Elsevier

Experimental Gerontology

Volume 48, Issue 10, October 2013, Pages 1062-1067
Experimental Gerontology

Comparing the effects of food restriction and overeating on brain reward systems

https://doi.org/10.1016/j.exger.2013.03.006Get rights and content

Highlights

  • Caloric restriction and overeating can affect reinforcement pathways in the brain.

  • Both food restriction and obesity appear among members of the elderly population.

  • Changes in brain reward systems may influence addictive behaviors, such as drug use.

Abstract

Both caloric restriction and overeating have been shown to affect neural processes associated with reinforcement. Both preclinical and some clinical studies have provided evidence that food restriction may increase reward sensitivity, and while there are mixed findings regarding the effects of overeating on reward sensitivity, there is strong evidence linking this behavior with changes in reward-related brain regions. Evidence of these changes comes in part from findings that show that such eating patterns are associated with increased drug use. The data discussed here regarding the differential effects of various eating patterns on reward systems may be particularly relevant to the aging population, as this population has been shown to exhibit altered reward sensitivity and decreased caloric consumption. Moreover, members of this population appear to be increasingly affected by the current obesity epidemic. Food, like alcohol or drugs, can stimulate its own consumption and produce similar neurochemical changes in the brain. Age-related loss of appetite, decreased eating, and caloric restriction are hypothesized to be associated with changes in the prevalence of substance misuse, abuse, and dependence seen in this cohort.

Introduction

A unique situation is emerging among the aging population. Although caloric consumption has been shown to significantly decrease with age (Briefel et al., 1995), obesity is on the rise among members of this cohort (Salihu et al., 2009). Patterns of over- and under eating may have deleterious consequences on both the neurochemistry and behaviors associated with reward and reinforcement of behavior. Of particular relevance is the prediction that by the year 2020 the number of individuals over the age of 50 with substance abuse disorder will be two times higher than estimates from each year between 2002 and 2006 (Han et al., 2009). This prediction highlights the importance of better understanding behaviors, such as under- and overeating, which are known to cause alterations in brain reward functioning and therefore may contribute to the pathology of substance abuse.

Both preclinical and some clinical studies suggest that prolonged food restriction leads to heightened reward sensitivity (Carr, 2002, Frank et al., 2005, Frank et al., 2012). Studies examining the effects of overeating on reward sensitivity are mixed, and several theories have been developed to explain what appear to be conflicting findings (Verbeken et al., 2012). Before discussing the effects of food deprivation or overeating on reward sensitivity, however, it is important to review the neural components associated with responses to reinforcing and rewarding stimuli. Although the brain reward system is complex and consists of a number of different components (i.e., opioids, GABA), this paper will primarily review clinical and preclinical studies investigating the effects of differential feeding behavior on dopamine (DA). Mesolimbic DA neurons project from the ventral tegmental area (VTA) to the nucleus accumbens (NAc), and dopamine is considered to play an important role in influencing motivation for and the reinforcing and rewarding experiences of food consumption, drug use, and other stimuli (Everitt and Robbins, 2005, Schultz, 2010).

By studying the effects of food deprivation and overeating, it may be possible to gain a clearer understanding of the mechanisms that underlie changes in reward response or functioning due to non-homeostatic eating behaviors. In addition, by reviewing findings of studies using laboratory animal models, we may be able to gain insight into the associated biological factors without the psychological variables that may accompany aberrant eating behaviors.

Section snippets

Laboratory animal studies

When laboratory animals are food restricted, they show alterations in behavior that suggest increased reward sensitivity. Rats that have been even acutely food deprived exhibit higher rates of intravenous self-administration of drugs of abuse, such as cocaine and phencyclidine (Carroll et al., 1981). Further, chronic food restriction, accompanied by weight loss, has been shown to decrease the amount of drug necessary to experience its rewarding effects. For example, lateral hypothalamic

Laboratory animal studies

There appears to be a strong causal relationship between food restriction and drug use, as food deprivation has been shown to increase self-administration of a number of different drugs in animals (Carr, 2002). Interestingly, overeating (with or without food restriction) may also precipitate addictive behavior, and there have been several studies that suggest neurochemical and behavioral similarities between drug addiction and the more recently researched topic of “food addiction” (Allen et

Relationship between these findings and the aging population

The information reviewed in this paper may be particularly relevant to the aging population. First, caloric intake has been shown to decrease considerably as age increases. In fact, in the 60 years following 20 years of age, both men and women have been found to substantially decrease their caloric intake per day, with men exhibiting an even greater decrease than their female counterparts (Briefel et al., 1995). If malnutrition is not present, caloric restriction has been reported to delay

Conclusion

Reward sensitivity may be heightened when feeding behavior is reduced as an incentive to eat, thus promoting survival. Such an increase in reward sensitivity may prove maladaptive, however, especially in the absence of need, as is the case in many societies today. Instead, increased sensitivity to reward may result in increased consumption of food and drugs of abuse. Overeating on the other hand, may reduce reward sensitivity over time, potentially perpetuating a cycle of overeating that may

Conflict of Interest

Author has confirmed that there is no conflict of interest.

Acknowledgements

Supported by the University of Florida, DA-03123 (NMA) and Kildehoj-Santini (NMA).

References (63)

  • A. Hajnal et al.

    Accumbens dopamine mechanisms in sucrose intake

    Brain Res.

    (2001)
  • A. Marco et al.

    Feeding and reward: ontogenetic changes in an animal model of obesity

    Neuropharmacology

    (2012)
  • J. Peters et al.

    Neural representations of subjective reward value

    Behav. Brain Res.

    (2010)
  • E.N. Pothos

    The effects of extreme nutritional conditions on the neurochemistry of reward and addiction

    Acta Astronaut.

    (2001)
  • H.M. Salihu et al.

    Obesity: what is an elderly population growing into?

    Maturitas

    (2009)
  • A. Schienle et al.

    Binge-eating disorder: reward sensitivity and brain activation to images of food, Biol

    Psychiatry

    (2009)
  • N. Siep et al.

    Hunger is the best spice: an fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex

    Behav. Brain Res.

    (2009)
  • P.P. Silveira et al.

    Early life experience alters behavioral responses to sweet food and accumbal dopamine metabolism

    Int. J. Dev. Neurosci.

    (2010)
  • E.M. Tricomi et al.

    Modulation of caudate activity by action contingency

    Neuron

    (2004)
  • I.P. Tzanetakou et al.

    “Is obesity linked to aging?“: adipose tissue and the role of telomeres

    Ageing Res. Rev.

    (2012)
  • A.M. Valdes et al.

    Obesity, cigarette smoking, and telomere length in women

    Lancet

    (2005)
  • S. Verbeken et al.

    How is reward sensitivity related to bodyweight in children?

    Appetite

    (2012)
  • L.A. Verhagen et al.

    Dopamine and serotonin release in the nucleus accumbens during starvation-induced hyperactivity

    Eur. Neuropsychopharmacol.

    (2009)
  • N.D. Volkow et al.

    Measuring age-related changes in dopamine D2 receptors with 11C-raclopride and 18F-N-methylspiroperidol

    Psychiatry Res.

    (1996)
  • G.J. Wang et al.

    Brain dopamine and obesity

    Lancet

    (2001)
  • R.M. Anderson et al.

    Caloric restriction and aging: studies in mice and monkeys

    Toxicol. Pathol.

    (2009)
  • M. Avanzi et al.

    Prevalence of pathological gambling in patients with Parkinson's disease

    Mov. Disord.

    (2006)
  • V. Bassareo et al.

    Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state

    Eur. J. Neurosci.

    (1999)
  • K.C. Berridge

    Wanting and liking: observations from the neuroscience and psychology laboratory

    Inquiry

    (2009)
  • M.M. Boggiano et al.

    High intake of palatable food predicts binge-eating independent of susceptibility to obesity: an animal model of lean vs obese binge-eating and obesity with and without binge-eating

    Int. J. Obes.

    (2007)
  • K.S. Burger et al.

    Variability in reward responsivity and obesity: evidence from brain imaging studies

    Curr. Drug Abuse Rev.

    (2011)
  • Cited by (24)

    • Transient food insecurity during the juvenile-adolescent period affects adult weight, cognitive flexibility, and dopamine neurobiology

      2022, Current Biology
      Citation Excerpt :

      Our neurobiological data are consistent with other studies of FR and diet induced obesity in adult rodents. A previous study found that adult rats that experienced 3–4 weeks of FR had lower AMPAR- and/or NMDAR-mediated currents compared with rats that were fed AL.61 Food and feeding experience in adult animals have also been found to affect dopamine release at axonal terminals in both ventral and dorsal striatum.62–69 Our study adds to these existing data by showing that feeding history during development can generate changes in the mesolimbic and nigrostriatal dopamine systems that can be observed in adulthood, 20 days after FI experience has ended.

    • The role of nutrition in addiction recovery: What we know and what we don’t

      2018, The Assessment and Treatment of Addiction: Best Practices and New Frontiers
    • Effects of 3-week total meal replacement vs. typical food-based diet on human brain functional magnetic resonance imaging food-cue reactivity and functional connectivity in people with obesity

      2018, Appetite
      Citation Excerpt :

      Our recent review (Kahathuduwa, Boyd, Davis, O'Boyle, & Binks, 2016), noted there is little research directly examining human brain functional magnetic resonance imaging food-cue reactivity (fMRI-FCR) involving ECR, as most studies focus on total fasting (typically 24–48 h). Evidence suggests that ECR may be associated with decreased food-cue reactivity in brain regions regulating energy balance (e.g. hypothalamus (Rosenbaum, Sy, Pavlovich, Leibel, & Hirsch, 2008)), some regions of the dopaminergic reward system (e.g. orbitofrontal cortex (Bruce et al., 2014; Rosenbaum et al., 2008), anterior cingulate cortex (Murdaugh, Cox, Cook, & Weller, 2012; Rosenbaum et al., 2008) amygdala (Rosenbaum et al., 2008)), nucleus accumbens (Avena, Murray, & Gold, 2013) and regions that execute ingestive behavior (e.g. precentral gyrus (Rosenbaum et al., 2008)). This decrease in reactivity in the dopaminergic reward system, homeostatic regions, and regions associated with ingestion from ECR is frequently accompanied by increased activation in the middle frontal gyrus (i.e. dorsolateral prefrontal cortex) (Rosenbaum et al., 2008).

    View all citing articles on Scopus
    View full text