The impact of a junk-food diet during development on ‘wanting’ and ‘liking’

Highlights

• Junk-food (JF) exposure during development reduces weight gain in two strains of rats.

• JF-induced weight gain has opposite effects on cue attraction in males and females.

• JF gainers work harder for cues and are more attracted to a JF context.

• JF exposure in Long-Evans, but not Sprague-Dawley rats, blunts sucrose ‘liking’.

• JF exposure reduces anxiety-like behavior in males, but not females.

Abstract

The global increase in obesity rates has been tied to the rise in junk-food availability and consumption. Increasingly, children are exposed to a junk-food diet during gestation and early development. Excessive consumption of junk-food during this period may negatively impact the development of brain motivation and reward pathways. In this study we investigated the effects of a chronic junk-food diet throughout development on cue-motivated behavior (‘wanting’), hedonic ‘liking’ for sweet tastes, as well as anxiety and weight gain in male and female Long-Evans (LE) and Sprague-Dawley (SD) rats. Here we found that chronic exposure to a junk-food diet resulted in large individual differences in weight gain (gainers and non-gainers) despite resulting in stunted growth as compared to chow-fed controls. Behaviorally, junk-food exposure attenuated conditioned approach (autoshaping) in females, particularly in non-gainers. In contrast, junk-food exposed rats that gained the most weight were willing to work harder for access to a food cue (conditioned reinforcement), and were more attracted to a junk-food context (conditioned place preference) than non-gainers. Hedonic ‘liking’ reactions (taste reactivity) were severely blunted in LE, but not SD rats, and ‘liking’ for sucrose negatively correlated with greater weight gain. Finally, junk-food exposure reduced anxiety-like behavior (elevated plus maze) in males but not females. These results suggest that junk-food exposure during development may give rise to dissociable differences in ‘liking’ and ‘wanting’ neural systems that do not depend on weight gain and may not be detected through Body Mass Index monitoring alone.

Introduction

Obesity is a global health risk, and the rapid escalation of its prevalence suggests shifting environmental factors may have a role in its growth. As of 2012, over 15% of children and over 30% of adults in the United States are obese, while another 30% of the population is overweight [1]. These numbers are representative of a growing obesity epidemic [1], [2], [3]. The growing accessibility of inexpensive processed foods and their increasingly pervasive advertising may play a role in this alarming trend [4], [5]. Many of these processed foods are saturated with sugar, salt, and fat. Yet they lack adequate protein and other nutrients that are important for day-to-day health and normal growth and development, categorizing them as “junk-food”. In countries with high and rising obesity rates, daily food intake is not exclusively driven by hunger or energy demand. It is suggested that for some individuals, the increased palatability and accessibility of junk-food has seized neural reward and motivation mechanisms and turned food-seeking into errant food craving, which may lead to diet-induced obesity [6], [7].

When a new food is first ingested, its sensory qualities may trigger sensations of hedonic pleasure and ‘liking’, which in turn promote ‘wanting’ to consume that food again [6], [8]. With repeated exposure, however, the environmental cues associated with the junk-food may gain more motivating power and incentive value. The salience of cues associated with food is facilitated through activity in mesocorticolimbic systems, which makes rewards and their cues desired and ‘wanted’ [9], [10], [11]. The neural systems for ‘liking’ and ‘wanting’ typically function in close synchrony, but data show that they can be changed independently. For example, with repeated consumption of a reward, such as palatable junk-food, ‘wanting’ becomes sensitized [11], [12]. Sensitization of ‘wanting’ was first described in the ‘incentive sensitization’ theory of addiction, and can result in a dissociation of ‘wanting’ and ‘liking’ that leads to strong feelings of desire for particular rewards and their cues, despite no increase and sometimes a reduction in ‘liking’ [13]. Although it was initially applied to drugs and their cues, recent evidence suggests this theory also applies to food cues. Food cues can play a similar role by triggering visual attention and enhancing the desire to eat [14], [15], [16], [17], particularly in obese individuals who might be hyper-responsive to the motivational properties of these cues [18], [19], [20].

However, susceptibility to (incentive) sensitization appears to show a large degree of individual variation, with marked sex differences [21]. For example, there is evidence for individual variation in the level of attraction and motivation to junk-food cues [12], [22], [23]. In particular, we recently demonstrated that animals that gained excessive weight on a junk-food diet (gainers) displayed greater cue-induced approach to food cues even before gaining access to the diet [12], and were also more willing to work for the presentation of those cues (conditioned reinforcement) after obesity onset. However, many of these studies were carried out in adults. The current ease of access and high palatability of these foods means that exposure to a junk-food diet may begin as early as childhood or even prior to birth through the mother’s diet.

Childhood obesity has been implicated as a cofactor in a number of lifetime diseases such as depression, anxiety, diabetes, elevated blood pressure, orthopedic problems, and pulmonary complications [24], [25], [26], and has been associated with early mortality [27], [28]. Previous studies have shown that a mother’s diet during pregnancy alters the protein make-up of the offspring’s cerebral cortex despite cross-fostering [29], while also producing changes in dopaminergic activity [30]. Developmental perspectives on the obesity epidemic are necessary to understand the increasing prevalence of childhood obesity across generations [1], [25], and dissociations between ‘liking’ and ‘wanting’ could have a lasting impact when occurring within the plastic neural networks of a maturing brain. However, it is currently unclear whether overconsumption of junk-food is related to distortions of either ‘liking’ or ‘wanting’, or both, when exposure begins prenatally.

Here we examined the effect of lifetime exposure to junk-food on ‘wanting’ by measuring the degree to which food cues 1) elicit approach (autoshaping), 2) reinforce operant responding (conditioned reinforcement), and 3) by determining the attraction of a junk-food paired context (conditioned place preference). We also measured the impact of lifetime exposure to a junk-food diet on hedonic orofacial ‘liking’ reactions, using taste reactivity measures [31] in response to sucrose. In addition, since anxiety is often associated with increased consumption of fatty-sugary foods [32], we also evaluated individual differences in the impact of junk-food on levels of anxiety-like behavior using the elevated plus maze. Finally there are marked sex differences in the motivation for food [33], [34]. Recent findings also show strain and sex differences for spatial learning [35], [36], behavior toward unfamiliar foods [37] and metabolic responses [38]. Therefore measures of ‘wanting’, ‘liking’ and anxiety were determined in males vs. females, across two strains of rats, Long-Evans and Sprague-Dawley.