The control of feeding behavior is regulated by two key systems: homeostatic, necessary for basic metabolic processes and survival, and hedonic, driven by sensory perception or pleasure (Rossi and Stuber, 2018). It is important to note that the hypothalamus, specifically the arcuate nucleus (ARC), is crucial in regulating homeostatic feeding (Ullah et al., 2023). Furthermore, homeostatic regulation control interacts with hedonic controls (Berthoud et al., 2017). In this regard, hedonic hunger, related to hedonic regulation system, occurs in response to a desire to consume food for pleasure; it involves “liking,” which is a hedonic reaction to pleasure, and “wanting,” reflecting incentive motivation (Chmurzynska et al., 2021). Furthermore, hedonic eating, the desire to eat, is driven by the brain’s reward system, and may lead to food addictions and binge eating (de Oliveira et al., 2022). Binge eating is defined clinically as consuming a large amount of food, typically palatable food (PF), during intermittent episodes over a short period of time and a loss of control over what and/or how much is being eaten (Hildebrandt and Ahmari, 2021). Studies have found that hedonic hunger also appears to be closely related to loss of control and binge eating (Espel-Huynh et al., 2018).

In recent years, it has become evident that the hedonic/reward brain system can override the hypothalamic regulation of energy balance, particularly when exposed to a variety of palatable, energy dense, high fat and high sugar foods, leading to food overconsumption beyond homeostatic needs (Amin and Mercer, 2016). In this regard, intake of PF may be a risk factor that can lead to chronic overconsumption, contributing to obesity in non-homeostatic feeding conditions (Sallam and Borgland, 2021; Woodward et al., 2022), and inducing addiction-like deficits in brain reward function, which is considered an important source of motivation that may drive overeating (Johnson and Kenny, 2010). Recent studies have proposed a metabolic-reward circuit, which regulates hedonic intake, and is composed of hypothalamic-mesolimbic pathways, where lateral hypothalamus (LH) signaling activates dopaminergic structures such as the ventral tegmental area (VTA). It is proposed that the Nucleus accumbens (NAc)-LH pathway regulates hedonic intake. The proposed circuit involves the LH, VTA, and NAc, with the latter being a key structure in the regulation of appetitive behaviors (Francke et al., 2019).

Given that adolescence is a particularly sensitive period in central nervous system development, adolescents may be vulnerable to foods that are excessively reinforcing, increasing the risk of experiencing dysregulation of food reinforcement processes from early exposure and over time (Fazzino and Kong, 2022), and may also be more likely to be overweight or obese in adulthood (de Andrade Silva et al., 2021; Kimin et al., 2022). In a study comparing adolescent, adult, and aged rats, adolescent rats consumed more PF in an operant paradigm, both in fixed and progressive ratio, indicating that these rats display a higher motivation to obtain the PF reinforcer (Amancio-Belmont et al., 2017). Additionally, an experiment using adolescent and adult rats showed that limited access to PF three or five times per week resulted in significantly more binge-like eating in adolescents than in adults (Bekker et al., 2014).

It has been proposed that preclinical approaches to the study of binge eating help break it into three clinically-significant parts: (1) consumption of a large amount of food, (2) food consumption over a short period of time, and (3) loss of control over eating (Hildebrandt and Ahmari, 2021). In this regard, access to PF may be a factor that contributes to the first two components of binge-like eating. In this respect, it has been shown that ad libitum and continuous restricted access to PF have differential effects on adult male rats, with restricted access inducing binge-like eating behavior to PF, determined as consuming ≥20% of the total daily kilocalories from PF within 1 h access (Muñoz-Escobar et al., 2019). Furthermore, studies have also indicated that young rats exposed to continuous or intermittent access to PF overeat PF on access days (Kreisler et al., 2017; Spierling et al., 2018). Another study showed that exposure to PF during adolescence in short or long operant sessions induces binge-type eating, but the long-access group exhibits significant hyperphagia of PF, indicating that the time of exposure in restricted access models induces changes in PF intake (Curtis et al., 2019). The impact of ad libitum and restricted access to PF on binge eating behavior and the risk of overeating under non-homeostatic conditions is well-established. However, it remains unclear how different restricted access protocols to PF can affect these behaviors in adolescent rats. Therefore, the current study aimed to determine which PF access protocol is the most effective in inducing increased PF intake and binge-like eating behavior in adolescent rats.

The present study aimed to evaluate which PF access protocol is the most sensitive to induce increased intake and binge-like eating behavior of PF during adolescence. Our results show that all access protocols induce binge-like intake, and that the intermittent access model is the most sensible to provoke this type of eating behavior, as evidenced by a significantly different weekly escalation in the binge index, as well as significantly more intake during the binge test. These results are consistent with previous studies that indicate that intermittent 3 times/week access for 1 h to PF significantly increases intake when compared to a daily restricted access model in adult rats (Vazquez-Herrera et al., 2021). Furthermore, it has also been reported that short (30-min) intermittent 3 times/week access to a PF significantly increases binge-like eating behavior when compared to continuous access (Kreisler et al., 2017) or continuous 5 times/week access (Bekker et al., 2014), and that after 4 weeks of 3 times/week feeding protocol, food intake during the access period increases to approximately 70% of chow-only 24-h energy intake (Corwin and Wojnicki, 2006), even though rats are not food deprived. In addition to these findings, our study also included a weekend access model (three continuous times/week), which interestingly showed lower PF caloric and binge-like intake than the continuous (non-significant) and intermittent access models. It is important to note that the results of the continuous group (1 h of access daily) are also in line with previous studies that demonstrated that binge-like eating is induced in restricted daily access models to PF (Muñoz-Escobar et al., 2019; Zepeda-Ruiz et al., 2020). Additionally, intermittent presentations of PF have been shown to increase binge-like eating, in adult rats when compared to continuous access (Wojnicki et al., 2008). Nevertheless, these studies started the access to PF in adult rats. In this regard, our results provide a novel approach showing that during adolescence and adulthood (PND 30 through 72) the development of binge-like eating is related to PF access.

On the other hand, our results show that increased binge-like intake depends on the type of exposure of PF, not necessarily on caloric needs, and that access protocol to PF can lead to caloric overconsumption (Berland et al., 2022). This indicates that the development of binge-like intake in adolescents rats is not dependent on caloric restriction, which is the same as in real-life situations, and is per se a risk factor in the development of obesity in adults (Bekker et al., 2014). Usually, caloric restriction is used to improve motivation for binge-like eating behavior (Placidi et al., 2004; Zepeda-Ruiz et al., 2020), a condition where homeostatic control of food intake is essential for survival; additionally, PF may produce powerful changes in the brain reward circuitry that we did not evolve for, leading to overconsumption (Morin et al., 2017). Our study shows that binge-like intake increases in a chronic exposure from adolescence to adulthood according to PF availability without an apparent caloric need, given that rats are not food deprived. The findings from our study also show in a preclinic model that PF overconsumption in adolescents rats among adolescent rats is not solely driven by caloric necessity, indicating that PF has a high reward salience that can lead to consumption and overconsumption, given that it can occur in sufficient energy reserve conditions (Harb and Almeida, 2014). This result may provide insight into the neurobiological mechanisms that underlie overconsumption.

Studies on binge-like intake during adolescence have mainly focused on alcohol intake, and few studies have evaluated the binge-like intake of PF during this critical period. In this regard, it is important to note that adolescence demands higher nutritional and requirements, and poor diet quality and eating habits established during this period can have long-term consequences, including obesity (Mumena et al., 2023; Wahl, 1999), and eating patterns and behaviors during this period are influenced by many factors, including food availability (Das et al., 2017). The effects of early chronic exposure to PF in restricted access protocols during this period are of particular interest in understanding the development of binge-like eating over time. In this regard, it has been demonstrated that binge-like sucrose intake in adolescent rat models reduces dendritic length and complexity of principal neurons in the basolateral amygdala (Novelle and Diéguez, 2018). Our preclinical study provides useful information on how chronic restricted access to PF in these three models increases binge-like eating in adolescent rats.

It has also been shown that caloric restriction can induce binge-like eating behavior in mice in a 2 h period (Hambly and Speakman, 2015). Regarding PF, the time of exposure to PF has the strongest effect on increasing caloric intake, weight gain, and binge-like intake, and long-term intermittency has been shown to promote larger binge-like intake of PF (Kreisler et al., 2017). Also, restricted access to PF has shown to rapidly induce binge-like intake, with briefer access periods leading to greater intake on initial time of access (Curtis et al., 2019; Kreisler et al., 2018). In our study, results confirm that access plays a salient role in binge-like eating.

Our study also identified the effects of early consumption of PF in adolescent rats and indicated that the longer the exposure to intermittent and daily access to PF, the stronger the effects on these measures, and that it also induces overeating. This is helpful in understanding the effects of long-term consumption of PF during adolescence, suggesting that overconsumption strongly depends on PF access, even without caloric needs, and that these effects continue to grow over time.

It is also important to note that in preclinical studies, limited access models of animal binge-like eating provide a useful tool to evaluate behavioral changes with regard to restricted high sucrose/fat/mixed diets, whereas chow and water are free access (Rospond et al., 2015). In this regard, it has been shown that restricted access to PF can increase its consumption and induce binge-like eating in adult rats (Boggiano et al., 2007; Espitia-Bautista and Escobar, 2021), but little is known about the effects of chronic access to PF during adolescence.

Our preclinical limited access study provides helpful information on the distinct effects that three restricted access models to PF have on binge-like eating behavior when rats are chronically exposed during adolescence. Additionally, our results indicate that food access protocol appears particularly important for increasing energy intake, and for the development and intensity of binge-like eating behaviors, which contributes to understanding how chronic access to PF in different access protocols alters these measures when starting in early adolescence.

Regarding binge-like intake after a withdrawal period, it has been shown that rats exposed to a 2-day access/5-days no access to PF for 7 weeks showed compulsive eating when renewing access to PF, indicating that this behavior alleviates a withdrawal-induced negative emotional state (Iemolo et al., 2012). Our results indicated that rats with intermittent access showed the highest binge index in the Binge Test after a 7-day withdrawal period, which may indicate the highest withdrawal symptoms in this group after 6-weeks of alternating 1-day access/1 day no-access to PF, compared to the weekend group that underwent 4-days with no access for the 6 weeks protocols were maintained. Interestingly, the continuous access group showed the lowest binge-index during the test, confirming that chronic intermittent access to PF induces negative emotional effects, and renewing access relieves withdrawal-induced negative affects (Iemolo et al., 2012), indicating that rewarding and hedonic effects of PF may result in a positive emotional reaction, reducing negative states, playing a major role in overeating and obesity (Singh, 2014).

PF qualities are also important for inducing increased intake and binge-like eating. In this regard, Tenk and Felfeli (2017) analyzed the intermittent access of PF for a single ingredient or a combination (sweetness and fat), and showed that combined PF consumption is significantly higher than that of a single ingredient (Tenk and Felfeli, 2017). Furthermore, a study by Kendig et al. (2022) showed that a solid diet produces more marked effects on energy intake than liquid sugar; in their study, rats were chronically exposed to a solid cafeteria diet (high-fat high-sugar) and/or a 10% sucrose water solution, finding that all rats exposed to cafeteria diet had significantly increased energy intake when compared to rats exposed only to a 10% sucrose water solution and control rats (Kendig et al., 2022). In our study, the PF provided (chocolate sandwich cookies) combines high-sugar, high-fat and solid diet qualities, which offers a strong model of PF to evaluate energy intake and binge-like eating behavior.

Finally, the findings from the present study suggest that different access protocols to PF impacts differentially in the body weight gain, and this effect depends on the developmental stage. Moreover, our data indicates that adolescent rats are undergoing a normal growth development, which is important to consider. Future studies may be conducted to analyze how PF kcal intake is correlated to body weight and body weight gain during this development. Furthermore, the present study included only male subjects, a potential limitation. However, research indicates that the prevalence of eating disorders in men has increased in the last few years (Gorrell and Murray, 2019; Halbeisen et al., 2022), and that some developmental variables of the BED do not differ between men and women (Barry et al., 2002). In this regard, we consider that our results support valuable evidence about the effect of different diet PF access protocols on BED development during adolescence. Sex differences in these results may be explored in future studies. Our findings also highlight that after withdrawal, higher binge like eating index persisted only in rats intermittently exposed to the PF, suggesting that mechanism controlling food seeking and craving may be driven the binge relapse. Further studies are needed to fully understand the neurobiological mechanism controlling hedonic responses to the orosensory properties of the PF, and how that increases the risk for development of overweight and obesity.

In summary, PF intake is mainly related to hedonic responses related to the orosensory properties of the foods (e.g., caloric content, taste). In the present study, even when sated, rats consumed PF in a binge-like manner, suggesting that rats consumed the PF by its intrinsic value instead of homeostatic needs. Different access paradigms to PF can be helpful in studying binge-like intake, which is related to food addiction and binge eating disorder. In addition, determining the most sensible access protocol during adolescence can be helpful in studying how other variables (e.g., stress) may alter PF intake in hedonic feeding regulation from early life stages. Furthermore, understanding the impact of other factors, such as food availability, physical activity, and genetic factors on PF intake during adolescence is crucial in elucidating the complex interplay between developmental, cognitive, and emotional factors that shape feeding behavior.