BEHAVIORAL AND NEURAL INVESTIGATIONS OF PERCEPTUAL AFFECT by Edward Allen Vessel A Dissertation Presented to the FACULTY OF THE GRADUATE SCHOOL UNIVERSITY OF SOUTHERN CALIFORNIA In Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY (NEUROSCIENCE) May 2004 Copyright © 2004 Edward Allen Vessel ii ACKNOWLEDGMENTS First and foremost, I would like to thank my advisor, Irving Biederman, for his professional, financial, and personal support. He gave me this wonderful opportunity to work on this incredibly interesting idea, and the confidence to believe that I could do great things with it. He provided extensive guidance during the design, execution, and analysis of the experiments, and very efficiently gave me feedback on drafts of this document. Most important of all, he put up with my many idiosyncrasies and enthusiastically encouraged my successes. Special thanks are also due to Mark Cohen of the UCLA Brain Mapping Center for his extensive guidance and friendship through all the phases of the brain imaging study, including design, running subjects, data analysis, and interpretation. I would also like to thank the members of my dissertation committee. Zhonglin Lu gave me assistance with brain imaging analysis and group statistics in addition to general guidance & support. My discussions with Richard Thompson about learning and habituation proved very helpful, as was his general guidance and support. Bartlett Mel had many helpful thoughts on the modeling of preference. Mitchell Earleywine provided helpful iii comments on the factor analysis of preference, as well as personal support in becoming a better writer and researcher. In addition, I am indebted to a number of other USC faculty have helped me with aspects of this work. Bosco Tjan provided an algorithm for creating the spectrally equivalent images, assisted with the computation of RMS contrast, provided scripts for the LO localizer scan, and gave extensive assistance in brain imaging analysis and Linux system administration. Alan Watts and Larry Swanson provided valuable insights into peptide systems, cortical output, anatomy, and emotion. The simulated annealing algorithm used to design imaging sequences was designed with the assistance of Laurent Itti, and Laura Baker provided assistance with the multiple regression analyses used in both the behavioral and imaging experiments. This work would also have been quite difficult without the extensive input and support from my fellow graduate students, and I would like to thank them. In particular, Michael Mangini engaged me in many helpful discussions on this work, assisted with the multiple regression analysis, and provided some much needed distractions. My officemate Marissa Nederhouser provided assistance with statistical analyses, good music, and interesting conversation over the years. Several undergraduates also assisted in running subjects iv and creating stimuli, including Michelle Greene, Henry Nguyen, Tiger Nguyen, Viet Nguyen and Ali Narayan. This work would also not have been possible without extensive help from a number of researchers around the world, and they deserve my heartfelt thanks. Moshe Bar (currently at Massachusetts General Hospital) provided many helpful discussions on preference, priming, and scene perception, and assisted in my selection of imaging parameters and fMRI sequence design. David Glahn (currently at UTHSCSA) assisted with the imaging study design and analysis, particularly in the use of the AFNI software. At UCLA, graduate student Richard Albistegui-Dubois provided extensive instruction on and assistance with operating the magnet and data analysis, and both Zrinka Bilusic and Anne Firestine provided analysis help and assistance with the magnet. Craig Stark (JHU) provided assistance with the AFNI software and the region of interest (ROI) analysis. Geoff Boynton (UCSD) aided extensively in the design and analysis of the imaging experiment. Russ Poldrack (UCLA) provided assistance with impulse response functions and general analysis. Bob Cox (NIMH) provided help with the AFNI software, especially as it pertains to the general linear model, deconvolutions, and motion correction. Douglas Ward (Medical College of Wisconsin) assisted with the deconvolution of my imaging data using the program 3dDeconvolve. Stephen Smith and the rest of FMRIB group (Oxford University Center for v Functional MRI of the Brain) were a tremendous help with the analysis of my imaging data using the FSL software. Randy Buckner (WUSTL), also provided helpful analysis information. I would also like to thank Jean-Marc Fellous (UCSD Salk Institute) for bringing the opioid gradient to the attention of Dr. Biederman. I would like to my heartfelt gratitude to my many friends who put up with me while working on these experiments, and for keeping me sane. In particular, my housemates Jason, Trystan, Ian, and Adam deserve thanks for allowing me to bring my work home with me, as do Roxanne, Ann, and Walid for interesting discussions and being great friends. Lastly, Shari Cha deserves special thanks for providing a peaceful place to write, helping me relax, keeping me motivated, and cheering my spirits! The Dartmouth Summer Institute deserves acknowledgment for giving me a first chance to get some practical experience with imaging and analysis and for introducing me to a number of people that have been very helpful. While this work was being completed, I was supported by a variety of sources, including an NIH Predoctoral Cognitive and Computational Training Grant to USC (T32 MH20003-05), and grants awarded to Irving Biederman from the Human Frontiers Science Program Organization (RG0035/2000B), vi The Army Research Office (MURI ARO DAAG55-98-1-0293), the National Science Foundation (IMSC NSF EEC-9529152), and the James S. McDonnell Foundation (99-53). vii TABLE OF CONTENTS ACKNOWLEDGMENTS……………………………………………………………ii LIST OF TABLES………………………………………………...………………... x LIST OF FIGURES………………………………………………………………... xi ABBREVIATIONS……………………………………………………..…………. xiv ABSTRACT……………………………………………..………………………. xvi I. INTRODUCTION………………………………………………………...……….1 II. A THEORY OF COGNITIVE AND PERCEPTUAL AFFECT………………. 9 Positive Affect in the Ventral Visual Pathway……………………………9 A Neurochemical Index of Interpretability…..…………………. 12 Behavioral Effects of Opioid Antagonists……………… 16 Opioid Systems in the Brain…………………………..… 17 Novelty, Priming, and Competitive Learning………………...…26 Perceptual Affect in a Systems Perspective…………………... 32 Predictions and Extensions………………………………………………37 III. VISUAL PREFERENCE………………………………………………………43 Background……………………………………………………………..… 43 Complexity vs. Interpretability……………………………………43 Effects of Previous Exposure…………………………………… 46 Arousal and Emotional Valence……………………………...….54 A Stimulus Set for Testing Positive Perceptual Affect………………...57 Calibration Experiment……………………………………...…… 57 Stimuli……………………………………......................... 58 Subjects…………………………………………............... 58 Method………………………………………………..…… 59 Results………………………………………………….…. 61 IV. REPETITION……………………………………………………………….….65 Experiment 1: Effects of Repetition, Between-Subjects Design…….. 66 Methods………………………………………………………….... 66 Subjects………………………………………………….... 66 viii Stimuli……………………………………………………... 67 Procedure…………………………………………….…… 67 Results…………………………………………………………..… 68 Conclusions from Experiment 1……………………………....... 73 Experiment 2: Selection of Image Sets for FMRI…………………...…7 5 Methods………………………………………………………….... 76 Subjects………………………………………………….... 76 Stimuli……………………………………………………... 76 Procedure…………………………………………………. 79 Results………………………………………………………….…. 80 Conclusions from Experiment 2……………………………….... 88 V. ENVIRONMENTAL UTILITY……………………………………………….... 90 An Evolutionary Account of Scene Preference……………………….. 90 Experiment 3: Predicting Scene Preference from Environmental Utility……………………………………………………. 99 Methods………………………………………………………….... 99 Stimuli……………………………………………………… 99 Subjects………………………………………………..… 100 Procedure……………………………………………...… 101 Results………………………………………………………...…. 106 Individual Factor Results……………………………..…106 Consistency Results………………………………….… 113 Multiple Regression Results…………………………....114 Conclusions & Discussion………………………………………117 Biophilia and the Preference for Natural Environments…………………………………………...120 VI. FMRI INVESTIGATION OF SCENE PREFERENCE……….………….. 125 Background……………………………………………………………… 125 Experiment 4: Neural Correlates of Perceptual Affect……………… 131 Methods………………………………………………………….. 132 Subjects………………………………………………..… 132 Apparatus………………………………………………... 132 Imaging Protocol………………………………………... 133 Preference Experiment………………...………………. 135 Procedures…………………………………….… 135 Trial Sequence………………………………….. 137 LOC Localizer…………………………………………… 139 Procedures………………………………….…… 139 Analysis and Results……………………………………...……. 140 ix Single Subject Analysis Procedure………………...…. 140 Group Analysis: Whole Brain Voxelwise ANOVA…… 143 Group Analysis: Cluster-Level Significance……..…… 150 Selection of a Subset of Subjects……………...158 Group Analysis: Regions of Interest ANOVA…………163 Individual Differences in Activation Patterns………….169 Repetition “Rebound”……………………………….... 172 Image-Based Correlation Analysis……………………. 173 Conclusions ……………………………………………………. 181 VII. CONTRIBUTIONS AND FUTURE DIRECTIONS…………………..….. 184 Contributions…………………………………………………………….. 184 Future Directions………………………………………………………... 186 Behavioral Studies…………………………………………….... 187 Eyetracking……………………………………………………….188 Individual Differences in the Neural Correlates of Preference…..………………………...……………………….. 189 Pharmacology…………………………………………...……….190 Natural vs. Urban: Distribution of Image Factors in the Ventral Visual Pathway……...…………………………..…….190 Learning Effects…………………………………………….……192 Cross-Modal and Conceptual Priming………………………... 193 Direct Measures of Preference………………………………... 194 BIBLIOGRAPHY………………………………………………………………... 195 x LIST OF TABLES Table 4.1. Correlation of Average Preference Ratings for Experiments 2a and 2b………………………………………………………………………..… 86 Table 5.1. Factor Summary Statistics……………………………………...... 107 Table 5.2. Consistency of Factor Ratings…………………………………… 113 Table 5.3. Correlates of Preference: Multiple Regression Results……….. 114 Table 5.4. Correlates of Preference: Part Correlations for Each Model…..116 Table 6.1. Summary of BOLD Effects: Preference and Repetition……..…162 Table 6.2. Correlation with Preference by ROI……………………………... 179
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