Human Hedonic Experience During Thermal Alliesthesia: a Functional
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Human hedonic experience during thermal alliesthesia: A functional magnetic resonance imaging study A Thesis in The Department of Psychology Presented in Partial Fulfillment of the Requirements For the Degree of Master of Arts at Concordia University Montreal, Quebec, Canada November 2010 © Brian J. Dunn, 2010 CONCORDIA UNIVERSITY School of Graduate Studies This is to certify that the thesis prepared By: Brian John Dunn Entitled: Human hedonic experience during thermal alliesthesia: A functional magnetic resonance imaging study and submitted in partial fulfillment of the requirements for the degree of Master of Arts (Psychology) complies with the regulations of the University and meets the accepted standards with respect to originality and quality. Signed by the final Examining Committee: __________________________________________________ Chair Barbara Woodside _______________________________________________ Examiner Virginia Penhune _______________________________________________ Examiner Natalie Phillips _______________________________________________ Supervisor Peter Shizgal Approved by _______________________________ Jean-Roch Laurence Chair, Psychology Department December 14, 2010 ______________________________ Graham Carr Dean of Graduate Studies Abstract Human hedonic experience during thermal alliesthesia: A functional magnetic resonance imaging study Brian J. Dunn The primary aim of the present experiment was to distinguish and map the hemodynamic correlates of hedonic experience using functional magnetic resonance imaging (fMRI). To accomplish this, we exploited a functional distinction between thermosensory perception and hedonic valuation. We used a water-perfused suit, both to deviate core temperature and to deliver thermal stimulation to the skin. We acquired two fMRI scans of each participant, under opposite core temperature deviations, in a single experimental session. During each scan we alternated the temperature of the circulating water in the suit from hot to cold every 2.25 minutes, for 18 minutes. Participants rated their thermal comfort and the suit temperature on 11-point Likert scales during alternating nine-second epochs. The critical feature of our design is that the hedonic sequence was the same in the two scans whereas the sequence of peripheral thermal stimuli, and the core temperature deviations were opposite. We present behavioral evidence that the opposite sequences of thermal stimuli induced a common pattern of hedonic experience. Furthermore, concurrent hedonic ratings tracked the blood oxygenation level dependent (BOLD) signal recorded from spatially conjoint cortical areas in pairs of scans from the same individuals. In cross-subject mixed effects analyses, we grouped the functional scans acquired under each core temperature deviation. We then used a conjunction analysis of iii the group statistical maps to identify common hemodynamic correlates of the pattern of hedonic experience in both scans. Spatially conjoint (i.e., co-localized) BOLD signal correlates of the hedonic ratings were observed in bilateral subregions of the orbitomedial prefrontal cortex (OMPFC). A second analysis, based on a normative model of hedonic response, yielded spatially conjoint BOLD signal correlates in a more broadly distributed area of the OMPFC, including the subgenual cingulate and bilateral temporal poles. iv Acknowledgements This experiment demands the efforts of a large team of people, all of whom deserve my sincere gratitude. My heartfelt thanks go first to Peter Shizgal, my advisor and the originator of this experiment. Whatever is clear and compelling in this document is due to him; the present account of the experiment captures only a small part of his understanding and much of my confusion. I would like to thank Kent Conover, without whom the scanning and analysis would not have been possible, and who has been a generous colleague and friend. Many thanks to Gilles Plourde and Louise Ullyatt, who cared for me and for our participants, keeping us safe and making the experiment work. Thanks to David Munro, for his clarity and effort from the beginning and for never turning away a request for help. Thanks to Robert Kilgour for his advice and for allowing me to recruit his students. To everyone who assisted us in acquiring these data, including Marie-Pierre Cossette, Levi Riven, Karine Eigenman, Karine Paquin Boisvert, Brendan Parsons, Ian Moreau, and Catherine Cowan, many thanks. Special thanks to Christophe Lower for saving many scans and fixing more than he was ever asked to fix. Thanks to everyone in the Shizgal Lab during my studies, who encouraged and tolerated me: Giovanni Hernandez, Yannick-André Breton, Rebecca Solomon, Ivan Trujillo, Marie- Pierre Cossette, and Marc-André Bacon. I have been a hedgehog among foxes. I must also thank everyone at the Brain Imaging Center of the MNI/H, particularly André Cormier, David Costa, Ron Lopez, Louise Marcotte, Mike Ferreira, and Stacey Peixoto. I v must thank everyone who completed our study, despite the difficulty. And I must thank Gene Heyman for drawing me into psychological research and helping me stay. Finally, my thanks go to my partner, Elizabeth Zeeuw, who took the great risk of coming to Montréal without knowing what would happen and who has cared for me throughout. vi Table of Contents List of Tables and Figures..................................................................................................ix List of Appendices..............................................................................................................xi Introduction.........................................................................................................................1 Method...............................................................................................................................14 Participants.............................................................................................................14 Apparatus...............................................................................................................16 Temperature and physiological monitoring…………………………………...…20 Stimuli....................................................................................................................21 Procedure...............................................................................................................22 Data Analysis.....................................................................................................................39 Results................................................................................................................................50 Behavioral Results.................................................................................................52 Functional Neuroimaging Results: Hedonic ratings……………………………..55 Group analyses of hedonic ratings EVs…..……………………………….……..60 Conjunction analysis of hedonic ratings maps………….…………………….…66 Group analyses of normative alliesthesia EVs…..………………………….…...68 Conjunction analysis of normative alliesthesia maps..............……………….....74 Non-conjoined area in the hedonic conjunction map…………………………...77 Discussion………………………………………………………………………………79 Thermal alliesthesia…………………………………………………………….79 Distinguishing features of the present study……………………………………81 vii Behavioral evidence of altered hedonic response………………………………83 Distinction of hedonic responses from sensory processes……………………...85 Location of conjoint hemodynamic response…………………………………..86 Single-cell recording studies in human subjects………………………….....….90 Single-cell recording studies in non-human primates....………………….....….93 A functional model of orbitomedial prefrontal cortex (OMPFC)………….….100 FMRI studies of hedonic valuation…………………………..........……….….105 FMRI studies of primary rewards and punishers.………………………….….112 Limitations…………………………………………………………………….120 Future Directions……………………………………………………………...129 References......................................................................................................................133 viii List of Figures and Tables Figure 1..............................................................................................................................16 Figure 2..............................................................................................................................17 Figure 3..............................................................................................................................19 Figure 4..............................................................................................................................27 Figure 5..............................................................................................................................29 Figure 6..............................................................................................................................30 Figure 7..............................................................................................................................32 Figure 8..............................................................................................................................35 Figure 9..............................................................................................................................36 Figure 10............................................................................................................................38 Figure 11............................................................................................................................48