Abstract
Obesity is associated with alterations in dopaminergic transmission and cognitive function. Rodent studies suggest that diets rich in saturated fat and refined sugars (HFS), as opposed to diets diets low in saturated fat and refined sugars (LFS), change the dopamine system independent of excessive body weight. However, the impact of HFS on the human brain has not been investigated. Here, we compared the effect of dietary dopamine depletion on dopamine-dependent cognitive task performance between two groups differing in habitual intake of dietary fat and sugar. Specifically, we used a double-blind within-subject cross-over design to compare the effect of acute phenylalanine/tyrosine depletion on a reinforcement learning and a working memory task, in two groups that are on opposite ends of the spectrum of self-reported HFS intake (low vs high intake: LFS vs HFS group). We tested 31 healthy young women matched for body mass index (mostly normal weight to overweight) and IQ. Depletion of peripheral precursors of dopamine reduced the working memory specific performance on the operation span task in the LFS, but not in the HFS group (P=0.016). Learning from positive- and negative-reinforcement (probabilistic selection task) was increased in both diet groups after dopamine depletion (P=0.049). As a secondary exploratory research question, we measured peripheral dopamine precursor availability (pDAP) at baseline as an estimate for central dopamine levels. The HFS group had a significantly higher pDAP at baseline compared to the LFS group (P=0.025). Our data provide the first evidence indicating that the intake of HFS is associated with changes in dopamine precursor availability, which is suggestive of changes in central dopamine levels in humans. The observed associations are present in a sample of normal to overweight participants (ie, in the absence of obesity), suggesting that the consumption of a HFS might already be associated with altered behaviours. Alternatively, the effects of HFS diet and obesity might be independent.
Highlights
Over recent decades, obesity has become a global health burden, making research on the development and maintenance of obesity more relevant than ever
We used a double-blind within-subject cross-over design to compare the effect of acute phenylalanine/tyrosine depletion on a reinforcement learning and a working memory task, in two groups that are on opposite ends of the spectrum of self-reported high fat sugar (HFS) intake
None showed moderate or severe depressive symptoms assessed with the Beck Depression Inventory (BDI), indicated by total scores < 19.44 We decided to only include female participants because previous studies reported larger behavioural effects of acute phenylalanine/ tyrosine depletion (APTD) in women compared to men,[42,45] an effect potentially explained by higher striatal dopamine synthesis capacity in women.[40]
Summary
Obesity has become a global health burden, making research on the development and maintenance of obesity more relevant than ever. Throughout their daily life, people are constantly exposed to food advertisements and available food products Such external food cues have the potential to enhance the motivation to obtain and consume food, even in a satiated state.[2] Recently, it has been shown that people with obesity outperform people with normal weight when learning and tracking the reward predicting value of cues associated with a food reward.[3] In addition, individuals with a higher body mass index (BMI) compared to a lower BMI (normal weight to obese) continue to respond to such food reward cues with the same intensity, despite their decreased motivation to consume the food rewards after devaluation[4,5] In a meta-analysis, García-García et al[6] showed that people with obesity exhibit hyperactivation in reward-related brain areas and proposed that this enhanced focus on rewards may lead to compulsive-like behaviours. Reinforcement learning and working memory both depend on action of dopamine in the striatum and prefrontal cortex (PFC) and optimal levels are crucial for proper functioning.[14,15,16]
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