The Influence of Diet and Gastric Bypass on Behaviorally Assessed Taste Function in a Rodent Model
Hyde, Kellie M. (author)
Spector, Alan C. (professor directing dissertation)
Roper, Michael Gabriel (university representative)
Williams, Diana L. (committee member)
Houpt, Thomas A. (committee member)
Kelley, Colleen M. (committee member)
Florida State University (degree granting institution)
College of Arts and Sciences (degree granting college)
Department of Psychology (degree granting department)
2021
text
doctoral thesis
Obesity is a pervasive public health concern that is associated with several comorbidities like Type 2 diabetes and cardiovascular disease (Abdelaal, le Roux, & Docherty, 2017; Fruh, 2017; Pi-Sunyer, 2009; Williams, Mesidor, Winters, Dubbert, & Wyatt, 2015). Diet, specifically high intake of calorically dense high-fat or high-sugar foods, significantly impacts the likelihood of developing obesity (Blundell & Cooling, 2000; Williams et al., 2015) and a factor which uncontestably influences diet is taste. Taste signals are channeled into circuits that a) provide information about the sensory features of a food stimulus (sensory-discriminative), b) drive or discourage intake (ingestive motivation), and c) trigger physiological reflexes (cephalic phase responses), all of which influence our dietary choices (Epstein, Carr, Lin, & Fletcher, 2011; Kershaw & Mattes, 2018; Kourouniotis et al., 2016; Negri et al., 2012; A. C. Spector, 2000). Nevertheless, the relationship between obesity and taste has not been fully elucidated. One of the most fundamental processes of any sensory system, including taste, is the detection of the stimulus. Research on the impact of obesity on taste detection in humans is largely inconsistent with some studies finding higher (Kindleysides et al., 2017; Overberg, Hummel, Krude, & Wiegand, 2012; Park et al., 2015; Tucker, Edlinger, Craig, & Mattes, 2014), some lower (Hardikar, Höchenberger, Villringer, & Ohla, 2017; Pasquet, Frelut, Simmen, Hladik, & Monneuse, 2007), and others no differences (Asano et al., 2016; Costanzo, Orellana, Nowson, Duesing, & Keast, 2017; Heinze et al., 2018; Monneuse et al., 2008; Tucker, Nuessle, Garneau, Smutzer, & Mattes, 2015) in sensory thresholds of obese versus lean patients to various taste stimuli. Moreover, taste detection thresholds in a rodent model of obesity for which factors like diet exposure, stimulus experience, and long-term test conditions can be controlled have yet to be examined. Historically, the assessment of a sensory system at the limens of sensitivity, coupled with experimental manipulations, has been exceptionally effective in discerning the contribution of sites along the gustatory neural axis to taste function, especially in animal models (Bales, Schier, Blonde, & Spector, 2015; Blonde, Bales, & Spector, 2015; Laugerette et al., 2005; Sun, Yan, Sun, Song, & Yan, 2017). While there are few nonsurgical treatment options for morbid obesity, bariatric surgery, such as Roux-en-Y gastric bypass (RYGB), reliably induces substantial weight loss that is maintained long-term via a complex of physiological and behavioral postoperative mechanisms (Lutz & Bueter, 2014; Pournaras & le Roux, 2009; L. Sjöström, 2013). Decreases in appetite accompanied by increased satiation, altered concentrations of postprandial gut hormones, and progressive changes in diet choice and preference are among the postsurgical outcomes hypothesized to promote the long-term success of this surgery (le Roux & Bueter, 2014; Lutz & Bueter, 2014; Miras & Le Roux, 2010; L. Sjöström, 2013; Lars Sjöström et al., 2004; Zoon et al., 2018). Research on the changes in intake and choice induced by RYGB has focused primarily on processes related to motivation, reward, and post-ingestive consequences, while very few studies have examined the impact of this surgery and of diet on post-surgical taste sensitivity. Of the few studies that have measured taste sensitivity in humans (M. Bueter et al., 2011; Burge, Schaumburg, Choban, DiSilvestro, & Flancbaum, 1995; El Labban, Safadi, & Olabi, 2016; Holinski, Menenakos, Haber, Olze, & Ordemann, 2015; Scruggs, Buffington, & Cowan, 1994), there is little agreement. Much of this inconsistency may be due to methodological differences across studies and limited control over environmental factors that are endemic in human-subjects research and can be influential on these outcomes (M. B. Livingstone, 1995; Schoeller, 1995). Thus, whether RYGB has effects on sensory-discriminative taste function remains an open issue. Chapter 2 focuses on the influence of Roux-en-Y gastric bypass (RYGB) surgery on ingestive motivation domain of taste function. Licking response to, caloric intake of, and preference (vs. water) for sucrose and glucose solutions were measured in female rats with and without RYGB. The rats did not display differences in concentration-dependent licking to sucrose or glucose when these stimuli were presented in brief access (10 s) trials. This effect was maintained even after significant home-cage stimulus experience, and after a marked decrease in fluid and caloric intake and preference for high concentrations to these sugars. These data suggest that reported changes in post-surgical diet preferences may not be attributable to a change in motivational potency of the taste of sugars in female rats. In Chapter 3, tastes sensitivity was assessed again to determine the influence of RYGB on detection thresholds in female rats maintained on 3 diet conditions. Again, there was no effect of RYGB on threshold concentration for NaCl or sucrose when rats are maintained on chow diet, but RYGB was associated with a decrease in NaCl threshold in rats maintained on a high-fat diet. These data support that RYGB does not influence sensory-discriminative taste function but may interact with diet to influence changes in some taste sensitivity. Further, these data compliment the results found in Chapter 2 and together, suggest that taste function may not be a primary factor in reported changes in diet choice or preference following RYGB. Finally, because the vast majority of RYGB patients are women (H. Buchwald, Buchwald, & McGlennon, 2014; Henry Buchwald et al., 2004; Kizy et al., 2017), but the bariatric rodent model literature is largely based on male animals, our surgical experiments were conducted on female rats. Male rats were also included in the experiments conducted in Chapter 3 to determine the effects of fat exposure on taste detection and microstructural patterns of licking. Here, there was no diet-specific differences in taste thresholds for NaCl or sucrose; however, males maintained on high-fat diet expressed attenuated licking responses that traditionally reflect stimulus palatability. These experiments are the first to directly assess sensory-discriminative taste function in these diet and surgical contexts. Collectively, these data reveal that reported RYGB-induced changes in food preference and related ingestive behaviors do not rely heavily on taste sensitivity as surgery alone does not inherently drive changes in the sensory-discriminative domain of taste function. Additionally, fat content of a diet does not interact with detection thresholds in male rats but does have some influence on hedonic responding to palatable stimuli, suggesting a potential association between diet and reward processing or facets of the motivational domain of gustatory function.
Bariatric Surgery, High-Fat Diet, Obesity, Taste
March 24, 2021.
A Dissertation submitted to the Department of Psychology in partial fulfillment of the requirements for the degree of Doctor of Philosophy.
Includes bibliographical references.
Alan Spector, Professor Directing Dissertation; Michael Roper, University Representative; Diana Williams, Committee Member; Thomas Houpt, Committee Member; Colleen Kelley, Committee Member.
Florida State University
2020_Summer_Fall_Hyde_fsu_0071E_16471