Monday, September 3, 2012

Why We Are Slaves Of Food Obsession.

A 95 years old psychology article holds the key to solving the obesity epidemic. It's not about a long forgotten medicine or an ancient psycho-trick. It's a simple observation about the dynamics of feeding. Vindicated by neurohormonal research, here is what it means to your struggle with extra pounds. [tweet this].

When Wallace Craig dissected the feeding behavior of doves, his experimental animal of choice, he discovered the existence of two distinct phases - an appetitive and a consummatory phase [1].  He defined appetite as "a state of agitation", which continues until food is presented, whereupon phase 2 begins. That's the phase you and I call eating. It's followed by a third phase of relative rest, which Craig called the state of satisfaction. You are forgiven if you now ask "what science nugget could possibly be hidden in this platitude". But the best-hidden gems are often those, which are in plain sight. In this case it's nothing less than the model explaining why so many of us wear dress sizes, ranging from "XL" to "Oh my God, look at this!", while none of us actually wants to be seen in them.  

Before I get to the beauty of Craig's observation, let me also tell you what's the acid test for any biological model: it must make sense in evolutionary biology. If it does, it still may not be the final word, but if it doesn't we can safely discard it into the heap of wishful thinking. Keeping this in mind, let's get cracking.

When Craig published his paper in 1917 he described the behaviors of his doves as instinctive. In other words, being driven by some innate processes which require no conscious decision making nor any degree of intellect. Today we know a lot more about those "innate processes", particularly that they are the result of a complex conversation between neurons and hormones playing out in the recesses of the animal brain. Not only do we know the chains of command running from brain centre to periphery we also know the hormones (at least some of them) by names, such as Neuropeptide Y (NPY) or Leptin. You don't need to remember them. What you need to remember is that "instinctive" has matured from a black box stage to the stage of neurohormonal mechanisms, which can be tested quantitatively in the lab with experimental animals. 

As you may have guessed, I didn't mention NPY and leptin by chance. Both are relatively new kids on the block, with NPY having been discovered in 1982, followed by leptin 12 years later.  Now what do they have to do with eating behavior?

NPY is the most potent "orexigenic" peptide currently known. That's science speak for appetite stimulating peptide. Now you also know what it means when I tell you that leptin's effect is just the opposite, that is, anorexigenic, or appetite suppressant. Inject NPY into the right places of a rat's brain and it will turn into a voracious eater. Give obese rats leptin, and they slim down.   
Wonderful, you might say, so we do have a cure for obesity. That's what researchers thought, too. But it turned out that leptin administration does not help overweight people to lose weight. That's one of the problems with animal experiments: What works in rats does not necessarily work in man, even if our behaviors are often indistinguishable. 

Back to our feeding issue. With ethics boards being as they are, we won't get their approval for experimental NPY injections into people's brains just to watch their eating behaviors. But we do know that NPY is operational in humans as much as in rats and many other animals, and within the same brain centers. So, a rat model is still our best bet at studying how hormones affect human feeding habits. 
Now, one of behavioral sciences' problems with animal experiments in the lab is that an animal, which is kept in a cage, is not a good model for that animal's behavior under free-living conditions. Of relevance to our topic is the free-living animal's need to procure food before it can consume it. This go-and-get-food stage typically involves a fair amount of foraging or hunting, depending on the type of animal and its position on the food chain. It's what Craig had called the state of agitation of his captive doves. How is all this relevant to NPY's orexigenic role? Well, in 1995 Seely and his colleagues wanted to know exactly how NPY does its fattening job [2]. In an experiment they discovered that NPY injection did not increase the amount of food rats ingested from an orally injected sugar solution. What they did increase was their trips to a bottle from which they had been trained to take food (sugar solution). In other words, NPY sort of activated the rats go-get-food autopilot, but it didn't drive them to ingest more food when this food was presented intra-orally.  

That's when the first suspicions arose that the equation "NPY=feeding frenzy" is not as straight forward as it had seemed. In an ingeniously designed experiment with lab rats Ammar and colleagues wanted to see whether and how NPY and leptin affect the appetitive and the consummatory aspect of feeding behavior differently [3]. 

The results of this experiment show a much more complex hormonal effect of NPY and leptin than what had previously been thought. While NPY infusion made rats increase their physical activity to get food it inhibited their intake of food, when it was made available to them by oral infusion while they  were on the "go-get" for food. Just the opposite was the case with leptin. While leptin made rats drop their efforts to get food, it made them increase their intake of food when it was delivered by oral infusion. The researchers experimented with male rats exclusively, not because they thought that females would react differently, but because they wanted to see how specific the effect of NPY is on the animal's drive to become physically active. So they used the one stimulus with the best track record of throwing males off any course of action, regardless whether those males are rats or men: the presence of a sexually receptive female. Now, this must be very illuminating to my female readers: under the influence of NPY male rats were "more into food than into females" so to speak. Definitely more than when NPY was taken out of the equation. 

Just as an aside: what does this mean for women's belief that men are operating under one of three mindsets: "I'm hungry, I'm thirsty, I'm horny"? It means that the order of priority is obviously determined more by hormones such as NPY, than by female manipulation. Of course, as I already mentioned, rats are not necessarily a template for human biology. Which is why we should hope, for the sake of female rodents, that their male peers' mindsets are a little more sophisticated than what human females observe in their male counterparts. 

But let's not talk rats for a while, let's talk humans. More specifically humans in what was their natural habitat throughout 99% of our evolution: the pre-agricultural world which our ancestors had roamed as hunter/gatherers. In this world it will have made great sense to be kick-started into a go-get-food mood when one's energy reserves began to deplete. And it would have made equally great sense to have one's pre-occupation with food knocked down a few pegs once energy reserves have been replenished. 
Interestingly, the circuitry which accomplishes this behavioral feat has been preserved over the eons of evolution, from mouse to man. And in this circuitry we find the same hormones, NPY and leptin, playing essentially the same roles, too. Obviously this neurohormonal architecture has been a recipe for survival throughout the evolution of species. It is easy to see how evolution had trained this architecture to align every species' feeding behavior (a) with its energy needs, (b) with the energy density of the food available to it, and (c) with the effort necessary to get this food.
Now here is where it all comes together in our obesity plagued times: in our modern environment this inherited circuitry has turned from an asset into a liability. What use is NPY's drive to get physically active for the procurement of food, when the necessary physical activity has been reduced from spear-hunting a deer to opening the fridge? What use is NPY signaling the reduction of energy stores when your and my stores are too high in the first place? What use is leptin's stimulative effect on eating once food is available, when food is available everywhere and all the time? Not only have these drives become useless, they have become hazardous to our health. I'll spare you the proof: The much quoted statistics of overweight and obesity. 

When Wallace Craig first painted the architecture of feeding 95 years ago, obesity wasn't a problem at all. Now you might say "Wait a minute, his generation wasn't exactly the hunter/gatherer type. If all this talk about hormones and feeding behavior is correct, why were they not fat?" Good point. One part of the answer is, that the obesity epidemic has been paralleled by an epidemic of rapidly declining physical activity. The other part of the answer is, again, a hormonal circuitry. A much more dangerous one. I will address it in my next post, and then we will construct a comprehensive model of feeding behaviour which not only explains your personal failures, or triumphs, in your personal war against the XL  sizes. It will also explain why and how, despite all those inherited neurhormonal mechansims driving our feeding behavior, you still can win this war. [tweet this].    

1. Craig W: Appetites and Aversions as Constituents of Instincts. Proc Natl Acad Sci U S A 1917, 3(12):685-688.
2. Seeley RJ, Payne CJ, Woods SC: Neuropeptide Y fails to increase intraoral intake in rats. Am J Physiol 1995, 268(2 Pt 2):R423-427.
3. Ammar AA, Sederholm F, Saito TR, Scheurink AJ, Johnson AE, Sodersten P: NPY-leptin: opposing effects on appetitive and consummatory ingestive behavior and sexual behavior. American journal of physiology Regulatory, integrative and comparative physiology 2000, 278(6):R1627-1633.

Craig W (1917). Appetites and Aversions as Constituents of Instincts. Proceedings of the National Academy of Sciences of the United States of America, 3 (12), 685-8 PMID: 16586767

Seeley RJ, Payne CJ, & Woods SC (1995). Neuropeptide Y fails to increase intraoral intake in rats. The American journal of physiology, 268 (2 Pt 2) PMID: 7864237

Ammar AA, Sederholm F, Saito TR, Scheurink AJ, Johnson AE, & Södersten P (2000). NPY-leptin: opposing effects on appetitive and consummatory ingestive behavior and sexual behavior. American journal of physiology. Regulatory, integrative and comparative physiology, 278 (6) PMID: 10848532
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