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Physiology& Behavior. Vol. 48, pp. 899-903. e Pergamon Press plc, 1990. Printed in the U.S.A.
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On the Waterfront: Predictive and Reactive Regulatory Descriptions of Thirst and Sodium Appetite I N E I L E. R O W L A N D 2
Department o f Psychology, University o f Florida, Gainesville, FL 32611-2065
ROWLAND, N. E. On the waterfront: Predictive and reactive regulatory descriptions of thirst and sodium appetite. PHYSIOL BEHAV 48(6) 899-903, 1990.--The concepts of homeostasis and regulation are discussed and examples are given in which current regulatory models of ingestive behavior inadequately predict or explain the observed phenomena. The implications of this for the choice of experimental paradigms, and the interpretation of neurobiological data obtained therein, are discussed. Paradigms that allow the expression of behavioral strategies and learned responses may be biologically more relevant than the more popular but highly constrained 'physiologic' paradigms. Homeostasis
Regulation
Strategy
Thirst
Sodium appetite
THE explosive growth in the number and relative ease of performing various types of molecular analyses of biological tissues has progressively infiltrated studies of mechanism in ingestive behavior, as seen, for example, in the number and diversity of papers at this Congress. For the benefit of new colleagues whose primary expertise is in these molecular fields, but also as a reminder to some of us who once knew better, it is evident that there is not a corresponding abundance of ideas or concepts of ways in which functions devolve from these components, or how these functions are integrated together to produce behavior. This type of discrepancy is by no means unique to biobehavioral sciences, but presents challenges to develop new integrative concepts and constructs. It is necessary fast to appreciate that behavior, or what might constitute an explanation of behavior, can be approached at several different levels (Table 1). Most of the research presented at this Congress falls into the category of 'the way it works.' However, this should not overshadow but rather should complement the other levels at which we seek to explain ingestive behavior. A similar point has been made by Bunge (1) insofar as animals, and human beings in particular, span levels from global societies down to subatomic particles. Each of a variety of intermediate and hierarchical levels (e.g., cells, organs, 'supersystems' such as CNS) need to interface with each other in order for science to present an adequate explanation of a phenomenon such as ingestive behavior. While the analytical or ' t o p down' ap-
Nycthemeral rhythm
proach to a problem is fruitful insofar as it is relatively easy to generate and test hypotheses, the synthetic or 'bottom u p ' approach is also necessary. Bunge thus advocates a multilevel approach in which 'every system should be studied at its own level as well as a component of a supersystem and as composed of lower level things.' He also notes that 'physiological psychology contributes powerfully to the synthesis . . . . ' a viewpoint with which I concur. HOMEOSTASIS For over 50 years, the principal theoretical paradigm of our area has been homeostasis, the active regulation of certain variable(s) within limits conducive to optimal functioning. Davis (4) made a most important distinction between, on the one hand, the general use of the term homeostasis to explain motivated behavior and, on the other hand, using control systems theory and its associated regulatory mechanistic view to model motivated behavior. To some extent, this distinction is isomorphic with that of homeostasis as a description either of a behavioral state of affairs or as an internal constancy. The former exercise is uncontroversial, if we understand that homeostasis is a description rather than an explanation. The latter aspect is only one way in which internal homeostasis might be achieved. Hogan [(8), p. 19], discussing these same issues, has gone so far as to suggest that 'it seems inappropriate to apply the concept of homeostasis to the analysis of motivational processes.'
~This manuscript develops one of the themes from an address 'Future studies of ingestive behavior: animal models, conceptual questions, and therapeutic applications' given at the Xth International Congress on the Physiology of Food and Fluid Intake, Pads, July 1989. This work was funded in part by the National Science Foundation (BNS 8909439). 2Send correspondance to this address, or by electronic mail to: rowland @ webb.psych.ufl.eda.
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TABLE 1 TYPES OF EXPLANATIONOF BEHAVIOR The animal behaves the way it does because . . . 1. of the way its ancestors evolved 2. of the way it developed 3a. of the way it responds to situation 3b. of the way it works 4. that behavior promotes survival
Some of these difficult problems in the analysis of feeding are considered by Collier and Johnson (3).
Adrenalectomy and Salt Appetite Evolutionary history Developmental history Motivation (causation) Physiology (causation) Function
From Sibly (25). In common with the concerns of Davis and Hogan, Weingarten (29) has considered three types of regulatory mechanism: negative feedback, anticipation/feedforward, and ' adaptive control,' all of which contribute to homeostasis (his examples are in relation to body energy and feeding). The third of these, adaptive control, may act at any or all of the levels of comparator (i.e., altering an effective set point), gain in the feedback loop, or output control mechanism of a simple negative feedback regulatory system. Weingarten also suggests that alimentary learning is manifest through changes in adaptive control. This concept is in some respects similar to Collier's (2) 'house economist' whose function is to interface the needs of a 'resident physiologist' with the outside world. Collier and Johnson (3) further address these issues in this volume. One key feature of any regulatory system is that in order to generate output (behavior) a deficit needs to be detected relative to a reference or normal value [see Davis (4) on the use, or misuse, of the term set point]. Critics of this type of model have noted instances in which ingestion occurs without any identifiable deficit, and some authors have used the term 'nonhomeostatic' to describe such intake. As discussed by Davis (4), Hogan (8) and myself (15,16), this is not a particularly useful term because any and all ingestive behavior that promotes survival also subserves homeostasis. Fitzsimons (7) made a careful distinction between primary drinking, precipitated by identifiable physiologic deficits, and secondary drinking that occurs in the absence of such deficits but nonetheless may subserve longer term homeostatic function. The terms regulatory and nonregulatory drinking appear to be identical to primary and secondary, respectively, and refer to a process rather than a state. One way of articulating these distinctions was used in another context by Moore-Erie (10) and can be extrapolated to ingestive behavior (17). He distinguished between reactive homeostasis, which refers to restoring a system after it has become imbalanced, and predictive homeostasis, which may anticipate a recurrent imbalance and so prevent it from occurring. From the foregoing, I am no longer [cf. (17)] sure that homeostasis is the right term to use in this behavioral extrapolation; I will instead use the terms predictive and reactive regulation. Examples of predictive regulation include nycthemeral or seasonal changes in feeding and body weight, and many of the conditioned aspects that pervade the normal ingestion. The following four examples illustrate cases in which ingestive behavior does not conform to a simple feedback or 'reactive regulatory' model. These examples, from my own work, use the simple systems of water and salt balance. Hydromineral systems are likely more amenable to homeostatic analysis because, from a physiologic standpoint they may be more tightly regulated than energy balance, and from a psychological perspective there are only a few commodities to consider compared with the cornucopia faced in analysis of feeding behavior.
Richter first described the salt appetite of adrenalectomized rats and explained this in terms of a regulatory behavioral process. In studying such animals, we noted that their ad lib intake of NaC1 solution was at least 80% nocturnal, despite the fact that daytime excretion of Na + was much higher than in adrenally intact controls (18). Thus, relative to these controls, adrenalectomized rats showed a greater negative Na +

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