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Salience Attribution in Addiction and Psychosis

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Salience Attribution in Addiction and Psychosis Salience Attribution in Addiction and Psychosis Tom Parsons Freeman Submitted for the degree of Doctor of Philosophy University College London December 2012 1 I, Tom P Freeman confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. …………………… 2 Abstract Salience attribution, the process by which particular stimuli come to selectively grab one’s attention, is heightened towards drug-associated cues in substance users and irrelevant cues in psychosis. In Chapter 1 I review this literature. Despite their theoretical link and the substantial co-morbidity of substance use in psychotic disorders, the extent to which these processes overlap is not well understood. The aim of this thesis was to investigate their relationship. The ability of drug cues to impact on associative learning processes was examined in Chapter 2 using a newly developed task. Overshadowing by drug cues was found alongside smoking-related attentional bias in abstinent smokers but not in satiated smokers or controls. This overshadowing effect is replicated in Chapter 3 among frequent ketamine users and polydrug-using controls. Ketamine users showed elevated psychotic-like symptoms, a reduction in associative blocking and a stronger impact of drug cues on blocking compared to polydrug controls. These results are indicative of a shared disruption of salience attribution in addiction and psychosis, which I investigated in Chapter 4 among smokers with a diagnosis of schizophrenia. Associative blocking was reduced in these individuals compared to control smokers but both groups displayed an absence of blocking towards drug cues. The patient group also showed higher drug-cue attentional bias that correlated with positive psychotic symptoms. In Chapter 5 I examined the role of dopamine in salience attribution in smokers. The dopamine D2/D3 agonist pramipexole (0.5mg) reduced urges to smoke and decreased attentional bias towards smoking-related images relative to monetary images when compared to placebo. In Chapter 6 I discuss the theoretical and clinical implications of these findings. The effects of drug cues on associative learning provide a methodological advance, and these findings offer preliminary support for a link between disruptions of salience attribution in addiction and in psychosis. 3 Acknowledgements I would like give the warmest thanks to my supervisor Val Curran for her continued support along every step of the journey. I feel incredibly lucky to have had her expert guidance during this time and look forward to working with her in the future. Val is one of the kindest people I know and takes a genuine interest in helping the people around her develop and progress. She creates a research environment that is welcoming, enriching, challenging and diverse. I couldn’t have asked for anything better than this. I would also like to give a special mention to Celia Morgan. Celia’s work has been an inspiration and her creativity, determination and hardiness to any challenge never ceases to amaze me. It has been a pleasure to collaborate with James Stone, Tom Beesley, Ravi Das and Sunjeev Kamboj. I would like to thank Jon Roiser, Peter Dayan, Quentin Huys, Oliver Mason and David Shanks for valuable discussions and Sharinjeet Dhiman, Louise Noronha, Beatriz Orgaz, Chandni Hindocha, Fiona Pepper, Stephanie Minchin and Brigitta Brander, Jiye Shen, Billy Schmidt, Leah Markwick and Hannah Powles for their help with this work. I am hoping to escape the PhD office alive following James Bisby and Lorna Stewart. To all those that made it out, all those that didn’t and others who’s time will come (James Harris, Fabi Lorencatto, Chia-Ying Chou, Alice Anokhina, Ravi Das; also Mike Down, John Weymer, Becky Chamberlain) thanks for being great company! I would like to thank my family (Pam and Pete Freeman, Jeremy Parsons) for personal and academic sustenance (Parsons, 2012) and finally my partner Abigail Moss who has done an incredible job of putting up with me over the past three years. Her encouragement has been unconditional and I am very grateful for this. 4 The work presented in this thesis has given rise to the following publications: Freeman, T. P., Morgan, C. J. A., Beesley, T., & Curran, H. V. (2012). Drug cue induced overshadowing: selective disruption of natural reward processing by cigarette cues amongst abstinent but not satiated smokers. Psychological medicine, 42(1), 161. Freeman, T. P., Morgan, C. J., Pepper, F., Howes, O. D., Stone, J. M., & Curran, H. V. (2012). Associative blocking to reward-predicting cues is attenuated in ketamine users but can be modulated by images associated with drug use. Psychopharmacology, doi:10.1007/s00213-012-2791-0 Freeman, T. P., Morgan, C. J., Brandner, B., Almahadi, B., & Curran, H. V. (2012). Dopaminergic involvement in effort-based but not impulsive reward processing in smokers. Drug and Alcohol Dependence. doi: 10.1016/j.drugalcdep.2012.10.016. 5 Preface: a salient personal experience In February 2012 a friend of mine kindly offered to service and replace all of the parts on my bike as a birthday present. The finished job was impressive but included some unsavoury looking bright red tyres. Unfortunately the bike was stolen with chain cutters after just one ride! I wasn’t very happy about this, and after the event I constantly found my attention being drawn towards similar looking bikes on the road. Given the size of London, it is incredible that one day I did actually spot the bike. I was with friends and we challenged the man riding the bike, and took a photo (see below). The salience of my bike may have led to it being stolen, but also might have helped me get it back. I finally got the bike back in June after a long-winded police process. Luckily, I no longer find that my attention is directed towards red bike tyres. 6 Contents Abstract 3 Acknowledgements 4 Preface: a salient personal experience 6 Contents 7 List of tables 10 List of figures 11 1 Chapter 1: Introduction to salience attribution in addiction and psychosis 13 1.1 Background 13 1.2 What is salience? 15 1.3 Attentional bias and aberrant salience attribution in drug users 22 1.4 Beyond attentional bias 27 1.5 Salience attribution in psychosis 31 1.6 Salience attribution and comorbid substance abuse and psychosis 40 1.7 Aims of this thesis 49 1.7.1 Research questions and hypotheses 49 1.7.2 Methodological aims 50 2 Chapter 2: Salience attribution and associative learning in smokers 52 2.1 Introduction 52 2.2 Methods 54 2.2.1 Design and participants 54 2.2.2 Assessments 54 2.2.3 Procedure 60 2.2.4 Statistical analysis 60 2.3 Results 62 7 2.4 Discussion 70 3 Chapter 3: Salience attribution in ketamine users with symptoms of dependence and subclinical delusional beliefs 75 3.1 Introduction 75 3.2 Methods 78 3.2.1 Design and participants 78 3.2.2 Assessments 78 3.2.3 Procedure 80 3.2.4 Statistical analysis 81 3.3 Results 82 3.4 Discussion 90 4 Chapter 4: Salience attribution in smokers with a diagnosis of schizophrenia 96 4.1 Introduction 96 4.2 Methods 98 4.2.1 Design and participants 98 4.2.2 Assessments 98 4.2.3 Procedure 102 4.2.4 Statistical analysis 103 4.3 Results 104 4.4 Discussion 115 5 Chapter 5: The role of dopamine in salience attribution in smokers 120 5.1 Introduction 120 5.2 Methods 123 5.2.1 Design and participants 123 8 5.2.2 Assessments 123 5.2.3 Procedure 126 5.2.4 Preparation of eye movement and manual RT data 127 5.2.5 Statistical analysis 128 5.3 Results 129 5.4 Discussion 139 6 Chapter 6: General discussion 145 6.1 Summary of findings 146 6.2 All that glitters is not gold (or ketamine): associative learning processes in addiction 149 6.3 A common role for salience attribution in substance use and psychosis? 156 6.4 Salient regrets 166 6.5 If it’s not about blocking, don’t come knocking 168 Postscript: overshadowing by doctoral research 171 References 172 Appendices 207 9 List of tables Table 2.1: Design of the DCRPET 57 Table 2.2: Smoking behaviour and group demographics 63 Table 2.3: Accurcy and importance scores from the test stage of the DCRPET 66 Table 2.4: Attentional bias on the dot probe task 69 Table 3.1: Design of the DCRPET 79 Table 3.2: Demographic data, psychosis-like symptoms and other drug use in controls and ketamine users 83 Table 3.3: Accuracy and importance scores from the test stage of the DCRPET 86 Table 4.1 Design of the DCRPET short version 100 Table 4.2: Demographics, smoking behavior and symptom scores 105 Table 4.3: Accuracy and importance scores from the DCRPET-short. 110 Table 5.1: Behavioural data from the visual probe and picture rating tasks 132 Table 5.2: Test data from the DCRPET-short 134 Table 5.3: Mood and physical symptoms, smoking urges and tobacco craving 137 10 List of figures Figure 1.1: The incentive-sensitization theory 16 Figure 1.2: An illustration of ‘overshadowing’ 19 Figure 1.3: A demonstration of ‘blocking’ 20 Figure 1.4: An example of ‘latent inhibition’ 21 Figure 1.5 A neuropsychopharmacological model of drug addiction 24 Figure 1.6: Indexing biases in visual selective attention 30 Figure 1.7: A model of aberrant salience in psychosis 32 Figure 1.8: The role of latent inhibition and blocking in psychosis 37 Figure 1.9: The role of dopamine in salience attribution in comorbid psychosis and substance abuse 44 Figure 2.1: trial structure of the DCRPET 56 Figure 2.2: Learning cue-outcome contingencies during the training stages of the DCRPET.
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