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An Investigation of the Acute and Chronic Effects of Ketamine on Cognition

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An Investigation of the Acute and Chronic Effects of Ketamine on Cognition An Investigation of the Acute and Chronic Effects of Ketamine on Cognition Celia J.A. Morgan University College London Submitted for the degree of Doctor of Philosophy University of London May 2005 l UMI Number: U593077 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U593077 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 Abstract The work presented in this thesis aimed to investigate the consequences and causes of ketamine abuse and compare them with the acute effects of the drug. Seven experimental chapters report the findings of a total of 9 studies: 5 with ketamine users, 3 administering ketamine to healthy volunteers and 1 with psychosis-prone individuals. Acute studies with volunteers demonstrated ketamine-induced impairments to item recognition, source memory, controlled semantic processing, working memory and procedural learning. There was also a suggestion of a disruption in self-monitoring but perceptual priming and executive functioning were largely preserved. Ketamine was subjectively reinforcing in healthy volunteers. Suggested chronic effects of ketamine in drug users included deficits in source memory and controlled semantic processing indicative of a degraded semantic store. Following substantial reduction in ketamine use, semantic function appeared to recover whilst episodic and attentional impairments appeared persistent. Overall, this thesis suggested that ketamine, both acutely and chronically, produces selective cognitive impairments, particularly to those functions that require integration of contextual information. The implications of this thesis are drawn out for an acute versus ‘chronic’ model of psychosis. Chronic deficits in ketamine users may reflect neurological changes associated with repeated NMDA- receptor antagonism and hence may be more similar to changes observed in the later stages of schizophrenia, whereas acute ketamine may better model the acute phase. Persisting cognitive impairments are of concern in light of the burgeoning population of ketamine users. 2 Acknowledgments I could not have completed this thesis without the help of so many colleagues and friends. Most of all, I will be forever indebted to my supervisor Professor Val Curran for her wisdom and insight. She has been a true inspiration and her encouragement, confidence in my abilities, and above all patience and good humour throughout the completion of this work has been astonishing. Thankyou, Val, I will always be proud to have been a member of ‘the Unit’! I also was incredibly lucky to have shared an office with the other notable member of the Unit, Rosa Hoshi, who kept me from the vortex and is the best ‘Pi’ mate anyone could ever wish to have. To Sally Zlotowitz, a big high five, thankyou for always so skilfully separating the ‘wheat from the chaff. Thankyou also to Lee Rowland, Dr. Mat Whalley and Robin Hayman , the other members of the Marlborough Army. I feel truly fortunate to have met such an amazing group of individuals to share all the high’s and low’s of this process with; you are all the ‘Proof I need that it was worthwhile. I would also like to thank the Centre for Anaesthesia in particular Brigitta Brandner, Ali Mofeez and James Smart for their time and dedication. For their help with data collection my thanks go to Fiona Pepper, Jake Bird , Charlie Maitland, Grazia Pac, Marcio Ricelli and Rachael Lippett. I am also grateful to Dr. Susan Rossell and Professor John Krystal, Professor Chris Frith, Professor Judith Ford and Professor Cyril D’Souza for valuable discussions. My grateful thanks to Leslie Muetzelfeldt for helping me with many computer and administrative issues. Thankyou also to my family for their kindness and sense of humour. To Dr. Nick Jones, even though you don’t agree with acknowledgments, thanks for everything, you will always be the better scientist. Finally, I would like to thank all the people who enthusiastically participated in these experiments. 3 The work presented in this thesis has also been published in the following journal articles: Morgan CJA, Mofeez A, Brandner B, Bromley L, Curran HV (2004a) Acute effects of ketamine on memory systems and psychotic symptoms in healthy volunteers. Neuropsychopharmacology 29: 208-218 Morgan CJA, Mofeez A, Brandner B, Bromley L, Curran HV (2004b) Ketamine impairs response inhibition and is positively reinforcing in healthy volunteers: a dose response study. Psychopharmacology 172: 298-308 Morgan CJA, Monaghan L, Curran HV (2004c) Beyond the K-hole: A 3-year longitudinal investigation of the cognitive and subjective effects of ketamine, in recreational users who have substantially reduced their use of the drug. Addiction 99:1450-61. Morgan CJA, Ricelli M, Maitland CH, Curran HV (2004d) Long-term effects of ketamine: evidence for a persisting impairment of source memory in recreational users. Drug and Alcohol Dependence 75: 301-308 Morgan, CJA, Rossell SL, Peppr, F, Smart, J, Blackburn, J, Brandner, B, Curran HV (submitted) Semantic priming after ketamine acutely in healthy volunteers and following chronic self-administration in substance users. 4 Abstract................................................................................................................................... 2 Acknowledgments ................................................................................................................. 3 List of Tables........................................................................................................................ 15 List of Figures.......................................................................................................................18 Selected Abbreviations and Acronyms...............................................................................21 Chapter 1: Introduction ........................................................................................................22 1.1. History of the use of ketamine and related compounds in anaesthesia ............22 1.2 History the abuse of ketamine and PCP by recreational users ..............................23 1.3 Basic pharmacology of ketamine, PCP and dizocilipine ........................................25 1.4 The chemical mechanism of the arylcyclohexylamines .........................................26 1.5 Glutamate, the NMDA -receptor complex and Long-Term Potentiation ...........27 1.6. Effects on other neurotransmitter systems ............................................................28 1.7 PET and BOLD fMRI studies with ketamine and PCP ..........................................29 1.8 Summary.................................................................................................................... 31 LITERATURE REVIEW....................................................................................................32 PART I: ACUTE EFFECTS OF NMDA-R ANTAGONISM ON COGNITIVE FUNCTION..........................................................................................................................33 1.9.1 Animal studies of cognitive function after acute administration of NMDA-R antagonists ........................................................................................................................33 1.9.2 Memory Systems and NMDA-R Hypofunction .................................................. 34 1.9.3 Episodic Memory .................................................................................................. 35 1.9.4 Working Memory, Attention and Executive functioning ................................... 38 1.9.5. Semantic Memory ............................................................................................... 43 1.9.6 Procedural Memory and Perceptual Representation System (PRS) ................ 43 1.9.7.Summary of acute cognitive effects ..................................................................... 44 PART II: SCHIZOPHRENIC SYMPTOMS AND NMDA-R ANTAGONISTS 44 1.10.1 Background to theories of cognitive dysfunction in schizophrenia ................ 45 1.10.2 Schizophrenia and NMDA-R Antagonists .........................................................46 1.10.3 Animal models of other psychotic symptoms ................................................... 48 1.10.4. Human studies of psychotic symptoms following NMDA-R antagonism 49 1.10.5. Administration of NMDA-R antagonists to schizophrenic patients .................52 1.10.6. Interactive effects of ketamine with other drugs .............................................. 53 1.10.7. Summary of acute psychotomimetic effects......................................................56 PART III: CHRONIC EFFECTS OF NMDA-R ANTAGONISTS................................ 58 1.11.1 NMDA-R antagonist associated neurotoxicity studies ......................................58 1.11.2. Studies of the behavioural and cognitive effects of chronic NMDA-R antagonists in animals ......................................................................................................60 1.11.3 Chronic behavioural and
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