistlin,et al.  Visual cells in the temporal cortex sensitive to face view and gaze direction , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[61]  M. Coltheart,et al.  Understanding minds and understanding communicated meanings in schizophrenia , 2002 .

[62]  M. Radcliffe You talkin' to me? , 2001, Nursing times.

[63]  Michael Morales,et al.  Following the direction of gaze and language development in 6-month-olds , 1998 .

[64]  R P Bentall,et al.  Social cognition in schizophrenia. , 1997, Psychological bulletin.

[65]  C. Moore,et al.  Joint attention : its origins and role in development , 1995 .

[66]  A. Kendon Some functions of gaze-direction in social interaction. , 1967, Acta psychologica.