Physiological state tunes mesolimbic signaling: Lessons from sodium appetite and inspiration from Randall R. Sakai

Fortin, Samantha M.; Roitman, Mitchell F.

doi:10.1016/j.physbeh.2016.11.021

Cited by 9 publications

(4 citation statements)

References 103 publications

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“…Our data suggest the absence of compensatory sodium ingestion. As oral sodium consumption rapidly quenches sodium appetite [72,73], an altered hedonic valance of sodium depending on the body's needs is assumed [71,74,75]. To measure the 'liking' of taste solutions, short-term preference tests were performed (Figure 3).…”

Section: Discussionmentioning

confidence: 99%

Sodium Imbalance in Mice Results Primarily in Compensatory Gene Regulatory Responses in Kidney and Colon, but Not in Taste Tissue

2020

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Renal excretion and sodium appetite provide the basis for sodium homeostasis. In both the kidney and tongue, the epithelial sodium channel (ENaC) is involved in sodium uptake and sensing. The diuretic drug amiloride is known to block ENaC, producing a mild natriuresis. However, amiloride is further reported to induce salt appetite in rodents after prolonged exposure as well as bitter taste impressions in humans. To examine how dietary sodium content and amiloride impact on sodium appetite, mice were subjected to dietary salt and amiloride intervention and subsequently analyzed for ENaC expression and taste reactivity. We observed substantial changes of ENaC expression in the colon and kidney confirming the role of these tissues for sodium homeostasis, whereas effects on lingual ENaC expression and taste preferences were negligible. In comparison, prolonged exposure to amiloride-containing drinking water affected β- and αENaC expression in fungiform and posterior taste papillae, respectively, next to changes in salt taste. However, amiloride did not only change salt taste sensation but also perception of sucrose, glutamate, and citric acid, which might be explained by the fact that amiloride itself activates bitter taste receptors in mice. Accordingly, exposure to amiloride generally affects taste impression and should be evaluated with care.

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Section: Discussionmentioning

confidence: 99%

Sodium Imbalance in Mice Results Primarily in Compensatory Gene Regulatory Responses in Kidney and Colon, but Not in Taste Tissue

2020

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“…A key example of this is the phenomenon of sodium appetite, where motivation to obtain and consume sodium changes drastically depending on body fluid balance. Indeed, sodium deprivation produces a robust, selective, and innate appetite for sodium that is in turn reflected in goal-directed behaviors to seek out and ingest sodium [see ( 104 ) for review]. For example, animals that have never before encountered a hypertonic sodium solution express powerful and preferential intake of it immediately upon sodium depletion ( 105 , 106 ).…”

Section: Physiological and Neural Control Of Homeostasismentioning

confidence: 99%

“…Importantly, within the pre-LC and PBel-inner, sodium sensitive neurons that express Forkhead box protein 2 (FoxP2) have direct projections to the VTA. Thus, one logical pathway through which sodium deficiency and body fluid homeostasis is relayed to mesolimbic pathways is via a polysynaptic pathway that traverses through NTS/AP HSD2 neurons → Pre-LC/PBel-inner FoxP2 neurons → VTA dopamine neuron circuitry ( 104 ).…”

Section: Neuronal Inputs To Mesolimbic Pathways That Regulate Homeostmentioning

confidence: 99%

Parallels and Overlap: The Integration of Homeostatic Signals by Mesolimbic Dopamine Neurons

2018

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Motivated behaviors are often initiated in response to perturbations of homeostasis. Indeed, animals and humans have fundamental drives to procure (appetitive behaviors) and eventually ingest (consummatory behaviors) substances based on deficits in body fluid (e.g., thirst) and energy balance (e.g., hunger). Consumption, in turn, reinforces motivated behavior and is therefore considered rewarding. Over the years, the constructs of homeostatic (within the purview of the hypothalamus) and reward (within the purview of mesolimbic circuitry) have been used to describe need-based vs. need-free consumption. However, many experiments have demonstrated that mesolimbic circuits and “higher-order” brain regions are also profoundly influenced by changes to physiological state, which in turn generate behaviors that are poised to maintain homeostasis. Mesolimbic pathways, particularly dopamine neurons of the ventral tegmental area (VTA) and their projections to nucleus accumbens (NAc), can be robustly modulated by a variety of energy balance signals, including post-ingestive feedback relaying nutrient content and hormonal signals reflecting hunger and satiety. Moreover, physiological states can also impact VTA-NAc responses to non-nutritive rewards, such as drugs of abuse. Coupled with recent evidence showing hypothalamic structures are modulated in anticipation of replenished need, classic boundaries between circuits that convey perturbations in homeostasis and those that drive motivated behavior are being questioned. In the current review, we examine data that have revealed the importance of mesolimbic dopamine neurons and their downstream pathways as a dynamic neurobiological mechanism that provides an interface between physiological state, perturbations to homeostasis, and reward-seeking behaviors.

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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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Physiological state tunes mesolimbic signaling: Lessons from sodium appetite and inspiration from Randall R. Sakai

Cited by 9 publications

References 103 publications

Sodium Imbalance in Mice Results Primarily in Compensatory Gene Regulatory Responses in Kidney and Colon, but Not in Taste Tissue

Sodium Imbalance in Mice Results Primarily in Compensatory Gene Regulatory Responses in Kidney and Colon, but Not in Taste Tissue

Parallels and Overlap: The Integration of Homeostatic Signals by Mesolimbic Dopamine Neurons

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

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