Impact of Early Consumption of High-Fat Diet on the Mesolimbic Dopaminergic System

Naneix, Fabien; Tantot, Frédéric; Glangetas, Christelle; Kaufling, Jennifer; Janthakhin, Yoottana; Boitard, Chloé; Smedt-Peyrusse, Véronique de; Pape, Jean‐Rémi; Vancassel, Sylvie; Trifilieff, Pierre; Georges, François; Coutureau, Étienne; Ferreira, Guillaume

doi:10.1523/eneuro.0120-17.2017

Cited by 45 publications

(40 citation statements)

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“…More importantly we highlight the increased sensitivity of the dopamine system during adolescence to the deleterious effects of a diet that is inadequate in protein. Adolescence is characterized by important maturation events within dopamine circuitry and dopamine-related processes [47][48][49][50][51][52] and numerous studies have now demonstrated that adolescence is an important vulnerability window for diet-related alterations of cognitive and neurobiological functions [42][43][44][45][46]. How protein restriction during adolescence may have different, and potentially long-term, impacts on dopamine-related behaviors considering its opposite effects on the mesolimbic and nigrostriatal pathways remains to be investigated.…”

Section: Discussionmentioning

confidence: 99%

“…Early life periods like childhood and adolescence are periods of particular vulnerability to the deleterious impact of various diets on corticolimbic circuits and reward-related processes [40][41][42][43][44][45][46]. Interestingly, the dopamine system undergoes delayed maturation taking place during adolescence making it vulnerable to external insults [46][47][48][49][50][51][52].…”

Section: Introductionmentioning

confidence: 99%

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Age dependent effects of protein restriction on dopamine release

Naneix

Peters

Young

et al. 2020

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Despite the essential role of protein intake for health and development, very little is known about the impact of protein restriction on neurobiological functions, especially at different stages of the lifespan. The dopamine system is a central actor in the integration of food-related processes and is influenced by physiological state and food-related signals. Moreover, it is highly sensitive to dietary effects during early life periods such as adolescence due to its late maturation. In the present study, we investigated the impact of protein restriction either during adolescence or adulthood on the function of the mesolimbic (nucleus accumbens) and nigrostriatal (dorsal striatum) dopamine pathways using fast-scan cyclic voltammetry in rat brain slices. In the nucleus accumbens, protein restriction in adults increased dopamine release in response to high frequency trains of stimulation (10-20 Hz) with no effect on single pulse evoked release. By contrast, protein restriction performed at adolescence decreased nucleus accumbens dopamine release evoked by both single pulses and trains of stimulation pulses (5-10 Hz). In the dorsal striatum, protein restriction has no impact on dopamine release when performed at adulthood but in adolescent rats we observed frequency-dependent increases in stimulated dopamine release. Taken together, our results highlight the sensitivity of the different dopamine pathways to the effect of protein restriction, as well as their vulnerability to deleterious diet effects at different life stages.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Age dependent effects of protein restriction on dopamine release

Naneix

Peters

Young

et al. 2020

Preprint

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“…It has been reported that DA and its metabolites, 3,4-dihydroxyphenylacetic acid and HVA, increase significantly in the cerebral cortex following a long-term HFD intake (Wakabayashi et al, 2015). Furthermore, it was also recently reported that a HFD was associated with sensitization of the DA mesolimbic pathway, with higher bursting activity of DA neurons and enhanced DA release, and greater expression of tyrosine hydroxylase and D2 receptors in the nucleus accumbens (Naneix et al, 2017). In the present study, the significantly increased levels of 5-HT, DA, and NE in the amygdala of the HFD group suggest that chronic HFD exposure for 8 weeks also triggered the synthesis of these brain levels of monoamines in the amygdala.…”

Section: Chronic High-fat Diet-induced Anxiety-like Behaviors Are Weamentioning

confidence: 98%

Gamma Oryzanol Alleviates High-Fat Diet-Induced Anxiety-Like Behaviors Through Downregulation of Dopamine and Inflammation in the Amygdala of Mice

et al. 2020

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Background: A high-fat diet (HFD) can induce obesity and metabolic disorders that are closely associated with cognitive impairments, and the progression of several psychiatric disorders such as anxiety. We have previously demonstrated the anxiolytic-like effect of Gamma oryzanol (GORZ) in chronic restraint stressed mice.Objective: We studied the neurochemical and molecular mechanisms that underlie the preventive effect of GORZ in HFD-induced anxiety-like behaviors, monoaminergic dysfunction, and inflammation.Methods: Eight-week-old Institute of Cancer (ICR) male mice weighing 33-34 g were divided into the following groups and free-fed for 8 weeks: control (14% casein, AIN 93M); HFD; HFD + GORZ (0.5% GORZ). Body weight gain was checked weekly. The anxiolyticlike effects of GORZ were examined via open-field test (OFT) and elevated plus maze (EPM) test. Brain levels of monoamines [5-hydroxy tryptamine (5-HT), dopamine (DA), and norepinephrine (NE)] and their metabolites [5-hydroxyindole acetic acid (5-HIAA), homovanillic acid (HVA), and 3-methoxy-4-hydroxyphenylglycol (MHPG)], proinflammatory cytokines such as tumor necrosis factor-aa (Tnf-a) mRNA levels, and interleukin 1-b (Il-1b) mRNA levels in the cerebral cortex and amygdala were examined using high-performance liquid chromatography-electrochemical detection (HPLC-ECD), and real-time reverse transcription-polymerase chain reaction (RT-PCR), respectively.Results: Mice fed a HFD for eight weeks showed anxiety-like behaviors in association with HFD-induced body weight gain. GORZ potentially blocked HFD-induced anxiety-like behaviors via significant improvement of the primary behavioral parameters in behavioral tests, with a minor reduction in HFD-induced body weight gain. Furthermore, GORZ treatment significantly downregulated HFD-induced upregulation of dopamine levels in the brain's amygdala. Significant reduction of the relative mRNA expression of Tnf-a and Il-1 b was also observed in the amygdala of HFD + GORZ mice, compared to HFD mice. Conclusions:Our findings strongly suggest that 0.5% GORZ exerts anxiolytic-like effects, possibly through downregulation of dopamine, and via expression of proinflammatory cytokines Tnf-a and Il-1 b in the case of chronic HFD exposure.

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“…High sugar and high fat foods have been shown to potently stimulate this pathway (Avena, Rada, Moise, & Hoebel, ; Del Parigi, Chen, Salbe, Reiman, & Tataranni, ; Kenny, ). Moreover, excessive consumption of junk foods evokes enduring changes in the dopamine signaling within regions involved in both reward processing and higher cognitive function (i.e., decision making): the nucleus accumbens (Rada, Avena, & Hoebel, ; Sharma, Fernandes, & Fulton, ; Naneix et al, ), the hippocampus (Kaczmarczyk et al, ; Krishna et al, ), and the PFC (Wakabayashi, Numakawa, Ooshima, Hattori, & Kunugi, ). As such, the increased drive toward engaging in rewarding behaviors in adolescents and a readily available source of highly palatable foods within the environment can potentiate over‐consumption of highly “rewarding” palatable junk food.…”

Section: Reward Signaling In Adolescence—implications For Feeding Behmentioning

confidence: 99%

“…The late maturation of inhibitory GABAergic signaling in the brain also results in a prolonged period of vulnerability within the highly plastic adolescent brain. The consumption of poor quality, hypercaloric foods during adolescence triggers functional changes in dopaminergic signaling (Baladi, Horton, Owens, Daws, & France, , Naneix et al, ), which in turn may modulate the developing inhibitory GABAergic signaling in the PFC (Reichelt, ). As the balance of excitatory and inhibitory neurotransmission in the mature PFC is critical for high‐order cognition and the control of behavior (Tseng & O'Donnell, ), this cascade of changes in dopaminergic, and subsequently GABAergic signaling, triggered by junk food consumption can produce profound and lasting effects on behavior.…”

Section: Diet‐induced Alterations In Reward Neurocircuitrymentioning

confidence: 99%

The impact of junk foods on the adolescent brain

Reichelt

Rank

2017

Birth Defects Research

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Adolescence is a significant period of physical, social, and emotional development, and is characterized by prominent neurobiological changes in the brain. The maturational processes that occur in brain regions responsible for cognitive control and reward seeking may underpin excessive consumption of palatable high fat and high sugar "junk" foods during adolescence. Recent studies have highlighted the negative impact of these foods on brain function, resulting in cognitive impairments and altered reward processing. The increased neuroplasticity during adolescence may render the brain vulnerable to the negative effects of these foods on cognition and behavior. In this review, we describe the mechanisms by which junk food diets influence neurodevelopment during adolescence. Diet can lead to alterations in dopamine-mediated reward signaling, and inhibitory neurotransmission controlled by γ-aminobutyric acid (GABA), two major neurotransmitter systems that are under construction across adolescence. We propose that poor dietary choices may derail the normal adolescent maturation process and influence neurodevelopmental trajectories, which can predispose individuals to dysregulated eating and impulsive behaviors.

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Impact of Early Consumption of High-Fat Diet on the Mesolimbic Dopaminergic System

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Cited by 45 publications

References 71 publications

Age dependent effects of protein restriction on dopamine release

Age dependent effects of protein restriction on dopamine release

Gamma Oryzanol Alleviates High-Fat Diet-Induced Anxiety-Like Behaviors Through Downregulation of Dopamine and Inflammation in the Amygdala of Mice

The impact of junk foods on the adolescent brain

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