Is It Me or My Hormones?

Neuroendocrine Activation Profiles to Visual Food Stimuli Across the Menstrual Cycle

Yardena Arnoni-Bauer; Atira Bick; Noa Raz; Tal Imbar; Shoshana Amos; Orly Agmon; Limor Marko; Netta Levin and Ram Weiss

Disclosures

J Clin Endocrinol Metab. 2017;102(9):3406-3414. 

In This Article

Abstract and Introduction

Abstract

Context: Homeostatic energy balance is controlled via the hypothalamus, whereas regions controlling reward and cognitive decision-making are critical for hedonic eating. Eating varies across the menstrual cycle peaking at the midluteal phase.

Objective: To test responses of females with regular cycles during midfollicular and midluteal phase and of users of monophasic oral contraception pills (OCPs) to visual food cues.

Design: Participants performed a functional magnetic resonance imaging while exposed to visual food cues in four time points: fasting and fed conditions in midfollicular and midluteal phases.

Patients: Twenty females with regular cycles and 12 on monophasic OCP, aged 18 to 35 years.

Main Outcome Measures: Activity in homeostatic (hypothalamus), reward (amygdala, putamen and insula), frontal (anterior cingulate cortex, dorsolateral prefrontal cortex), and visual regions (calcarine and lateral occipital cortex).

Setting: Tertiary hospital.

Results: In females with regular cycles, brain regions associated with homeostasis but also the reward system, executive frontal areas, and afferent visual areas were activated to a greater degree during the luteal compared with the follicular phase. Within the visual areas, a dual effect of hormonal and prandial state was seen. In females on monophasic OCPs, characterized by a permanently elevated progesterone concentration, activity reminiscent of the luteal phase was found. Androgen, cortisol, testosterone, and insulin levels were significantly correlated with reward and visual region activation.

Conclusions: Hormonal mechanisms affect the responses of women's homeostatic, emotional, and attentional brain regions to food cues. The relation of these findings to eating behavior throughout the cycle needs further investigation.

Introduction

Food consumption and eating behavior are driven by a complex interaction of hormones and metabolites in multiple brain areas[1] influenced by homeostatic as well as hedonistic signals. Homeostatic cues may signal positive or negative energy balance, whereas hedonistic cues indicate palatability and reward.[2] The brain faces multiple hormonal and biochemical signals from organs, but also nonhomeostatic signals from the environment, and coordinates caloric intake and energy expenditure based on the integration of these cues.[3] Brain regions involved in homeostasis as well as reward responses have sex hormone receptors for estrogen and progesterone, making these hormones' active participants in the coordination of eating behavior via affecting gene expression of relevant molecules.[4–6]

Studies in primates and humans have shown that eating patterns vary across the menstrual cycle, reaching a peak at the midluteal phase compared with the follicular phase.[7,8] Such fluctuations in food intake in humans reach on average ~250 kcal/d, yet may exceed 500 kcal/d,[9] and are considered part of the attempt to meet the needs of the possible pregnancy. However, the physiological mechanism of this phenomenon is unknown. Because obesity is considered the epidemic of the 21st century[10] and because the majority of dietary regimens eventually fail in the long run,[11] there is growing interest in unraveling mechanisms that drive and modulate eating behavior.[7] To unravel mechanistic insights into the differential eating patterns during the menstrual cycle, we tested hormonal levels and functional magnetic resonance imaging (fMRI) brain responses to visual food cues of lean females with a regular cycle during midfollicular and midluteal phases.[12] An additional group of females on monophasic oral contraception pills (OCPs), characterized by a stable elevated progesterone analog level reminiscent of the luteal phase of regularly cycling females, was studied as well. Activity in homeostatic, reward, and decision-making regions as well as in afferent (visual) cortex was assessed. The responses were evaluated in two prandial states (fasting and fed ("fed" representing the period following glucose ingestion).

We postulated that unique brain pattern activity mediated by the hormonal profile may explain the different eating behavior along the menstrual cycle. We postulated that sex hormones, specifically progesterone, modulate brain reward region activation that will be increased in the luteal phase. Furthermore, we anticipated the presence of uniform brain reward activation throughout the cycle in females on monophasic oral contraception, that will be similar the luteal phase of regularly cycling females.

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