Elsevier

Physiology & Behavior

Volume 103, Issue 5, 6 July 2011, Pages 594-599
Physiology & Behavior

Food anticipation and subsequent food withdrawal increase serum cortisol in healthy men

https://doi.org/10.1016/j.physbeh.2011.04.020Get rights and content

Abstract

The anticipation of food intake comprises endocrine changes that according to animal experiments include a rise in HPA axis activity. In humans, HPA axis responses to food anticipation and withdrawal, although of clinical relevance, have not been thoroughly examined. We assessed neuroendocrine and psychological effects of food anticipation and of withholding anticipated food in healthy human subjects. Food anticipation was induced in 14 men at 0800 h by the announcement and subsequent presentation of a breakfast buffet. The expected meal was surprisingly withheld at 1000 h under the pretense of an organizational problem. Fifteen fasted controls were informed at 0800 h that they would remain fasted throughout the experiments. In both groups, hunger, mood and circulating concentrations of glucose, insulin, cortisol, ACTH, leptin and ghrelin were assessed. At 1200 h, all subjects were allowed to eat from a plate of cookies. Compared to non-anticipation, food anticipation was associated with a relative increase in serum cortisol levels, an acute drop in plasma glucose and increased self-rated hunger. When anticipated food was withheld, self-rated mood deteriorated and cortisol levels remained elevated, while plasma glucose levels decreased with a delay of 50 min. Other endocrine parameters and cookie intake were comparable between groups. Our results indicate that food anticipation without subsequent food reward increases cortisol levels and reduces blood glucose availability. They support the assumption that dietary restraint, being associated with habitually extended periods of anticipating food that is temporarily withheld, may contribute to the development of overweight by detrimental effects on HPA-axis activity.

Research highlights

► Food anticipation increases serum cortisol concentrations in healthy men. ► Withholding anticipated food intake decreases blood glucose levels in men. ► Dietary restraint might favor obesity via detrimental neuroendocrine effects. ► Breakfast anticipation might be a determinant of the cortisol awakening response.

Introduction

The anticipation of food comprises a pattern of metabolic and physiological reactions known as ‘cephalic phase’ responses [1], [2], [3]. Most prominently, a preprandial rise in gastric acid secretion [4], enhanced insulin secretion [5], a drop in blood glucose levels [6] and a rise in ghrelin levels [7] have been assumed to represent food anticipatory mechanisms. These responses may be interpreted as an early activation of postprandial metabolism, i.e., the organism's attempt to facilitate the imminent digestion and absorption of nutrients [1].

Animal studies furthermore suggest a modulating influence of food anticipation on hypothalamic-pituitary-adrenal (HPA) axis activity (for review see ref. 8). In meal entrainment paradigms based on restricted feeding, rodents display a corticosterone peak before food intake [9], [10] that has likewise been found under free-living conditions in doe rabbit pups [11]. Thus, it has been a long-held assumption that food anticipation in humans is associated with increased cortisol secretion as well [12]. To the best of our knowledge, however, this assumption lacks straight-forward experimental evidence inasmuch earlier studies focused on rises in HPA axis activity emerging in parallel with food intake or on the non-anticipatory presentation of food stimuli [13], [14], [15]. Moreover, most human [16], [17] and in particular animal experimental studies [7], [9], [10], [18] have investigated food anticipatory responses by conditioning and meal entrainment paradigms in which the valuation of anticipated food reward is a function of previous experience. In contrast, the physiological responses elicited by instructed anticipation, i.e. by giving the simple information that food is to be expected within a certain time period, as often found in everyday situations, are largely unexplored. Likewise, neuroendocrine coping reactions to the withdrawal of anticipated food – that may be expected to include a stress-related increase in HPA axis activity – have received little attention so far. However, this issue is of clinical relevance given that dietary restraint, which is characterized by extended periods of food anticipation and self-imposed food withdrawal [19], is a common phenomenon in our obesigenic environment and has been reported to be associated with elevated cortisol concentrations [20]. In order to test the hypothesis that food anticipation is associated with an increase in circulating cortisol levels, we investigated the effect of food anticipation induced by meal announcement and of the subsequent withholding of anticipated food on neuroendocrine and behavioral parameters in healthy men.

Section snippets

Subjects

Experiments were conducted in 30 healthy, normal-weight men (body mass index, BMI, mean ± SEM: 22.8 ± 0.28 kg/m2) aged 18 to 34 years who were recruited by posters and flyers on campus and by ads in the local newspapers. They were non-smokers and did not show signs of habitual dietary restraint as assessed by the German version of the Three Factor Eating Questionnaire [21]. Subjects were informed that the study focused on the relationship between blood parameters and cognition but were unaware that

Behavioral parameters

At baseline, all behavioral parameters were comparable between groups (all p > 0.21). Food anticipation (0800–1000 h) strongly increased rated hunger (p < 0.001; Fig. 1A) and thirst (p < 0.02), but did not influence sleepiness and anxiety ratings (all p > 0.3). In the Anticipation compared to the No Anticipation group, MDBF scales indicated a slight increase in agitation during food anticipation (p < 0.06; Fig. 1B). The unexpected announcement at 1000 h that no breakfast would be served was associated with

Discussion

Food anticipatory ‘cephalic phase’ responses are determined by the sensory modalities involved and the intensity of anticipatory stimuli [4]. We demonstrate that anticipatory responses including a strong increase in hunger ratings can be successfully prompted in an acute setting by formally instructing subjects to expect meal intake. Notably, our approach was based on the simple announcement of a meal along with the visual and olfactory presentation of food items and, in contrast to previous

Acknowledgements

We thank Janna-Marit Zemlin for her expert assistance and Kirstin Nordhausen and Jutta Schwanbom for their invaluable laboratory work. Supported by Deutsche Forschungsgemeinschaft (KFO 126/B5). The funding source had no input in the design and conduct of this study; in the collection, analysis, and interpretation of the data, or in the preparation, review, or approval of the manuscript.

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