Energy homeostasis from Lavoisier to control theory

Abstract

The intellectual history of energy homeostasis, focusing on food intake and energy storage, is briefly reviewed. Physiological energetics was founded by Lavoisier, who in the late eighteenth century invented direct and indirect calorimetry and discovered the role of oxygen in combustion and respiration. Energy was understood well enough by the mid-nineteenth century to realize the physiological energy-balance equation, that energy intake – energy expenditure = energy storage, but this did not greatly influence physiological research for another century. Homeostasis, the concept that many vital physiological variables are actively regulated in narrow envelopes, was developed by Bernard and Cannon between approximately 1870–1940 and remains a central principle of physiology. Kennedy coined the term lipostasis in 1953 to refer to the constancy of fat mass, which Mayer argued was the mechanism regulating body weight. A parameterized control-theory model suggests that a proportional negative-feedback control system incompletely compensates weight loss during persistent negative energy balance, suggesting that Cannon's idea of constancy within a narrow envelope may not fit body-weight regulation well. This modelling encourages further application of control theory to issues in energy homeostasis, including to the development of obesity. It also sets the stage for understanding the underlying neuroendocrine mechanisms. This article is part of a discussion meeting issue ‘Causes of obesity: theories, conjectures and evidence (Part I)’.

Models of body weight and fatness regulation

“…As pointed out by Geary [129] the control theory model can generate a similar pattern of response if there is a setpoint in the middle of the supposed zone of indifference, and a nonlinear feedback gain surrounding this point (fig. 2 in [129]). Geary has suggested that the control model is preferable to the DIP model because of its parsimony and mathematical tractability because it is rooted in a long history of engineering applications.…”

“…The model also explains why the response to leptin is asymmetrical without any need to invoke some mechanisms like 'leptin resistance' to explain it [9]. As pointed out by Geary [129] the control theory model can generate a similar pattern of response if there is a setpoint in the middle of the supposed zone of indifference, and a nonlinear feedback gain surrounding this point (fig. 2 in [129]).…”

“…where K 1 and K 2 are the gains of the control feedback loops and T i is the integral time constant [127][128][129][130].…”

“…Negative feedback has been known since the 1800s and the mathematics concerning such systems is known as 'control theory' (reviewed in [128,129]). The key aspect of such systems is the coupling of the feedback signal to the system under control defined by the magnitude of the 'gain' parameters (K 1 and K 2 ) and the mathematical properties of the feedback signal.…”

“…Second it also implies a set-point at the middle of the zone of indifference (the 0 value in fig. 2 of [129]) for which there is no biological explanation, or biological reality. The 'Hall-Guo' and 'operating point' models can also be formulated to generate behaviour similar to the DIP model.…”