FACE PROCESSING IN SCHIZOPHRENIA: AN INVESTIGATION OF CONFIGURAL PROCESSING AND THE RELATIONSHIP WITH FACIAL EMOTION PROCESSING AND NEUROCOGNITION Nicole R. Joshua Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy February 2010 The Mental Health Research Institute of Victoria and The Department of Psychiatry, Faculty of Medicine, Dentistry and Health Sciences The University of Melbourne i Abstract Cognitive impairment is a key characteristic of schizophrenia and is a clear predictor of functional outcome. This thesis explores the relationship between cognitive ability relating to social and non-social processing. Schizophrenia patients demonstrate an impaired ability to recognise, label and discriminate emotional expression within the face. The underlying mechanisms behind this social cognitive impairment are not yet fully understood. This thesis explores the notion that a basic perceptual impairment in processing facial information adversely impacts on the perception of more complex information derived from faces, such as emotional expression. Face perception relies on processing the featural characteristics of a face as well as the relationship between these features. Information pertaining to the spatial distances between features is referred to as configural information. A group of schizophrenia patients and healthy control participants completed a battery of tasks that assessed basic neurocognition, facial emotion processing and configural face processing. A model of face processing was proposed and used to systematically pinpoint specific deficits that may contribute to impaired face processing in schizophrenia. The results indicated that schizophrenia patients show impairments on three broad constructs; basic neurocognition, facial emotion processing, and most pertinently, deficits in configural processing. It was revealed that although neurocognitive and face processing both explained a significant proportion of the variance in facial emotion processing, the effect of neurocognition was indirect and mediated by face processing. To investigate the diagnostic specificity of these findings, a group of bipolar disorder patients was also tested on the task battery. The results indicated that bipolar disorder patients also show social and non-social cognitive impairments, however, not as severe as that demonstrated by the schizophrenia patients. Furthermore, the effect of neurocognitive performance on facial emotion processing appeared more direct for bipolar disorder patients compared to schizophrenia patients. Although deficits in face processing were observable in bipolar, they were not specific to configural processing. Thus, deficits in emotion processing were more associated to neurocognitive ability in bipolar disorder patients, and more associated to configural face processing in schizophrenia patients. The configural processing deficits in schizophrenia are discussed as a lower-order perception problem. In conclusion, the results of this thesis are discussed in terms of their implication for treatment. ii Declaration This is to certify that: a) This thesis comprises only my original work toward the PhD unless otherwise indicated b) Due acknowledgment has been made in the text to all other material used c) The thesis is less than 100,000 words in length, exclusive of tables, figures, bibliography and appendices ___________________________ Nicole R. Joshua September, 2009 iii Acknowledgements I would like to acknowledge a number of individuals who have helped me complete this research. Some have assisted from the very beginning and others have been influential along the way; many will be well into the future. Firstly, I would like to acknowledge the contribution of my three supervisors; Susan Rossell, Patrick Johnston and David Castle. I thank each of you for your practical assistance and for sharing your expertise in many aspects of this research. You have helped me develop my ideas and formulate methods to test these ideas. You have helped nurture my independence yet have always been available to give advice and encouragement. I would like to express my sincere gratitude to all the participants that took part in this research. Thank you for sharing your experiences and contributing your valuable time. Without your involvement this research would not have been possible. I would like to acknowledge the Mental Health Research Institute for providing the resources and technical support required for this research. Further acknowledgment goes to the University of Melbourne, Department of Psychiatry, specifically Elizabeth Horton-Bell for administrative support and to the Menzies Foundation who provided not only financial support but also a very encouraging, friendly environment. I would like to express my deep thanks and appreciation to Andrea Gogos and David O’Connor. You have both helped me so much along this journey, providing advice and tolerance and most of all friendship. I will always think back and laugh at our crazy centrifuge Friday antics. You are both very talented scientists who will undoubtedly continue to make significant contributions to your chosen areas of research. I am proud to have worked with you both. I would like to thank all my friends of whom there are too many to list but you all know who you are. You have provided essential support and understanding throughout. The many girls nights, aquatic adventures and countless coffees have kept me grounded and happy. iv I would like to give special thanks to Peter Knott who has impacted my life in so many ways. You have supported me through many times of quirk and eek, you have always listened and provided practical, rational and emotional support. Your laid back, level-headed, caring nature has been unquestionably valuable. I thank you for making me so happy and I look forward to the rest of our lives together. Finally, I would like to express the deepest of thanks to my Mum and Dad. You have supported me in every challenge I have taken on with unconditional love and care. You have always been there for me, providing words of wisdom; my candle may be slightly singed at each end but here is my pudding. I hope you are as proud of me as I am to be your daughter. I love you, thank you. v Publications & Presentations During Candidature Refereed journal articles Joshua N., Rossell S., 2009. Configural face processing in schizophrenia. Schizophr Res. 112(1-3), 99-103. Joshua N., Gogos A., Rossell S., 2009. Executive functioning in schizophrenia: A thorough examination of performance on the Hayling Sentence Completion Test compared to psychiatric and non-psychiatric controls. Schizophr Res. 114(1), 84-90. Gogos A., Joshua N., Rossell S., 2009. Using the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) to investigate group and gender differences in schizophrenia and bipolar disorder. Aust N Z J Psychiatry. (Accepted for publication 21/09/2009 awaiting DOI). Manuscripts in preparation Joshua N., Rossell S.L., 2009. Contour integration in chronic Australian schizophrenia outpatients. In preparation. Batty R.A., Joshua N., Rossell S., 2009. Does the N170 indicate phases of encoding in face perception? In preparation. Batty R.A., Rossell S.L., Innes-Brown H., Joshua N.R., Francis A.J.P., 2009. Neurophysiological correlates of face processing in schizotypy: Impoverished visual input or an isolated configural processing deficit? In preparation. Stefanovic A., Roiser J.P., Joshua N.R., Neill E., O'Regan A., Morgan C.J.A., Curran V., Rossell S.L., 2009. Modulated prefrontal BOLD response during a semantic priming task is associated with delusions in schizophrenia. Molecular Psychiatry. Under review. Oral presentations Configural Face Processing in Schizophrenia. North West Area Mental Health / Department of Psychiatry Colloquium. Melbourne, Australia (July, 2009). Configural Face Processing in Schizophrenia. Joint WPA/ASPR Scientific Meeting. Melbourne, Australia (December, 2007). Confirmation of Candidature Proposed Research Presentation. The University of Melbourne. Melbourne, Australia (January, 2006). Understanding Perceptual Organisation in Psychosis. Joint CINP/ASPR Scientific Meeting. Brisbane, Australia (December, 2005). Poster presentations National Joshua, N. & Rossell, S. Emotion Processing in Schizophrenia: What does the whole face tell us the eyes cannot? ASPR Scientific Meeting. Newcastle, Australia (2008). Joshua, N., O'Regan, A. & Rossell, S. Perceptual Organisation in Schizophrenia. Melbourne Health Research Week. Melbourne, Australia (2007). Joshua, N., O'Regan, A. & Rossell, S. Facial Emotion Processing in Psychosis. ASPR Scientific Meeting. Sydney, Australia (2006). O'Regan, A., Joshua, N., & Rossell, S. Are Affective Prosodic Deficits Evident in Bipolar Disorder? ASPR Scientific Meeting. Sydney, Australia (2006). McPhee, A., Joshua, N. & Rossell, S. Biased Perception Towards Fearful Words in Delusions. Joint CINP/ASPR Scientific Meeting. Brisbane, Australia (2005). Joshua, N. The Effects of 24 Hours of Sleep Deprivation on Task Performance. Australasian Society for Psychophysiology Annual Meeting. Melbourne, Australia (2004). International Configural Face Processing in Schizophrenia. Schizophrenia International Research Society. Venice, Italy (June, 2008). Joshua, N. & Rossell, S. Automatic and Controlled Emotion Processing: Preliminary Data. International Brain Research Organisation. Melbourne, Australia (July, 2007). vi Foreword I have been fascinated by the human brain since my first psychology class. The more I learnt about cortical functioning the more I realised how such a complex system is vulnerable to fault. Aberrant cognitive processing can lead to poor memory, planning, and attention for example. To me however, the social implications of cognitive error are just as, if not more debilitating to an individual. During many clinical interviews with schizophrenia patients this became particularly apparent. During interviews I asked questions such as "do you have any regrets in life?" and "what are your hopes for the future?". A recurring theme I observed was the need for closer social contacts and the desire to make more friends. This led me to an interest in social cognition in schizophrenia and a desire to understand not only why social skills are problematic for patients but also how they can be improved. This body of work is a collection of studies investigating social cognition in schizophrenia. vii Table of Contents Abstract---------------------------------------------------------------------------------------------------ii Declaration----------------------------------------------------------------------------------------------iii Acknowledgements------------------------------------------------------------------------------------ iv Publications & Presentations During Candidature---------------------------------------------- vi Foreword ------------------------------------------------------------------------------------------------vii Table of Contents-------------------------------------------------------------------------------------viii List of Figures-----------------------------------------------------------------------------------------xiii List of Tables------------------------------------------------------------------------------------------xiv List of Abbreviations----------------------------------------------------------------------------------xv Chapter 1 Introduction----------------------------------------------------------------------------- 1 1.1 Introduction to Schizophrenia--------------------------------------------------------------------1 1.2 The Costs of Schizophrenia-----------------------------------------------------------------------3 1.3 Cognition in Schizophrenia-----------------------------------------------------------------------3 1.4 Overall Aims & Hypotheses----------------------------------------------------------------------6 1.5 Study Questions-------------------------------------------------------------------------------------6 1.6 Significance of this Research----------------------------------------------------------------------7 1.7 Outline and Organisation of Thesis-------------------------------------------------------------7 Chapter 2 Methods---------------------------------------------------------------------------------- 9 2.1 Participant Information----------------------------------------------------------------------------9 2.1.1 Recruitment, Diagnosis & Inclusion Criteria---------------------------------------------9 2.1.2 Demographic Characteristics --------------------------------------------------------------10 2.1.3 Estimated Intelligence-----------------------------------------------------------------------10 2.1.4 Education-------------------------------------------------------------------------------------11 2.1.5 Employment----------------------------------------------------------------------------------11 2.1.6 Living Situation ------------------------------------------------------------------------------11 2.1.7 Mood Assessment ---------------------------------------------------------------------------11 2.1.8 Psychopathological Characteristics--------------------------------------------------------12 2.1.9 Global Assessment of Functioning-------------------------------------------------------13 2.1.10 Medication------------------------------------------------------------------------------------14 viii 2.2 Procedure, Testing Conditions and Apparatus -----------------------------------------------14 2.3 Task Battery ----------------------------------------------------------------------------------------15 2.4 Statistical Analysis ---------------------------------------------------------------------------------15 2.5 Summary--------------------------------------------------------------------------------------------18 Chapter 3 Neurocognition in Schizophrenia--------------------------------------------------19 3.1 Introduction----------------------------------------------------------------------------------------19 3.1.1 Background to Neurocognition in Schizophrenia--------------------------------------19 3.1.2 Memory----------------------------------------------------------------------------------------20 3.1.3 Visuospatial Ability--------------------------------------------------------------------------21 3.1.4 Language--------------------------------------------------------------------------------------22 3.1.5 Information Processing & Attention-----------------------------------------------------22 3.1.6 Executive Functioning----------------------------------------------------------------------23 3.2 Aims & Hypotheses-------------------------------------------------------------------------------24 3.3 Neurocognitive Tasks & Performance Results -----------------------------------------------25 3.3.1 Repeatable Battery for the Assessment of Neuropsychological Status (RBANS)-26 3.3.2 Zoo Map --------------------------------------------------------------------------------------33 3.3.3 Hayling Sentence Completion Test (HSCT)---------------------------------------------35 3.3.4 The Brixton Spatial Anticipation Test (Brixton Test)----------------------------------38 3.4 Neurocognitive Strengths & Weaknesses in Schizophrenia --------------------------------40 3.5 Discussion ------------------------------------------------------------------------------------------43 3.5.1 Limitations------------------------------------------------------------------------------------44 3.5.2 Implications of Impaired Neurocognition in Schizophrenia--------------------------44 3.5.3 Neurocognition & Social Cognition------------------------------------------------------45 3.6 Summary--------------------------------------------------------------------------------------------47 Chapter 4 Emotion Processing in Schizophrenia --------------------------------------------49 4.1 Background to Social Cognition ----------------------------------------------------------------49 4.1.1 Social Cognition in Schizophrenia --------------------------------------------------------50 4.2 Background to Facial Emotion Processing----------------------------------------------------53 4.3 Facial Emotion Processing in Schizophrenia--------------------------------------------------55 4.3.1 Emotion Processing and Stage of Illness ------------------------------------------------56 4.3.2 Emotion Processing in At-Risk Populations--------------------------------------------56 4.3.3 Associations between Emotion Processing and Clinical Characteristics------------57 4.3.4 Emotion Processing and Neurocognition-----------------------------------------------58 ix 4.3.5 Emotion Processing and Functional Outcome-----------------------------------------58 4.3.6 Assessment Methods of Emotion Processing in Schizophrenia---------------------59 4.3.7 Generalized or Emotion Specific Deficit?-----------------------------------------------61 4.3.8 Limitations of Previous Literature--------------------------------------------------------63 4.4 Aims & Hypotheses-------------------------------------------------------------------------------64 4.5 Task Methodology---------------------------------------------------------------------------------65 4.5.1 Facial Emotion Discrimination Task-----------------------------------------------------65 4.5.2 Facial Emotion Labelling Task------------------------------------------------------------66 4.6 Results-----------------------------------------------------------------------------------------------66 4.6.1 Facial Emotion Discrimination------------------------------------------------------------67 4.6.2 Facial Emotion Labelling-------------------------------------------------------------------69 4.6.3 Between-Task Correlations-----------------------------------------------------------------72 4.7 Discussion ------------------------------------------------------------------------------------------72 4.7.1 Limitations------------------------------------------------------------------------------------76 4.7.2 Treatment Implications---------------------------------------------------------------------77 4.8 Summary--------------------------------------------------------------------------------------------78 Chapter 5 Face Processing in Schizophrenia--------------------------------------------------81 5.1 Background to Face Processing-----------------------------------------------------------------82 5.1.1 History of Face Processing Research-----------------------------------------------------83 5.1.2 Featural Face Processing--------------------------------------------------------------------84 5.1.3 The Face Inversion Effect------------------------------------------------------------------86 5.1.4 Configural Face Processing ----------------------------------------------------------------88 5.1.5 Development of Configural Face Processing -------------------------------------------90 5.1.6 Configural Processing and Expertise-----------------------------------------------------92 5.1.7 Neural Basis of Configural Face Processing---------------------------------------------93 5.1.8 Models of Configural Processing----------------------------------------------------------95 5.2 Face Processing in Schizophrenia---------------------------------------------------------------98 5.2.1 Differential Deficit Design-----------------------------------------------------------------99 5.2.2 Configural Face Processing in Schizophrenia-----------------------------------------101 5.3 Aims and Hypotheses---------------------------------------------------------------------------102 5.4 Face Processing Tasks – Methods & Results------------------------------------------------103 5.4.1 Scrambled Faces Task---------------------------------------------------------------------104 5.4.2 Featural-Spacing Manipulation Tasks---------------------------------------------------107 5.4.3 Fractured Face Task-----------------------------------------------------------------------119 x
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