Mesolimbic dopamine and its neuromodulators in obesity and binge eating

Naef, Lindsay; Pitman, Kimberley A; Borgland, Stephanie L.

doi:10.1017/s1092852915000693

Cited by 56 publications

(42 citation statements)

References 127 publications

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“…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. Given the role of malnutrition and inadequate protein intake on neurodevelopmental psychiatric disorders [5,6] involving alterations of the dopamine system [17,73,74] and having their onset during adolescence [36,75], our current findings also represent a step towards a better understanding of the mechanisms regulating protein appetite, protein malnutrition, and the emergence of dopamine-related disorders.…”

Section: Discussionmentioning

confidence: 82%

Age dependent effects of protein restriction on dopamine release

Naneix

Peters

Young

et al. 2020

Preprint

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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: 82%

Age dependent effects of protein restriction on dopamine release

Naneix

Peters

Young

et al. 2020

Preprint

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“…The impacts of HFDs on dopaminergic pathways have also been reported in the literature. In humans, decreased DA concentration is observed with obesity [27]. Body mass index was found to be negatively correlated with 6-[ 18 F]-fluoro-L-m-tyrosine (FMT) uptake in the dorsal caudate while using FMT positron emission tomography to detect presynaptic DA [28].…”

Section: Discussionmentioning

confidence: 99%

High Fat Diet Suppresses Peroxisome Proliferator-Activated Receptors and Reduces Dopaminergic Neurons in the Substantia Nigra

Kao

Wei

Tsai

et al. 2019

IJMS

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Although several epidemiologic and animal studies have revealed correlations between obesity and neurodegenerative disorders, such as Parkinson disease (PD), the underlying pathological mechanisms of obesity-induced PD remain unclear. Our study aimed to assess the effect of diet-induced obesity on the brain dopaminergic pathway. For five months, starting from weaning, we gave C57BL/6 mice a high-fat diet (HFD) to generate an obese mouse model and investigate whether the diet reprogrammed the midbrain dopaminergic system. Tyrosine hydroxylase staining showed that the HFD resulted in fewer dopaminergic neurons in the substantia nigra (SN), but not the striatum. It also induced neuroinflammation, with increased astrogliosis in the SN and striatum. Dendritic spine density in the SN of HFD-exposed mice decreased, which suggested that prolonged HFD altered dopaminergic neuroplasticity. All three peroxisome proliferator-activated receptor (PPAR) subtype (PPAR-α, PPAR-β/δ, PPAR-γ) levels were significantly reduced in the SN and the ventral tegmental area of HFD mice when compared to those in controls. This study showed that a prolonged HFD induced neuroinflammation, suppressed PPAR levels, caused degeneration of midbrain dopaminergic neurons, and resulted in symptoms reminiscent of human PD. To our knowledge, this is the first study documenting the effects of an HFD on PPARs in dopaminergic neurons.

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“…The ventral tegmental area (VTA) and its mesolimbic dopaminergic projections relay information about environmental cues that predict motivationally relevant outcomes and are sensitive to changes in metabolic state (Naef et al, 2015;Fortin & Roitman, 2017a;Sandhu et al, 2018). Feeding increases dopamine release and dopamine turnover in the nucleus accumbens (NAc) and the magnitude is greater in hungry compared to sated states (Wilson et al, 1995;Bassareo & Di Chiara, 1999).…”

Section: Introductionmentioning

confidence: 99%

Insulin in the ventral tegmental area reduces cocaine‐evoked dopamine in the nucleus accumbens in vivo

Naef

Seabrook

Hsiao

et al. 2018

Eur J of Neuroscience

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Mesolimbic dopamine circuits, implicated in incentive motivation, are sensitive to changes in metabolic state such as weight loss and diet‐induced obesity. These neurons are important targets for metabolic hormones such as leptin, glucagon‐like peptide‐1, ghrelin and insulin. Insulin receptors are located on dopamine neurons in the ventral tegmental area (VTA) and we have previously demonstrated that insulin induces long‐term depression of excitatory synapses onto VTA dopamine neurons. While insulin can decrease dopamine concentration in somatodendritic regions, it can increase dopamine in striatal slices. Whether insulin directly targets the VTA to alter dopamine release in projection areas, such as the nucleus accumbens (NAc), remains unknown. The main goal of the present experiments was to examine NAc dopamine concentration following VTA administration of insulin. Using in vivo FSCV to detect rapid fluctuations in dopamine concentration, we showed that intra‐VTA insulin via action at insulin receptors reduced pedunculopontine nucleus‐evoked dopamine release in the NAc. Furthermore, intra‐VTA insulin reduced cocaine‐potentiated NAc dopamine. Finally, intra‐VTA or intranasal insulin decreased locomotor responses to cocaine, an effect blocked by an intra‐VTA administered insulin receptor antagonist. Together, these data demonstrate that mesolimbic dopaminergic projections are important targets of the metabolic hormone, insulin.

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Mesolimbic dopamine and its neuromodulators in obesity and binge eating

Cited by 56 publications

References 127 publications

Age dependent effects of protein restriction on dopamine release

Age dependent effects of protein restriction on dopamine release

High Fat Diet Suppresses Peroxisome Proliferator-Activated Receptors and Reduces Dopaminergic Neurons in the Substantia Nigra

Insulin in the ventral tegmental area reduces cocaine‐evoked dopamine in the nucleus accumbens in vivo

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