The impact of sleep deprivation on food desire in the human brain

Abstract

Epidemiological evidence supports a link between sleep loss and obesity. However, the detrimental impact of sleep deprivation on central brain mechanisms governing appetitive food desire remains unknown. Here we report that sleep deprivation significantly decreases activity in appetitive evaluation regions within the human frontal cortex and insular cortex during food desirability choices, combined with a converse amplification of activity within the amygdala. Moreover, this bi-directional change in the profile of brain activity is further associated with a significant increase in the desire for weight-gain promoting high-calorie foods following sleep deprivation, the extent of which is predicted by the subjective severity of sleep loss across participants. These findings provide an explanatory brain mechanism by which insufficient sleep may lead to the development/maintenance of obesity through diminished activity in higher-order cortical evaluation regions, combined with excess subcortical limbic responsivity, resulting in the selection of foods most capable of triggering weight-gain.

Fig. 1. Neural consequences of sleep deprivation on food desirability

Sleep deprivation lead to marked decreases in the anterior cingulate, left lateral orbital frontal cortex and anterior insula reactivity to food desirability (A). In addition, sleep deprivation lead to a significant increase in amygdala reactivity to food desirability but no significant difference in ventral striatum reactivity (B). All parameter estimates are from a GLM with a parametric contrast of individual “want” ratings from twenty-three participants. Whole brain analysis (above) thresholded at p<0.005 for display purposes for sleep deprivation increases (B) and decreases (A). Region of interest analysis (below) are mean parameter estimates with standard errors of the mean extracted from 5mm spheres centered at foci taken form previous literature (See methods; circles indicate general areas of interest not specific foci; * indicates p<0.05 uncorrected for paired t-tests across 23 participants and ** indicates p<0.05 with Bonferroni correction for five regions of interest). For completeness, and since this is the first study to our knowledge to assess neural responses to food desire after sleep loss, Table 2 reports whole brain activation differences between sleep rested and deprived conditions (p<0.001 uncorrected using voxel-wise paired t-tests). Error bars are s.d.

Fig. 2. Self reported hunger levels

Collected using a visual analog scale with a 10cm line, y-axis is in millimeters. There were no significant differences between sleep rested and sleep deprived sessions either at arrival or before the scan session. However, hunger levels were significantly greater before the scan compared to arrival in both groups (p < .05; paired t-tests across 23 participants). Error bars are s.d.

Fig. 3. Behavioral consequences of sleep deprivation on food desirability

Behavioral responses (taken from in-scan ratings) are shown for the percentage of wanted high and low calorie items respectively (A) and the degree to which individual differences in sleepiness (after sleep deprivation) predict high-calorie choices (B). High/low calorie items are based on median split on Calories per serving; wanted items were collapsed across “somewhat” and “strongly” wanted ratings (* indicates p<0.05; paired t-test across 23 participants). Error bars are s.d.

Fig. 4. Food desire task trial structure

Participants saw and rated 80 food items on a scale from 1–4 according to how much they wanted the food item at that moment under sleep rested and sleep deprived conditions.