Pattern of access determines influence of junk food diet on cue sensitivity and palatability
Introduction
Non-homeostatic eating behavior is strongly motivated by the rewarding effects of palatability and variety in flavor and texture (Rolls, Rolls, Rowe, & Sweeney, 1981). Overindulgence in such foods has been heavily implicated in the obesity epidemic sweeping developed nations (Hill et al., 1998), in which obesity rates have more than doubled in the last 30 years (Fryar et al., 2014, Ogden et al., 2014). Importantly, for many overweight and obese individuals, efforts to control their body weight prove challenging, with craving and compulsive consumption being major culprits (Heymsfield et al., 2007). In some cases, compulsive overeating can become so extreme that it has been compared with drug addiction, as they share many characteristics such as escalating intake over time despite negative consequences, such as foot shock in rats (Avena et al., 2008, Johnson and Kenny, 2010) or negative health or social consequences in humans (Colles et al., 2008, Davis and Carter, 2009, Gearhardt et al., 2009, Gearhardt et al., 2011, Heatherton and Baumeister, 1991).
A key component of maladaptive reward seeking is the acquisition of Pavlovian associations between the primary rewards themselves (e.g., food, drugs) and predictive stimuli in the environment (i.e., a context or discrete cue). With repeated pairings, such cues can come to trigger reward cravings (Childress et al., 1999, Ehrman et al., 1992) and drive efforts to procure reward (Stewart et al., 1984, Volkow et al., 2011, Wallace, 1989). This process, whereby reward-associated cues acquire motivational properties that allow them to become capable of eliciting reward seeking, is termed Pavlovian incentive motivation, frequently referred to in the literature as ‘wanting’. The motivational influence of drug-paired cues is well documented in the drug addiction literature, where drug-paired cues have been shown to potentiate drug seeking for alcohol (Chaudhri, Sahuque, Schairer, & Janak, 2010), nicotine (Liu et al., 2007), cocaine (LeBlanc, Ostlund, & Maidment, 2012), and morphine (Doherty, Ogbomnwan, Williams, & Frantz, 2009), and sensitivity to such cues is considered to underlie a vulnerability to craving, compulsive drug seeking and, consequently, addiction (Robinson and Berridge, 1993, Robinson and Berridge, 2000). Importantly, food-paired cues also become highly salient, capable of producing strong physiological reactions (e.g., increased salivation) and cravings (Jansen, 1998). Food-paired cues are well known to potentiate non-homeostatic (i.e., hunger state-independent) feeding, in both rats (Boggiano et al., 2009, Petrovich et al., 2007, Weingarten, 1983) and humans (Cornell et al., 1989, Jansen et al., 2011), as well as maladaptive overeating (Jansen et al., 2003) in both obese and normal-weight restrained eaters (i.e., such as when dieting) (Fedoroff et al., 1997, Jansen and van den Hout, 1991, Wardle, 1990).
Growing evidence from animal models suggests that, like drugs of abuse, poor diets (i.e., high-fat, high-sugar and refined foods) may have long-term consequences for behavior and cognition, making it difficult to determine whether a hypersensitivity to food-paired cues precedes maladaptive eating in humans, or emerges as a result of it. Indeed, poor quality diets have been shown to produce deficits in hippocampal-dependent learning and memory (Beilharz et al., 2014, Jurdak and Kanarek, 2009, Kanoski and Davidson, 2011), promote a shift from goal-directed to habitual responding (Ahn and Phillips, 2012, Furlong et al., 2014, Tantot et al., 2017), and alter reward liking and craving (Avena and Hoebel, 2003, Buda-Levin et al., 2005, Duca et al., 2014, Johnson and Kenny, 2010, Lesser et al., 2017, Shin et al., 2011a, Vendruscolo et al., 2010b, Vendruscolo et al., 2010b). While specific mechanisms are unclear, growing evidence supports a role for mesolimbic dopamine dysfunction (Johnson and Kenny, 2010, Robinson et al., 2015, Vollbrecht et al., 2016), though the hippocampus may also be preferentially vulnerable to the deleterious effects of junk foods (Lindqvist et al., 2006, Martire et al., 2014, Molteni et al., 2002). As alluded to above, behavioral responses to reward can be dissociated into ‘wanting’ - attributing motivational salience to reward-related stimuli, and ‘liking’ – the hedonic pleasure experienced by consuming reward (Berridge, Robinson, & Aldridge, 2009), and each has been shown to be impacted by such diets (Avena and Hoebel, 2003, Buda-Levin et al., 2005, Duca et al., 2014, Johnson and Kenny, 2010, Lesser et al., 2017, Shin et al., 2011a, Vendruscolo et al., 2010a, Vendruscolo et al., 2010b). A recent study (Robinson et al., 2015) supports a role for both pre-existing individual differences and junk-food-driven changes in reward seeking and liking: rats later identified as susceptible to junk-food-induced obesity show stronger pre-existing conditioned approach behavior than obesity-resistant rats, while junk food exposure, regardless of weight gain, dampened the hedonic impact of palatable foods. Other studies have shown that the pattern of consumption may also matter: sugar-binging rats display addiction-like behaviors not seen in rats with ad libitum sugar access or control rats (Avena and Hoebel, 2003, Buda-Levin et al., 2005). These data indicate that factors such as how the diet is consumed, in addition to individual predisposition to weight gain, must be considered when investigating diet-induced changes in behavior.
Here, we investigated whether a junk food diet could alter reward seeking and liking. Because of the differences between continuous overconsumption and binge eating, we used both ad libitum (24 h) and restricted, intermittent (2 h) daily access to junk food. To probe these behavioral effects, we used the Pavlovian-to-instrumental transfer (PIT) paradigm (a test of cue-evoked incentive motivation, or wanting, for food) and microstructural analysis of licking behavior for a palatable solution (a measure of reward liking) (Davis and Smith, 1992, Hsiao and Fan, 1993). PIT was employed because of the power of this approach to parse the incentive motivational impact of cues from their conditioned reinforcing effects (Berridge and Robinson, 2003, Dickinson and Balleine, 1994, Ostlund and Balleine, 2008). Since cue-invigorated food-seeking and consumption when hungry may be considered adaptive, and we were specifically interested in maladaptive food-seeking behavior, i.e., eating in the absence of hunger, our focus was on tests conducted when rats were sated on home chow, although tests were also conducted under the more conventional hungry condition. Our focus on the sated condition was also based on reports that cues invigorate food consumption in humans in the sated state (Birch et al., 1989, Cornell et al., 1989), and that this may contribute to overeating and obesity (Hetherington, 2007, Lowe and Butryn, 2007, Yeomans et al., 2004). We also examined how diet-induced weight gain relates to cue-evoked reward ‘wanting’ and ‘liking’ by comparing across high and low weight-gainers. We hypothesized that the incentive motivational properties of reward-paired cues in the sated state would increase with junk food exposure, and that, based on the literature cited above, intermittent-fed rats would be particularly vulnerable to this effect.
Section snippets
Subjects and apparatus
Adult (10 weeks old) male Sprague-Dawley rats (n = 79) were pair-housed for the duration of the experiment. Rats were food restricted to 85% of their free-feeding body weight during initial behavioral training. All behavioral training and testing took place in sound- and light-attenuating operant chambers (Med Associates, VT) equipped with a retractable lever, a white noise generator, a clicker audio generator, a food cup capable of delivering liquids, and a contact lickometer system capable of
Weight gain and adipose tissue content
Full details of these measures are provided in Supplementary Materials; only features potentially pertinent to interpretation of the results of the main focus of the study, namely effect of diet on cue-induced food seeking and palatability, are described here for clarity. Multivariate ANOVAs showed no difference among the various diet and duration groups in starting weight (mean 299.68 g, ± 1.72 SEM), but significant differences were apparent in weight gained by the day of euthanasia as a
Discussion
We probed how a junk food diet influences cue-evoked reward seeking and reward palatability, using the PIT test and licking microstructure analysis, respectively. Our focus was on the results of tests conducted under sated conditions because of their relevance to maladaptive food-seeking behavior, i.e. over-eating. We found that junk food consumption resulted in the emergence of different patterns of behavior under sated conditions depending on the schedule of junk food exposure (intermittent
Funding
This work was supported by the National Institutes of Health/National Institutes of Diabetes and Digestive and Kidney Disorders (grant number #DK098709 to NT Maidment, NP Murphy and SB Ostlund).
Author contributions
Alisa Kosheleff conducted the experiments with assistance from Jingwen Araki, Jennifer Hsueh, Andrew Le, Kevin Quizon. Experimental design, data analysis and interpretation, and writing were done by Alisa Kosheleff, Sean Ostlund, Nigel Maidment, and Niall Murphy.
Conflicts of interest
None to declare.
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