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An Investigation of the Neural Mechanism by Which the Prefrontal Cortex Facilitates Anti-Saccade Task Performance Western University Scholarship@Western Electronic Thesis and Dissertation Repository 11-2-2012 12:00 AM An Investigation of the Neural Mechanism by which the Prefrontal Cortex Facilitates Anti-saccade Task Performance Michael J. Koval The University of Western Ontario Supervisor Dr. Stefan Everling The University of Western Ontario Graduate Program in Neuroscience A thesis submitted in partial fulfillment of the equirr ements for the degree in Doctor of Philosophy © Michael J. Koval 2012 Follow this and additional works at: https://ir.lib.uwo.ca/etd Part of the Systems Neuroscience Commons Recommended Citation Koval, Michael J., "An Investigation of the Neural Mechanism by which the Prefrontal Cortex Facilitates Anti-saccade Task Performance" (2012). Electronic Thesis and Dissertation Repository. 1011. https://ir.lib.uwo.ca/etd/1011 This Dissertation/Thesis is brought to you for free and open access by Scholarship@Western. It has been accepted for inclusion in Electronic Thesis and Dissertation Repository by an authorized administrator of Scholarship@Western. For more information, please contact [email protected]. AN INVESTIGATION OF THE NEURAL MECHANISM BY WHICH THE PREFRONTAL CORTEX FACILITATES ANTI-SACCADE TASK PERFORMANCE (Spine title: The Neural Mechanism of Prefrontal Saccade Control) (Thesis format: Integrated-Article) by Michael J. Koval Graduate Program in Neuroscience A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy The School of Graduate and Postdoctoral Studies The University of Western Ontario London, Ontario, Canada © Michael J. Koval 2012 THE UNIVERSITY OF WESTERN ONTARIO SCHOOL OF GRADUATE AND POSTDOCTORAL STUDIES CERTIFICATE OF EXAMINATION Supervisor Examiners ______________________________ ______________________________ Dr. Stefan Everling Dr. Brian Corneil ______________________________ Advisory Committee Dr. Bruce Morton ______________________________ ______________________________ Dr. Paul Gribble Dr. Martin Paré ______________________________ ______________________________ Dr. Steve Lomber Dr. Susanne Schmid The thesis by Michael John Koval entitled: An Investigation of the Neural Mechanism by which the Prefrontal Cortex Facilitates Anti-saccade Task Performance is accepted in partial fulfilment of the requirements for the degree of Doctor of Philosophy Date__________________________ _______________________________ Chair of the Thesis Examination Board ii Abstract Cognitive control enables us to guide our behaviour in an appropriate manner, such as rapid eye movements (saccades) toward a location or object of interest. A well- established test of cognitive control is the anti-saccade task, which instructs subjects to look away from a suddenly-appearing stimulus. The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) are part of a cortical saccade control network that influences the superior colliculus (SC), which sends saccade commands to the brainstem saccade generator. To compare and contrast the roles of the dlPFC and ACC in saccade control, the cryoloop method of reversible cryogenic deactivation was used to identify the effects of dlPFC and ACC deactivation on pro-saccades and anti- saccades. Both dlPFC and ACC deactivation increased the incidence of ipsilateral saccades, but only dlPFC deactivation impaired contralateral saccades. An inhibitory model of prefrontal function has been proposed by which the prefrontal cortex suppresses the activity of SC saccade neurons on anti-saccade trials, to inhibit an unwanted saccade toward the stimulus. A direct test of this inhibitory model was performed by deactivating the dlPFC and recording the activity of SC saccade neurons. Unilateral dlPFC deactivation delayed the onset of saccade-related activity in the SC ipsilateral to deactivation, which suggests that the dlPFC has an excitatory influence on SC saccade neurons. There was also an increase of activity in the contralateral SC, which suggests that unilateral dlPFC deactivation caused a neural imbalance at the SC. Bilateral dlPFC deactivation, on the other hand, should not cause a neural imbalance, and thus was used to identify the effects of dlPFC deactivation that were caused by cognitive control impairments. Bilateral dlPFC deactivation increased the stimulus- related activity, and decreased the saccade-related activity, of SC saccade neurons. An increase of anti-saccade errors was more substantial in a “rule memorized” condition, which suggests that the dlPFC plays an important role in rule maintenance. Given an excitatory influence of the dlPFC on SC saccade neurons, I propose that the dlPFC facilitates anti-saccade task performance by first maintaining the relevant rule in working memory, then implementing the rule by enhancing the saccade-generating signal at the SC. iii Keywords Anterior cingulate cortex Anti-saccade task Cryogenic deactivation Dorsolateral prefrontal cortex Monkey neurophysiology Oculomotor control Response inhibition Superior colliculus Saccadic eye movements iv Co-Authorship Michael J. Koval1,3, Kevin Johnston1,2,4, Stephen G. Lomber1,2,3,4,5, Stefan Everling1,2,3,4,5 1 Brain and Mind Institute, London, Ontario, Canada 2 Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada 3 Graduate Program in Neuroscience, University of Western Ontario, London, Ontario, Canada 4 Department of Psychology, University of Western Ontario, London, Ontario, Canada 5 Robarts Research Institute, London, Ontario, Canada Michael Koval performed the experiments, analysed the data, assisted in the preparation of manuscripts for publication, and wrote the remaining chapters of this dissertation. Dr. Stefan Everling designed the experiments, Dr. Steve Lomber designed the equipment that was used for the experiments, and both Drs. Everling and Lomber performed surgeries to prepare the animals for the experiments. Dr. Everling and Dr. Kevin Johnston wrote the original manuscript for Chapter 3, while Drs. Everling and Lomber wrote the original manuscript for Chapter 4. I have modified these manuscripts to provide consistency across all chapters, and include additional information that I felt was necessary for the purposes of my dissertation. The results of the third experiment (Chapter 4) have been published in the Journal of Neuroscience as Koval MJ, Lomber SG, Everling S (2011) Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades. J Neurosci 31:8659-8668. The results of the second experiment (Chapter 3) have been accepted for publication in Cerebral Cortex as Johnston K, Koval MJ, Lomber SG, Everling S (2013). Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus. Cerebral Cortex (in press). Finally, it remains to be determined how the results of the first experiment (Chapter 2) will be included with the results of another experiment for the purposes of publication. v “Keep me safe and warm When I’m riding out my storm… A narrow bank, a narrow wall There’s room to hide here... Calm never fails, it merely shines” Dickinson, Rob. “The Storm.” Fresh Wine for the Horses. Sanctuary Records Group, 2005. vi I dedicate the completion of this, my PhD dissertation, both to my parents, John and Susan Koval, for having helped to get me this far, and to Christy Zhou, for helping to take me the rest of the way. vii Acknowledgements There are many people that I would like to thank for their friendship and assistance since I joined the Everling lab as an undergraduate Honours student in the Fall of 2003. Fellow students, of which there have been too many to name them all. In particular though, I’d like to thank the current lab members for helping to prepare me for the arduous task that is the thesis defense: Sahand Babapoor-Farrokhran, Jason Chan, Sabeeha Hussein, Kevin Skoblenick and Susheel Vijayraghavan. Also Tyler Peel from the Corneil lab, which is so close and yet strangely feels so far away. Jessica Phillips for having been here just about as long as I have, which makes me look better for not being the only one! Darren Pitre, our Registered Laboratory Animal Technician, for his unfailing devotion to animal care, and incredibly bizarre taste in music. Data, Chekov, Archer, and Bones, without whom none of this work would have been possible, and Worf for a chin and belly to scratch. Their lives helped bring greater knowledge to our world. Michela Rebuli and Jacek Majewski for also helping to take care of the animals. Kevin Barker, Sarah Hughes, Brian Soper, and Katherine Green for their assistance and technical skills. Amee Hall for intricately constructing the cryoloops, and Dr. Steve Lomber for somehow implanting them into such tiny sulci, despite having not so tiny hands. Also thanks to Dr. Lomber for always being so cheerful: it’s never a bad day when this guy is around! Dr. Kevin Johnston and Dr. Brian Corneil for strongly suggesting that I read more: they were right, I should have. Dr. Johnston for taking the time to explain things to me so well, Dr. Corneil for serving on pretty much every committee that I ever had, and suitably being the last one to sign-off on my dissertation. My mother, Dr. Susan Koval, and the Department of Microbiology and Immunology, for letting me store dry ice in their freezer, which allowed me to run experiments on weekends. My father, Dr. John Koval, for his expert advice on statistics, which was complicated somewhat by the fact that
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