Elsevier

Appetite

Volume 45, Issue 2, October 2005, Pages 177-181
Appetite

Brief Communication
Exercise energy expenditure is not consciously detected due to oro-gastric, not metabolic, basis of hunger sensation

https://doi.org/10.1016/j.appet.2005.01.012Get rights and content

Abstract

We tested the hypothesis that exercise energy expenditure (EEE) will elicit reflex metabolic compensations but no increases in hunger. Exercise expended 800 kcal once when fasted and at another time in a post-prandial state. During fasting exercise, pre-meal ratings of hunger were unaffected by EEE, but plasma concentrations of ghrelin, growth hormone and free fatty acids were higher than in the absence of EEE. We propose that the perception of hunger is based on the vagal, lateral hypothalamic and cortical projections of oral and gastro-intestinal (GI) stimuli and that EEE triggers neuroendocrine compensations and influences hunger indirectly by affecting GI functions.

Introduction

Of central interest to students of energy regulation is the relationship of the psychophysical sensation of hunger to metabolic energy needs. Attempts to gaining a better understanding of the connection between hunger and metabolic status have taken two very different approaches. One asserts that hunger represents conscious sensing of reduced energy availability, and that the meal taking reflects the magnitude of energy need in accordance with a homeostatic negative feedback concept. Supporting evidence includes (1) correlations between declines in plasma glucose concentration and meal initiation (Campfield et al., 1996, Melanson et al., 1999), (2) increased frequency of meal initiation and larger meal sizes in animals in response to substantial caloric restriction (Larue-Achagiotis & Le Magnen, 1980), and to (3) elicitation of eating after pharmacological blockade of carbohydrate (Ritter, Dinh, & Zhang, 2000) and lipid metabolism (Tu et al., 2005) in the central nervous system. These data suggest that glucoprivation or reduced lipid utilization is detected by the brain, and the degree of negative energy balance is communicated to hypothalamic and cortical circuits responsible for perception of hunger and elicitation of feeding. Another version of this view invests hormonal messengers ghrelin (Cummings et al., 2001) and leptin (Shintani et al., 2001) with communication of the magnitude of energy deficit to orexigenic peptides in the hypothalamus, such as neuropeptide Y, galanin, MCH, orexin (Schwartz et al., 2000) and cortical circuits responsible for conscious perception of hunger.

The alternative view is that hunger is an opportunistic, non-homeostatic response to circadian, olfactory, and alimentary sensory cues and to positive environmental and social circumstances, which ends following signals of gastro-intestinal repletion or perceptions of negative and stressful environmental circumstances. Evidence in favor of the non-homeostatic view includes (1) ultradian and circadian periodicity of meal taking (Cugini, Battisti, & Di Palma, 1991), (2) direct relationships of meal size to palatability of food (De Castro et al., 2000, Louis-Sylvestre et al., 1984), the variety of food stimuli (Le Magnen, 1999) or the degree of gastric volume depletion (Sturm et al., 2004); (3) relative constancy of meal volumes in the face of variable energy density of food (Lissner, Levitsky, Strupp, Kalkwarf, & Roe, 1987), and of increased (Stubbs et al., 2002) or decreased (Stubbs et al., 2004) volume of EEE; and (4) social facilitation of meal size (De Castro, 1997). We provide evidence consistent with the non-homeostatic alternative and present a hypothetical model allowing for integration of the non-homeostatic meal eating and homeostatic regulation of energy balance.

Since metabolic EEE does produce negative energy balance, we have examined perception of hunger in an experiment (to be reported separately in more detail) that generates an 800 kcal EEE. We hypothesized that EEE is not consciously detected but triggers compensatory reflexes for regulation of circulating metabolic fuels. Our specific aims were to measure (1) the psychophysical ratings of hunger and satiety using visual analog scales (VAS), (2) hormonal mediation of hunger and satiety using measurements of plasma insulin, ghrelin, growth hormone (GH) and cholecystokinin (CCK), and (3) metabolic reflexes using measurements of plasma glucose and free fatty acids (FFAs). Finally, to determine whether EEE alters secretion of the putative energy-status messengers insulin, ghrelin, GH, and CCK, we arranged for exercise to be performed on one occasion in a fasted and post-absorptive (FAST) state characterized by low levels of insulin and CCK, but high ghrelin and GH, and on another occasion in the post-prandial (FED) state characterized by high insulin and CCK, but low ghrelin and GH.

Section snippets

Methods

Subjects were 10 overweight but otherwise healthy post-menopausal women. Their age was 59.5±1.3 years (mean±SEM), weight was 75.3±4.58 kg, stature was 1.66±0.02 m, and body mass index was 27.37±1.55 kg/m2. The two meals at 10 and 17 h, provided about 1480 kcal that did not replace the added 800 kcal of EEE. Meals consisted of 63% carbohydrate, 14% protein, and 23% fat. Exercise consisted of two moderate-intensity (40% of maximal effort) walking bouts on a treadmill, one in the morning and the other

Results

EEE of approximately 800 kcal above the RMR did not affect VAS ratings of H, D, or C before the meals. The post-meal decline in these VAS ratings was attenuated after EEE in a FAST state compared to exercise in the FED state.

EEE in the FAST state produced significantly greater pre-meal plasma ghrelin and GH concentrations compared to a pre-meal sedentary FAST condition; and the post-prandial rise in CCK concentration was delayed after EEE in a FAST state compared to exercise in the FED state.

EEE

Discussion

Our results support the hypothesis that EEE is not consciously detected. Two bouts of EEE, each expending 400 kcal, did not affect VAS ratings of H, D, or C despite a significant decline in plasma glucose concentration. These data are consistent with the reported absence of increased hunger to EEE of between 250 and 500 kcal at moderate intensity of 40–50% of maximal effort (Stubbs et al., 2002). No compensatory consummatory responses were reported within 24 h of EEE (King Burley & Blundell, 1994)

Acknowledgements

Based on a presentation to the Columbia University Seminar on Appetitive Behavior, May 14, 2004, Harry R. Kissileff, Chairman, supported in part by GlaxoSmithKline and the New York Obesity Research Center, St Luke's/Roosevelt Hospital.

This research was supported in part by the grants MO 000543 to the University of Michigan General Clinical Research Center and by the National Science Foundation ADVANCE E. Crosby award.

The Figure is adapted from K. Borer, Exercise Endocrinology, Champaign, Il:

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