A history of human‐like dieting alters serotonergic control of feeding and neurochemical balance in a rat model of binge‐eating

Chandler‐Laney, Paula; Castañeda, Edward; Viana, J B; Oswald, Kimberly D.; Maldonado, Christine R.; Boggiano, Mary M.

doi:10.1002/eat.20349

Cited by 22 publications

(24 citation statements)

References 41 publications

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“…This increase in sucrose-licking activity in the LS-lesioned rats was independent from thirsting or fasting and was not eliminated by sucrose preloading (9). In addition to the plausible implication of the LS, the alterations in the activity of the dopamine, serotonin, and opioid systems may be involved in the mechanisms of regulation of feeding behavior in rats submitted to intermittent eating of palatable food (5,7,12,15,17,18,68,83).…”

Section: Discussionmentioning

confidence: 88%

Intermittent access to sucrose increases sucrose-licking activity and attenuates restraint stress-induced activation of the lateral septum

Martin

Timofeeva

2010

American Journal of Physiology-Regulatory, Integrative and Comp

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Martin J, Timofeeva E. Intermittent access to sucrose increases sucroselicking activity and attenuates restraint stress-induced activation of the lateral septum. Am J Physiol Regul Integr Comp Physiol 298: R1383-R1398, 2010. First published March 3, 2010 doi:10.1152/ajpregu.00371.2009.-Intermittent access to palatable food can attenuate anorectic and hormonal responses to stress in rats. The neuronal mechanisms of modulation of stress response by diets are not fully understood. The present study was conducted to create rat models with intermittent access to sucrose that demonstrate resistance to stress-induced hypophagia, to study the pattern of sucrose consumption by these rat models, and to investigate in which brain structures intermittent sucrose regimens modify stressinduced neuronal activation. The obtained results demonstrate that 6-wk intermittent access to sucrose without food restriction (4 day/wk ad libitum access to sucrose in addition to chow, and following 3 day/wk exclusive feeding of chow; SIA rats) and combined with food restriction (4 day/wk access to chow and sucrose restricted to 2 h/day, and following 3 days/wk on unrestricted chow; SIR rats) increased sucrose-licking activity. The alterations in the rats' feeding behavior were accompanied by a resistance of their body weight gain and food intake to 1-h restraint stress applied once per week. The chronic intermittent sucrose consumption significantly lowered, in the SIA and SIR rats, the levels of expression of corticotropin-releasing factor type 2 receptor and restraint stress-induced expression of c-fos mRNA in the medioventral part of the lateral septum. Conversely, the levels of the corticotropin-releasing factor type 2 receptor transcript in the ventromedial hypothalamic nucleus were decreased only in the foodrestricted SIR rats. The lower stress-induced neuronal activation in the medioventral part of the lateral septum may contribute to the attenuated anorectic stress response in the rats maintained on intermittent sucrose regimens. restraint stress; c-fos; corticotropin-releasing factor; hypothalamicpituitary-adrenal axis; corticotropin-releasing factor type 2 receptor ACCUMULATED EVIDENCE STRONGLY suggests that palatable diets can modify the effects of stress. Thus a feeding regimen with an option of eating palatable sucrose and lard may attenuate hypophagic responses to restraint stress (48). Restraint stress applied acutely and repeatedly usually promotes anorectic effects in rats fed regular chow (24,74,77). The anorectic effect of restraint stress apparently depends on the brain corticotropin-releasing factor (CRF) system, since the central application of the nonspecific CRF antagonist ␣-helical CRF considerably reversed restraint stress-induced anorexia (77). CRF is a key neuropeptide-regulating activity of the hypothalamic-pituitary-adrenal (HPA) axis. Activation of the HPA axis in response to stress has been extensively characterized. Briefly, exposure to stress activates the neurons in the parvocellular part of the paraventr...

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Section: Discussionmentioning

confidence: 88%

Intermittent access to sucrose increases sucrose-licking activity and attenuates restraint stress-induced activation of the lateral septum

Martin

Timofeeva

2010

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Despite the robustness of the HD+Stress model to alterations in experimental manipulations by us and others [33, 43, 53, 60–62, 89–92], we have not always been able to obtain binge-eating in the rats. Sometimes others, also, could not obtain the effect with foot shock or if they did, the binge-eating was attenuated [91, 92].…”

Section: The History Of Dieting + Stress (Hd+stress) Modelmentioning

confidence: 80%

“…Indeed, subsequent work from the Boggiano lab found that rats with a HD developed neurochemical and behavioral changes consistent with anhedonia despite normal energy balance. This was true regardless of experience with or without stress [53] and whether rats had intermittent, daily, or no exposure to palatable food during the HD [53, 54]. Translating to humans, “forbidden foods” (typically palatable foods) are often consumed during a binge [55, 56].…”

Section: The History Of Dieting + Stress (Hd+stress) Modelmentioning

confidence: 99%

“…In the HD+Stress model fluoxetine, a selective-serotonin reuptake inhibitor (SSRI) that is approved for the treatment of bulimia, decreased intake of HD+noStress rats as potently as the binge-eating of HD+Stress rats at 2 h. At 4 h post-treatment, fluoxetine was still effective in the binge-eating rats, but not in HD+noStress controls [53]. Hence, a HD may impose long-lasting changes on satiety regulation, a key function of serotonin, despite normal body weight.…”

Section: Selected Neurotransmitter Systems Implicated In Binge Eatingmentioning

confidence: 99%

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Feeding and reward: Perspectives from three rat models of binge eating

Corwin

Avena

Boggiano

2011

Physiology & Behavior

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264

187

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Research has focused on understanding how overeating can affect brain reward mechanisms and subsequent behaviors, both preclinically and in clinical research settings. This work is partly driven by the need to uncover the etiology and possible treatments for the ongoing obesity epidemic. However, overeating, or non-homeostatic feeding behavior, can occur independent of obesity. Isolating the variable of overeating from the consequence of increased body weight is of great utility, as it is well known that increased body weight or obesity can impart its own deleterious effects on physiology, neural processes, and behavior. In this review, we present data from three selected animal models of normal-weight non-homeostatic feeding behavior that have been significantly influenced by Bart Hoebel’s 40+-yr career studying motivation, feeding, reinforcement, and the neural mechanisms that participate in the regulation of these processes. First, a model of sugar bingeing is described (Avena/Hoebel), in which animals with repeated, intermittent access to a sugar solution develop behaviors and brain changes that are similar to the effects of some drugs of abuse, serving as the first animal model of food addiction. Second, another model is described (Boggiano) in which a history of dieting and stress can perpetuate further binge eating of palatable and non-palatable food. In addition, a model (Boggiano) is described that allows animals to be classified as having a binge-prone vs. binge-resistant phenotype. Lastly, a limited access model is described (Corwin) in which non-food deprived rats with sporadic limited access to a high-fat food develop binge-type behaviors. These models are considered within the context of their effects on brain reward systems, including dopamine, the opioids, cholinergic systems, serotonin, and GABA. Collectively, the data derived from the use of these models clearly show that behavioral and neuronal consequences of bingeing on a palatable food, even when at a normal body weight, are different from those that result from simply consuming the palatable food in a non-binge manner. These findings may be important in understanding how overeating can influence behavior and brain chemistry.

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“…This compound decreases the frequency of binge eating episodes and its severity and has been used before in animal models to inhibit binge eating-like behavior (36, 44–47). Therefore, we decided to evaluate if the administration of fluoxetine was able to inhibit the SBLB in our experimental conditions.…”

Section: Discussionmentioning

confidence: 99%

Wistar-Kyoto Female Rats Are More Susceptible to Develop Sugar Binging: A Comparison with Wistar Rats

Papacostas-Quintanilla

Ortíz-Ortega

López‐Rubalcava

2017

Front. Nutr.

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The hedonic component of the feeding behavior involves the mesolimbic reward system and resembles addictions. Nowadays, the excessive consumption of sucrose is considered addictive. The Wistar-Kyoto (WKY) rat strain is prone to develop anxiety and addiction-like behavior; nevertheless, a lack of information regarding their vulnerability to develop sugar binging-like behavior (SBLB) and how it affects the reward system persist. Therefore, the first aim of the present study was to compare the different predisposition of two rat strains, Wistar (W) and WKY to develop the SBLB in female and male rats. Also, we studied if the SBLB-inducing protocol produces changes in anxiety-like behavior using the plus-maze test (PMT) and, analyzed serotonin (5-HT) and noradrenaline (NA) concentrations in brain areas related to anxiety and ingestive behavior (brain stem, hypothalamus, nucleus accumbens, and amygdala). Finally, we evaluated whether fluoxetine, a drug that has been effective in reducing the binge-eating frequency, body weight, and severity of binge eating disorder, could also block this behavior. Briefly, WKY and W female rats were exposed to 30% sucrose solution (2 h, 3 days/week for 4 weeks), and fed up ad libitum. PMT was performed between the last two test periods. Immediately after the last test where sucrose access was available, rats were decapitated and brain areas extracted for high-performance liquid chromatography analysis. The results showed that both W and WKY female and male rats developed the SBLB. WKY rats consumed more calories and ingested a bigger amount of sucrose solution than their W counterpart. This behavior was reversed by using fluoxetine, rats exposed to the SBLB-inducing protocol presented a rebound effect during the washout period. On female rats, the SBLB-inducing protocol induced changes in NA concentrations on WKY, but not on W rats. No changes were found in 5-HT levels. Finally, animals that developed SBLB showed increased anxiety-like behavior in the PMT. In conclusion, WKY female rats can be considered as a more susceptible rat strain to develop SBLB.

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A history of human‐like dieting alters serotonergic control of feeding and neurochemical balance in a rat model of binge‐eating

Abstract: Despite lack of hunger, a history of human-like dieting alters serotonin function in ways suggesting consequences not only to feeding but also control of reward and mood that are dependent on dopamine/serotonin interactions.

Cited by 22 publications

References 41 publications

Intermittent access to sucrose increases sucrose-licking activity and attenuates restraint stress-induced activation of the lateral septum

Intermittent access to sucrose increases sucrose-licking activity and attenuates restraint stress-induced activation of the lateral septum

Feeding and reward: Perspectives from three rat models of binge eating

Wistar-Kyoto Female Rats Are More Susceptible to Develop Sugar Binging: A Comparison with Wistar Rats

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