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The paradox of satiation
Physiology & Behavior 82 (2004) 149 – 153
The paradox of satiation George Colliera,*, Deanne F. Johnsonb a
Rutgers, The State University of New Jersey, USA b Princeton University, Princeton, NJ, USA Received 1 March 2004; accepted 2 April 2004
Abstract Animals behave in bouts, and the process that causes feeding bouts to end is called satiation. Bout size or, in the case of feeding, meal size is the result both of the costs of food resources and the consequences of consuming a particular resource. Meal size increases as a function of increasing resource access cost; in this way, meal size is part of a strategy that economizes on time and energy spent acquiring food resources, thereby making time and effort available for competing activities. Meal size also varies as a function of the amount of the resource consumed and the animal’s requirements for that resource. The paradox of satiation is that it is both a tool for economizing and a consequence of feeding. D 2004 Elsevier Inc. All rights reserved. Keywords: Satiation; Meal size; Feeding bouts
1. Introduction Perhaps, the earliest account of satiation was by Plato in the dialogue, Timaeus: Those who framed our species know how ungovernable our appetite for drink and food would be, and how we should out of sheer greed consume more than a moderate or necessary amount; in order therefore to prevent our rapid destruction by disease and the prompt and untimely disappearance of our species, they made the lower belly, as it is called, into a receptacle to contain superfluous food and drink, and wound the bowels around in coils, thus preventing the quick passage of food, which would otherwise compel the body to want more and make its appetite insatiable, so rendering our species thru gluttony incapable of philosophy and culture, and unwilling to listen to the divinest element in us (Ref. [18], p. 100). Plato included all the elements of current accounts of feeding: Food and drink are consumed in meals, the stomach acts as a storage organ, and there are proximal * Corresponding author. Department of Psychology, Rutgers University, 152 Frelinghuysen Road, Piscataway, NJ 08854, USA. Tel.: +1-732445-2510; fax: +1-732-445-2263. E-mail address: [email protected] (G. Collier). 0031-9384/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2004.04.041
mechanisms for terminating meals. He even developed a semiecological account of its causation. He asked the two fundamental questions in biology: why and how [14]. The first, he answered with an appreciation of philosophy and culture. The second, he answered with an anatomical mechanism: coiled bowels, which slow the rate of the stomach emptying. For more recent reviews of proximal mechanisms, see Refs. [24,26]. The present account considers the why of satiation. It is our thesis that the range of meal sizes (and meal timing and frequencies, rates of consumption, and total intake) available to an animal is one aspect of its species’ adaptation to its niche and that meal size is adjusted by the individual animal according to the demands of its current habitat. The neglect of the why is often the result of the experimental paradigm in which satiation is typically studied. Classic laboratory studies are performed in an open economy, in which the experimenter provides the venue (experimental chamber), determines the session length and intersession interval, chooses and supplies the nutrient(s), and deprives (extends the intermeal interval) or depletes (reduces the body weight of) the animal. The rate and total consumption are studied as a function of the quality and kind of the nutrient and state of deprivation or depletion. These studies have been used to determine the direct or proximal causation of feeding patterns [24]. A second paradigm involves laboratory studies in closed economies
150
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
with freely feeding animals, in which the experimenter again provides the venue and chooses and supplies the nutrient(s), but the animal feeds in self-determined, multiple sessions (meals), determines the session (meal) length and intersession (intermeal) interval, and may or may not deprive or deplete itself. Meal parameters (frequency and size of meals, rate of ingestion, total, and intake) and body composition and size are studied to examine the determinants of the initiation and termination of meals, diet balancing, and the regulation of intake. Two additional paradigms have been used less often. One is a foraging paradigm, which is like the free-feeding paradigm, but in which the animal is additionally required to earn access to and to consume the nutrient(s). The effect of the costs of access and of consumption on meal parameters, diet balancing, and regulation of intake are studied. Finally, in field studies, freely feeding animals in their natural habitat choose the venue, the time and place, the nutrients, and their meal patterns and regulate their intake. Field studies may examine the indirect or ultimate causes of feeding patterns (e.g., Ref. [17]). These different methodologies yield radically different accounts of the determinants of feeding patterns [4]. As one proceeds from experimenter to animal control, the pattern of feeding becomes more and more a means of solving niche problems. The animal’s behavior begins to reveal how its species has evolved to exploit resources; thus, we learn more and more about the why—the ultimate causation of feeding patterns [14]. Individuals in variable, competitive, natural settings face nine imperatives in feeding behavior. For each feeding bout, they must (1) initiate the bout, (2) discover and identify a food resource (evolutionarily determined and niche-specific), (3) procure access to or capture the resource, (4) consume the resource, (5) terminate the bout, and (6) process the ingestant (Fig. 1). Throughout these processes, they must (7) avoid predators and defeat competitors, and, over a longer time frame, they also must (8) regulate their energy balance and (9) economize [17,23]. Of the many variables that define the parameters of a niche and affect meal patterns, we shall only consider costs, i.e., the time and energy an animal expends foraging for and consuming food. The role of costs within a niche became apparent to us when we were attempting to replicate the free-feeding model of Le
Fig. 1. The chain of behavior involved in feeding.
Magnen [13] in our laboratory paradigm. We developed an operant procedure in which the animal is required to make instrumental responses, e.g., bar presses, to procure access to a feeder at the initiation of a meal, and then to make instrumental responses to earn small portions to consume within the meal. We find that foraging and consumption costs have profound, but different, systematic effects on meal patterns.
2. Foraging Increasing capture or procurement costs results in a monotonic decrease in the frequency of initiating meals and a compensatory increase in meal size; the outcome is conservation of total intake. We have observed this function for all species tested (Fig. 2). What differs among the species is the maximum meal size and, thus, the maximum length of the intermeal interval. Maximum meal size depends upon storage capacity, e.g., stomach, crop, gut, or fat storage, etc., which are species-specific characteristics. For example, if it is to conserve daily intake, a rat must eat at least once a day, while a chicken can eat enough in one meal to last two days, and a cat can eat one meal every three or four days [3,6,12]. This cost-sensitive foraging strategy preserves intake while conserving both the number of instrumental responses and the time to access a meal as foraging costs increase. That is, reducing meal frequency means fewer responses and less time spent foraging than if meal frequency did not change. These functions occur in natural settings as well. For example, lions initiate the pursuit of game less often as the game becomes larger, scarcer, or more difficult to capture. However, as capture frequency declines, the amount consumed increases: Lions can consume more than 30% of their body weight after a successful capture [21]. Likewise, camels consume more water as the travel distance to a water hole increases. They, too, can consume up to 30% of their weight in water as access cost increases [22]. Numerous other examples can be adduced that show that adjustments in meal size and meal timing can be cost-saving solutions to niche problems: Diurnal chickens consume a large meal at the end of the light phase, apparently anticipating the nocturnal fast [25]. Furthermore, if the cost of food is lower, or the quality is greater, at night than during the day, then, they will eat large meals at night [19]. Similarly, nocturnal rats will shift to diurnal feeding, with larger meals occurring during the light, when the cost is greater at night [8]. Rats also will eat more frequent meals on days when costs are low compared with days when costs are high [16]. A final example is seen in many animals who must cope with seasonal differences in resource density. These animals manage their energy balance over a long time frame: During abundant seasons, they eat very large meals and store the nutrients, and then, these reserves see them
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
Fig. 2. Meal frequency, meal size, and daily intake as functions of increases in the cost of procuring access to food at the start of each meal.
through the lean times, when they eat infrequently or not at all [1,15].
151
the patch with larger pellets, the rats respond faster at that patch, but intake rate falls. Because the intake rate at the small-pellet patch does not change, when the price is high enough, the rats consume food faster at the small-pellet patch than at the large-pellet patch. In conjunction with this change in the cost and intake rate at the patches, the rat gradually shifts to eating more food at the patch with smaller pellets. This occurs via changes in acceptance and meal size at both patches, although the cost is only changing for the larger pellets. The rat rejects more opportunities at that patch and accepts more opportunities at the small-pellet patch, and it eats smaller meals of large pellets and larger meals of small pellets (Fig. 3). Note that this means that the amount of food that satiates the rat differs depending on which patch it happens to be eating from at the time. These functions can be understood as the behavior that tends to increase profitability (g/response or g/min) [9,10]. In this paradigm, where the rat can control costs by choosing the most cost-effective place to eat, the total daily intake from both patches remains constant despite the widely differing intake patterns. The generality of these results is demonstrated by the fact that rats
3. Consumption Changes in the cost of earning each portion (bites, sips, etc.) within a meal do not have the same effect as do changes in the cost of meal initiation [3]. There are much smaller effects on meal patterns. In this case, increasing consumption cost causes a modest decrease in meal size and an increase in meal frequency. Furthermore, these changes are often not compensatory, and both total intake and body weight are reduced at higher costs (Fig. 4). The most striking effect of increasing consumption cost is on the rate of instrumental responding—a behavior not affected at all by procurement cost. As consumption cost increases, response rate also increases. The change is not sufficient to compensate for the greater number of responses required, and hence, the rate of actual intake falls as cost increases [9]. However, the decrease in intake rate is not as great as it would be if response rate remained constant, thus, the animal’s behavior is a time-saving strategy. Consumption cost can be increased by requiring more responses per portion or by decreasing portion size, and both of these manipulations produce increases in response rate [5]. Note that this result (faster responding for smaller or more expensive portions) is exactly opposite to the prediction of the classic law of magnitude of reinforcement that describes behavior in open economies. All of these relations are illustrated in a choice paradigm in which rats searched for successive ‘‘food patches’’ where they can eat a meal; they could accept or reject each encountered patch. The patches differ in the size of their food portions (20-, 45-, or 94-mg pellets) and the bar-press price of each portion. When the pellet cost is equal at the patches, rats eat faster, accept a greater proportion of meal opportunities, eat larger meals, and, thus, eat more food daily at the patch with larger pellets. As the pellet cost increases at
Fig. 3. Acceptance of feeding (meal) opportunities and meal size in a twopatch habitat where the patches differ in the size of food pellets and the price of each pellet within the meal.
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G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
results require satiety mechanisms other than those normally considered. These data from freely feeding, foraging rats illustrate that there is a range of meal patterns that an animal may exhibit, and that the pattern that is seen at any particular time is a function of species-specific niche adaptations and habitat variables. The functions raise questions that have yet to be answered by current accounts of satiation:
Fig. 4. The mean ( F S.E.) rate of intake across meals (divided into deciles) of four rats earning 15-s sips of 16% sucrose solution at a price of 1 bar press per sip (a) or 45-mg chow pellets at a price of 10 bar presses per pellet (b). Rats had ad libitum access to both foods. With sucrose solution, standard chow was also available at no cost. Average rate is the number of items earned divided by the length of the decile; local rate excludes pauses in responding longer than 15 s.
(1) What are the proximal, physiological mechanisms that produce these economically determined feeding patterns? Clearly, meal frequency and size, rate of eating, and distribution of meals are, at least in part, functions of the economics of the animal’s niche and current habitat and are devoted to the efficient acquisition of resources [17,23]. The fact that meal size and intermeal interval can vary so widely in one individual requires a different or expanded account of satiety and satiation than is provided by the homoeostatic accounts of meal initiation and termination. For example, what mechanism allows an animal to ignore satiety signals that may normally limit meal size so that it can eat a large meal when that is the cost-effective strategy? (2) By what physiological mechanisms does the animal respond to the varying patterns of nutrient intake dictated by economical resource use? How do the varying eating rates and frequencies, sizes, and distributions of meals cumulate in a constant overall intake? What are the mechanisms that compare energy expenditure and energy intake? Over what time period do they operate and to what extent is the animal’s behavior anticipatory and to what extent reactive? Our attempts to discover the correlations, prandial and/or temporal, have been unsuccessful [2]. The paradox of satiation is that it is both a consequence of feeding and a tool for adapting to different feeding habitats and niches.
4. Perspectives foraging for water instead of food in this two-patch paradigm show the same functions relating patch choice and meal size to profitability [11]. As was the case for procurement costs, responses to consumption costs reveal that size and other meal parameters are functions of niche parameters, indirect causes, as well as direct or proximal mechanisms. We can also look at behavior across the meal for clues about the determinants of satiation. Most homeostatic accounts predict that the rate of food intake will decline as a meal progresses until, finally, ingestion ceases, and such is the case in animals tested in the classic, open-economy paradigm [7]. However, in freely feeding rats, the rate of intake is constant across a meal. The rat does not gradually slow down; rather, it eats and then abruptly stops. This is illustrated by data from rats earning 45 mg chow pellets or 15-s sips of sucrose solution (Fig. 4) and by a study of the microstructure of drinking in freely feeding rats [20]. These
In the development and evolution of my understanding of feeding behavior, Gerry Smith was a teacher, a stringent critic, and a supporter, encouraging my wayward, out-ofthe-mainstream thinking. He was a model of programmatic research, pursuing the ingestant from tongue to pylorus, ever concerned with (of course) the associated mechanisms of satiety. He epitomized what a Good Scientist should be and was the model for many of us. He was—and is my friend. G.C.
References [1] Belovsky GE. Diet optimization in a generalist herbivore: the moose. Theor Popul Biol 1978;14:105 – 34. [2] Collier G. The dialogue between the house economist and the resident physiologist. Nutr Behav 1986;3:9 – 26.
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153 [3] Collier G, Johnson DF. The time window of feeding. Physiol Behav 1990;48:771 – 7. [4] Collier G, Johnson DF. Who is in charge? Animal vs. experimenter control. Appetite 1997;29:159 – 80. [5] Collier G, Johnson DF, Morgan C. The magnitude of reinforcement function in closed and open economies. J Exp Anal Behav 1992; 57:81 – 9. [6] Collier G, Kaufman LW, Kanarek R, Fagen J. Optimization of time and energy constraints in the feeding behavior of cats. Carnivore 1978;1:34 – 41. [7] Davis JD. Measuring satiety: from meal size to the microstructure of ingestive behavior. In: Smith GP, editor. Satiation; from gut to brain. New York: Oxford, 1998. p. 71 – 96. [8] Jensen GB, Collier G, Medvin MB. A cost-benefit analysis of nocturnal feeding in the rat. Physiol Behav 1983;31:555 – 9. [9] Johnson DF, Collier G. Patch choice and meal size of foraging rats as a function of the profitability of food. Anim Behav 1989;38:285 – 97. [10] Johnson DF, Collier G. The relationship between feeding rate and patch choice. J Exp Anal Behav 1991;55:79 – 95. [11] Johnson DF, Collier G. Meal patterns of rats encountering variable procurement cost. Anim Behav 1994;47:1279 – 87. [12] Kaufman LW, Collier GH. Meal-taking by domestic chicks. Anim Behav 1983;31:397 – 403. [13] Le Magnen J. Advances in studies in the physiological control and regulation of food intake. In: Stellar E, Sprague JM, editors. Progress in physiological psychology. New York: Academic Press, 1971. p. 204 – 61.
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[14] Mayr E. The growth of biological thought. Cambridge (MA): Harvard Univ. Press, 1982. [15] Moen AN. Wildlife ecology. San Francisco: Freeman, 1973. [16] Morato S, Johnson DF, Collier G. Feeding patterns of rats when foodaccess cost is alternately low and high. Physiol Behav 1995;57:21 – 6. [17] Owen J. Feeding strategy. Chicago: University of Chicago Press, 1980. [18] Plato, Timaeus and Critias. Middlesex, England: Penguin Books, 1977 (originally written ca. 358, BC). [19] Rovee-Collier CK, Clapp BA, Collier GH. The economics of food choice in chicks. Physiol Behav 1982;28:1097 – 102. [20] Rushing PA, Houpt TA, Henderson RP, Gibbs J. High lick rate is maintained throughout spontaneous liquid meals in freely-feeding rats. Physiol Behav 1997;62:1185 – 8. [21] Schaller GB. The Serengeti lion: a study of predator – prey relations. Chicago: University of Chicago Press, 1972. [22] Schmidt-Nielsen K, Schmidt-Nielsen B, Houpt TR, Jarnum SA. The question of water storage in the stomach of the camel. Mammalia 1956;20:1 – 15. [23] Schoener TW. Theory of feeding strategies. Annu Rev Ecol Syst 1971;2:307 – 43. [24] Smith GPE. Satiation: from gut to brain. New York: Oxford Univ. Press, 1998. [25] Squibb RL, Collier G. Feeding behavior in chicks under three lighting regimens. Poultry Sci 1979;58:641 – 5. [26] Strubbe JH, Woods JC. The timing of meals. Psych Rev 2004;111(1): 128 – 40.
The paradox of satiation George Colliera,*, Deanne F. Johnsonb a
Rutgers, The State University of New Jersey, USA b Princeton University, Princeton, NJ, USA Received 1 March 2004; accepted 2 April 2004
Abstract Animals behave in bouts, and the process that causes feeding bouts to end is called satiation. Bout size or, in the case of feeding, meal size is the result both of the costs of food resources and the consequences of consuming a particular resource. Meal size increases as a function of increasing resource access cost; in this way, meal size is part of a strategy that economizes on time and energy spent acquiring food resources, thereby making time and effort available for competing activities. Meal size also varies as a function of the amount of the resource consumed and the animal’s requirements for that resource. The paradox of satiation is that it is both a tool for economizing and a consequence of feeding. D 2004 Elsevier Inc. All rights reserved. Keywords: Satiation; Meal size; Feeding bouts
1. Introduction Perhaps, the earliest account of satiation was by Plato in the dialogue, Timaeus: Those who framed our species know how ungovernable our appetite for drink and food would be, and how we should out of sheer greed consume more than a moderate or necessary amount; in order therefore to prevent our rapid destruction by disease and the prompt and untimely disappearance of our species, they made the lower belly, as it is called, into a receptacle to contain superfluous food and drink, and wound the bowels around in coils, thus preventing the quick passage of food, which would otherwise compel the body to want more and make its appetite insatiable, so rendering our species thru gluttony incapable of philosophy and culture, and unwilling to listen to the divinest element in us (Ref. [18], p. 100). Plato included all the elements of current accounts of feeding: Food and drink are consumed in meals, the stomach acts as a storage organ, and there are proximal * Corresponding author. Department of Psychology, Rutgers University, 152 Frelinghuysen Road, Piscataway, NJ 08854, USA. Tel.: +1-732445-2510; fax: +1-732-445-2263. E-mail address: [email protected] (G. Collier). 0031-9384/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2004.04.041
mechanisms for terminating meals. He even developed a semiecological account of its causation. He asked the two fundamental questions in biology: why and how [14]. The first, he answered with an appreciation of philosophy and culture. The second, he answered with an anatomical mechanism: coiled bowels, which slow the rate of the stomach emptying. For more recent reviews of proximal mechanisms, see Refs. [24,26]. The present account considers the why of satiation. It is our thesis that the range of meal sizes (and meal timing and frequencies, rates of consumption, and total intake) available to an animal is one aspect of its species’ adaptation to its niche and that meal size is adjusted by the individual animal according to the demands of its current habitat. The neglect of the why is often the result of the experimental paradigm in which satiation is typically studied. Classic laboratory studies are performed in an open economy, in which the experimenter provides the venue (experimental chamber), determines the session length and intersession interval, chooses and supplies the nutrient(s), and deprives (extends the intermeal interval) or depletes (reduces the body weight of) the animal. The rate and total consumption are studied as a function of the quality and kind of the nutrient and state of deprivation or depletion. These studies have been used to determine the direct or proximal causation of feeding patterns [24]. A second paradigm involves laboratory studies in closed economies
150
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
with freely feeding animals, in which the experimenter again provides the venue and chooses and supplies the nutrient(s), but the animal feeds in self-determined, multiple sessions (meals), determines the session (meal) length and intersession (intermeal) interval, and may or may not deprive or deplete itself. Meal parameters (frequency and size of meals, rate of ingestion, total, and intake) and body composition and size are studied to examine the determinants of the initiation and termination of meals, diet balancing, and the regulation of intake. Two additional paradigms have been used less often. One is a foraging paradigm, which is like the free-feeding paradigm, but in which the animal is additionally required to earn access to and to consume the nutrient(s). The effect of the costs of access and of consumption on meal parameters, diet balancing, and regulation of intake are studied. Finally, in field studies, freely feeding animals in their natural habitat choose the venue, the time and place, the nutrients, and their meal patterns and regulate their intake. Field studies may examine the indirect or ultimate causes of feeding patterns (e.g., Ref. [17]). These different methodologies yield radically different accounts of the determinants of feeding patterns [4]. As one proceeds from experimenter to animal control, the pattern of feeding becomes more and more a means of solving niche problems. The animal’s behavior begins to reveal how its species has evolved to exploit resources; thus, we learn more and more about the why—the ultimate causation of feeding patterns [14]. Individuals in variable, competitive, natural settings face nine imperatives in feeding behavior. For each feeding bout, they must (1) initiate the bout, (2) discover and identify a food resource (evolutionarily determined and niche-specific), (3) procure access to or capture the resource, (4) consume the resource, (5) terminate the bout, and (6) process the ingestant (Fig. 1). Throughout these processes, they must (7) avoid predators and defeat competitors, and, over a longer time frame, they also must (8) regulate their energy balance and (9) economize [17,23]. Of the many variables that define the parameters of a niche and affect meal patterns, we shall only consider costs, i.e., the time and energy an animal expends foraging for and consuming food. The role of costs within a niche became apparent to us when we were attempting to replicate the free-feeding model of Le
Fig. 1. The chain of behavior involved in feeding.
Magnen [13] in our laboratory paradigm. We developed an operant procedure in which the animal is required to make instrumental responses, e.g., bar presses, to procure access to a feeder at the initiation of a meal, and then to make instrumental responses to earn small portions to consume within the meal. We find that foraging and consumption costs have profound, but different, systematic effects on meal patterns.
2. Foraging Increasing capture or procurement costs results in a monotonic decrease in the frequency of initiating meals and a compensatory increase in meal size; the outcome is conservation of total intake. We have observed this function for all species tested (Fig. 2). What differs among the species is the maximum meal size and, thus, the maximum length of the intermeal interval. Maximum meal size depends upon storage capacity, e.g., stomach, crop, gut, or fat storage, etc., which are species-specific characteristics. For example, if it is to conserve daily intake, a rat must eat at least once a day, while a chicken can eat enough in one meal to last two days, and a cat can eat one meal every three or four days [3,6,12]. This cost-sensitive foraging strategy preserves intake while conserving both the number of instrumental responses and the time to access a meal as foraging costs increase. That is, reducing meal frequency means fewer responses and less time spent foraging than if meal frequency did not change. These functions occur in natural settings as well. For example, lions initiate the pursuit of game less often as the game becomes larger, scarcer, or more difficult to capture. However, as capture frequency declines, the amount consumed increases: Lions can consume more than 30% of their body weight after a successful capture [21]. Likewise, camels consume more water as the travel distance to a water hole increases. They, too, can consume up to 30% of their weight in water as access cost increases [22]. Numerous other examples can be adduced that show that adjustments in meal size and meal timing can be cost-saving solutions to niche problems: Diurnal chickens consume a large meal at the end of the light phase, apparently anticipating the nocturnal fast [25]. Furthermore, if the cost of food is lower, or the quality is greater, at night than during the day, then, they will eat large meals at night [19]. Similarly, nocturnal rats will shift to diurnal feeding, with larger meals occurring during the light, when the cost is greater at night [8]. Rats also will eat more frequent meals on days when costs are low compared with days when costs are high [16]. A final example is seen in many animals who must cope with seasonal differences in resource density. These animals manage their energy balance over a long time frame: During abundant seasons, they eat very large meals and store the nutrients, and then, these reserves see them
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
Fig. 2. Meal frequency, meal size, and daily intake as functions of increases in the cost of procuring access to food at the start of each meal.
through the lean times, when they eat infrequently or not at all [1,15].
151
the patch with larger pellets, the rats respond faster at that patch, but intake rate falls. Because the intake rate at the small-pellet patch does not change, when the price is high enough, the rats consume food faster at the small-pellet patch than at the large-pellet patch. In conjunction with this change in the cost and intake rate at the patches, the rat gradually shifts to eating more food at the patch with smaller pellets. This occurs via changes in acceptance and meal size at both patches, although the cost is only changing for the larger pellets. The rat rejects more opportunities at that patch and accepts more opportunities at the small-pellet patch, and it eats smaller meals of large pellets and larger meals of small pellets (Fig. 3). Note that this means that the amount of food that satiates the rat differs depending on which patch it happens to be eating from at the time. These functions can be understood as the behavior that tends to increase profitability (g/response or g/min) [9,10]. In this paradigm, where the rat can control costs by choosing the most cost-effective place to eat, the total daily intake from both patches remains constant despite the widely differing intake patterns. The generality of these results is demonstrated by the fact that rats
3. Consumption Changes in the cost of earning each portion (bites, sips, etc.) within a meal do not have the same effect as do changes in the cost of meal initiation [3]. There are much smaller effects on meal patterns. In this case, increasing consumption cost causes a modest decrease in meal size and an increase in meal frequency. Furthermore, these changes are often not compensatory, and both total intake and body weight are reduced at higher costs (Fig. 4). The most striking effect of increasing consumption cost is on the rate of instrumental responding—a behavior not affected at all by procurement cost. As consumption cost increases, response rate also increases. The change is not sufficient to compensate for the greater number of responses required, and hence, the rate of actual intake falls as cost increases [9]. However, the decrease in intake rate is not as great as it would be if response rate remained constant, thus, the animal’s behavior is a time-saving strategy. Consumption cost can be increased by requiring more responses per portion or by decreasing portion size, and both of these manipulations produce increases in response rate [5]. Note that this result (faster responding for smaller or more expensive portions) is exactly opposite to the prediction of the classic law of magnitude of reinforcement that describes behavior in open economies. All of these relations are illustrated in a choice paradigm in which rats searched for successive ‘‘food patches’’ where they can eat a meal; they could accept or reject each encountered patch. The patches differ in the size of their food portions (20-, 45-, or 94-mg pellets) and the bar-press price of each portion. When the pellet cost is equal at the patches, rats eat faster, accept a greater proportion of meal opportunities, eat larger meals, and, thus, eat more food daily at the patch with larger pellets. As the pellet cost increases at
Fig. 3. Acceptance of feeding (meal) opportunities and meal size in a twopatch habitat where the patches differ in the size of food pellets and the price of each pellet within the meal.
152
G. Collier, D.F. Johnson / Physiology & Behavior 82 (2004) 149–153
results require satiety mechanisms other than those normally considered. These data from freely feeding, foraging rats illustrate that there is a range of meal patterns that an animal may exhibit, and that the pattern that is seen at any particular time is a function of species-specific niche adaptations and habitat variables. The functions raise questions that have yet to be answered by current accounts of satiation:
Fig. 4. The mean ( F S.E.) rate of intake across meals (divided into deciles) of four rats earning 15-s sips of 16% sucrose solution at a price of 1 bar press per sip (a) or 45-mg chow pellets at a price of 10 bar presses per pellet (b). Rats had ad libitum access to both foods. With sucrose solution, standard chow was also available at no cost. Average rate is the number of items earned divided by the length of the decile; local rate excludes pauses in responding longer than 15 s.
(1) What are the proximal, physiological mechanisms that produce these economically determined feeding patterns? Clearly, meal frequency and size, rate of eating, and distribution of meals are, at least in part, functions of the economics of the animal’s niche and current habitat and are devoted to the efficient acquisition of resources [17,23]. The fact that meal size and intermeal interval can vary so widely in one individual requires a different or expanded account of satiety and satiation than is provided by the homoeostatic accounts of meal initiation and termination. For example, what mechanism allows an animal to ignore satiety signals that may normally limit meal size so that it can eat a large meal when that is the cost-effective strategy? (2) By what physiological mechanisms does the animal respond to the varying patterns of nutrient intake dictated by economical resource use? How do the varying eating rates and frequencies, sizes, and distributions of meals cumulate in a constant overall intake? What are the mechanisms that compare energy expenditure and energy intake? Over what time period do they operate and to what extent is the animal’s behavior anticipatory and to what extent reactive? Our attempts to discover the correlations, prandial and/or temporal, have been unsuccessful [2]. The paradox of satiation is that it is both a consequence of feeding and a tool for adapting to different feeding habitats and niches.
4. Perspectives foraging for water instead of food in this two-patch paradigm show the same functions relating patch choice and meal size to profitability [11]. As was the case for procurement costs, responses to consumption costs reveal that size and other meal parameters are functions of niche parameters, indirect causes, as well as direct or proximal mechanisms. We can also look at behavior across the meal for clues about the determinants of satiation. Most homeostatic accounts predict that the rate of food intake will decline as a meal progresses until, finally, ingestion ceases, and such is the case in animals tested in the classic, open-economy paradigm [7]. However, in freely feeding rats, the rate of intake is constant across a meal. The rat does not gradually slow down; rather, it eats and then abruptly stops. This is illustrated by data from rats earning 45 mg chow pellets or 15-s sips of sucrose solution (Fig. 4) and by a study of the microstructure of drinking in freely feeding rats [20]. These
In the development and evolution of my understanding of feeding behavior, Gerry Smith was a teacher, a stringent critic, and a supporter, encouraging my wayward, out-ofthe-mainstream thinking. He was a model of programmatic research, pursuing the ingestant from tongue to pylorus, ever concerned with (of course) the associated mechanisms of satiety. He epitomized what a Good Scientist should be and was the model for many of us. He was—and is my friend. G.C.
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