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UNIVERSITY of CALIFORNIA Los Angeles How Diet Can Alter UNIVERSITY OF CALIFORNIA Los Angeles How Diet Can Alter Reward-Seeking Behavior A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Psychology by Alisa Rose Kosheleff 2017 © Copyright by Alisa Rose Kosheleff 2017 ABSTRACT OF THE DISSERTATION How Diet Can Alter Reward-Seeking Behavior by Alisa Rose Kosheleff Doctor of Philosophy in Psychology University of California, Los Angeles, 2017 Professor Nigel T. Maidment, Co-Chair Professor Kate Wassum, Co-Chair The epidemic of chronic, preventable diseases such as obesity and diabetes remain a serious health concern, driven largely by 1) changes in the global food supply as the consumption of nutritive foods decreases and that of highly refined and processed foods increases, and 2) a subsequent inability to limit food consumption appropriately. While obesity remains at the forefront of preventable diseases, recent evidence suggests that it is strongly associated with insulin resistance and type 2 diabetes, so much so that the phrase “diabesity” has been coined to emphasize their comorbidity. Growing evidence suggests that the foods we eat can have serious consequences not just in the periphery (e.g., weight gain), but can alter our neurochemistry and behavior as well. ii The experiments presented here probe this issue in two parts. First, we examine whether a junk food diet can alter the use of external and internal cues to guide reward seeking behavior. To this end, we used general and outcome-specific Pavlovian-to-instrumental transfer (PIT) tests to probe incentive motivation and decision making, respectively, and a test of outcome devaluation to examine the sensitivity of reward seeking to a decrease in outcome value, after either intermittent or ad libitum junk food exposure. We found that intermittent junk food exposure disrupts general and outcome-specific PIT, promoting reward seeking in response to cues only loosely paired with reward and inconsistent with outcomes predicted by the cue. Ad libitum junk food exposure suppresses reward seeking during a general PIT test, and disrupts outcome- specific PIT similarly to intermittent junk food exposure. Junk food exposure also disrupts the ability of internal, interoceptive cues about satiety state to adjust reward seeking in a test of outcome devaluation, irrespective of the pattern of junk food exposure. We also examined whether an insulin-disrupting high fructose diet would alter incentive motivation in a general PIT test. We used fast-scan cyclic voltammetry to examine dopamine signaling during the PIT test, and in anesthetized animals to further assess dopamine reuptake kinetics. We found that insulin resistant rats were behaviorally and neurochemically sensitive to both reward-paired and “neutral” cues, demonstrating increased reward seeking and phasic dopamine release in response to both types of cues. We also found that dopamine reuptake was prolonged in insulin resistant rats, and that treatment with the insulin receptor sensitizing drug pioglitazone normalized reuptake and incentive motivation. iii The dissertation of Alisa Rose Kosheleff is approved. Alicia Izquierdo Edler Pamela J. Kennedy Kate Wassum, Committee Co-Chair Nigel T. Maidment, Committee Co-Chair University of California, Los Angeles 2017 iv TABLE OF CONTENTS LIST OF FIGURES ..................................................................................................................... vii LIST OF TABLES ..................................................................................................................... viii ACKNOWLEDGEMENTS ......................................................................................................... ix VITA ............................................................................................................................................ xi Chapter 1: General Introduction ............................................................................................... 1 1.1 The Mesolimbic Dopamine System and Reward ................................................................... 3 1.2 Mesolimbic Insulin Signaling ................................................................................................. 5 1.3 Dopamine And Behavior ........................................................................................................ 8 1.4 Reward Wanting: Drug- and Food-Driven Changes in Incentive Sensitization ................... 13 1.5 References ............................................................................................................................. 19 Chapter 2: Pattern of Access Determines Influence of Junk Food Diet on Cue Sensitivity and Palatability .......................................................................................................................... 33 2.1 Introduction ........................................................................................................................... 34 2.2 Methods ................................................................................................................................. 37 2.3 Results ................................................................................................................................... 43 2.4 Discussion ............................................................................................................................. 49 2.5 References ............................................................................................................................. 58 2.6 Supplementary Data .............................................................................................................. 67 Chapter 3: Junk Food Exposure Disrupts Outcome Devaluation and Outcome-Specific Pavlovian-To-Instrumental Transfer in Rats .......................................................................... 76 3.1 Introduction ........................................................................................................................... 77 3.2 Methods ................................................................................................................................. 80 3.3 Results ................................................................................................................................... 84 3.4 Discussion ............................................................................................................................. 88 3.5 References ............................................................................................................................. 99 Chapter 4: A High-Fructose Diet Impairs Brain Insulin Signaling, Dopamine Reuptake, and Incentive Motivation ........................................................................................................ 105 4.1 Introduction ......................................................................................................................... 106 4.2 Experiment 1. A high-fructose diet produces insulin resistance in the brain ..................... 108 Methods .......................................................................................................................... 108 Results ............................................................................................................................ 111 4.3 Experiment 2. A high-fructose diet decreases NAc DAT at the membrane ....................... 114 Methods .......................................................................................................................... 114 Results ............................................................................................................................ 116 v 4.4 Experiment 3. A high-fructose diet disrupts dopamine reuptake ....................................... 117 Methods .......................................................................................................................... 117 Results ............................................................................................................................ 120 4.5 Experiment 4. A high-fructose diet disrupts incentive motivation for food rewards ......... 123 Methods .......................................................................................................................... 123 Results ............................................................................................................................ 126 4.6 Experiment 5. A high-fructose diet increases dopamine release during a PIT test ............ 127 Methods .......................................................................................................................... 127 Results ............................................................................................................................ 132 4.7 Discussion ........................................................................................................................... 135 4.8 References ........................................................................................................................... 144 Chapter 5: General Discussion ............................................................................................... 152 5.1 Junk Food Disrupts the Appropriate Use of External Cues and Incentive Motivation ....... 153 5.2 A High-Fructose Diet Impairs Insulin Signaling, Dopamine Reuptake, and Incentive Motivation .................................................................................................................................
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