John (Jack) D. Davis, Ph.D.
Remembering John (Jack) D. Davis and His Science
Jack Davis’s research program began in 1959 with a stinging criticism of Spence’s motivational theory of the effects of different reward magnitudes on behavior (Davis and Keehn,1959). What ignited Davis was Spence’s use of the word “vigor” in the statement about a reinforcement mechanism that has motivational properties “that vary with the magnitude or vigor with which it occurs.” Davis found Spence’s “vigor” ambiguous: “The vigor of a response might, for instance, refer to the magnitude or strength of the response—that is, the amount of effort that goes into a single occurrence of that response; it might refer to the rate at which that response occurs (when it does occur); or it might refer to the persistence of that response in competition with other responses. Therefore, “vigor” might refer to the intension, tempo, or preservation of a response, or to any combination of these and other responses”….
Then Davis turned to method: “despite Spence’s contention to the contrary (Spence, 1956, p.144) it is possible to measure consummatory behavior directly in a Skinner-box situation. This method,… employed by Stellar and Hill (1952) has been utilized by one of us to record the drinking behavior of white rats when presented with various concentrations of sucrose, saccharin and saline in distilled water solutions.”
“The results in all cases were clear-cut; the local rate of drinking an acceptable solution was constant for each animal. If an animal drank at all, it drank at a constant rate, regardless of its state of deprivation and the concentration of the solution under test….Variations of the total amount of intake were a function solely of the duration of the pauses and the lengths of the sustained drinking periods. That is, differences in quantities of liquid consumed per unit of time represent not as Spence (1956) appears to believe, differences in the tempo of the consummatory response but differences in the perseveration of that response.”
Davis concluded: “Clearly, the amount of a reward substance consumed per unit of time is too coarse a measure. It does not describe how the substance is consumed. It tells us nothing about the temporal distribution of pauses, about the sustained periods of drinking, or about the rate of drinking when it occurs.”
These sentences are an irrefutable argument for the necessity of measuring ingestive behavior when investigating the controls of ingestive behavior. These sentences also identified the questions that drove Davis’s research program for 60 years. From now on, Davis’s critical cry was “Total Intake is not behavior.”
Davis recorded the pattern of licking in many subsequent experiments because it was an unambiguous, behavioral measure of ingestion. Its methodological advantage was that it was an unconditioned, ingestive movement that could be recorded precisely and quantitatively. Its interpretive advantage was that the meaning of changes in the pattern of licking depended on the experimental context. By 2001, Davis interpreted the meaning of changes of lick patterns in 10 different ways (Smith, 2001).
It was commonly believed that the controls of ingestion were spatially organized: food stimuli in the mouth increased food intake, and postoral food and digestive stimuli acted in a negative-feedback manner to decrease food intake. Davis frequently used sham feeding to disconnect orosensory and postoral stimulation. His early sham feeding experiments used withdrawal of ingested liquid food to produce sham feeding; later experiments used the chronic gastric cannula technique.
Davis also increased the relevance of his test conditions by using food deprivations within the range of normal intermeal intervals and by investigating the size of meals constructed by a rat rather than intake per arbitrary times selected by the investigator.
The first report of an experiment under these conditions was published in 1973 (Davis and Campbell, 1973). There was evidence for 2 control signals: One apparently arose from tension receptors in the wall of the stomach that set an upper limit on meal size. The other signal was a conditioned orosensory inhibitory control of ingestion because repeated experience with sham feeding led to a progressive increase of intake. The results were clear, but the characterization of the gastric signal was speculative.
These initial results were quickly confirmed and extended (Davis, 1973; Booth and Davis, 1973; Campbell and Davis, 1974a,b). In 1977, the accumulated results stimulated a superb review of the controls of food intake (Davis and Levine, 1977) that began on a strong note: “Furthermore, the tremendous amount of attention which has been focused on the hypothalamic control of feeding has tended to direct attention away from the fact that the CNS is basically a processor of information it receives from the body. If we are ever going to understand how the CNS controls ingestion we are going to have to know what kind of information is being processed. That is, we are going to have to have peripheral theories of hunger as well as central theories.
“Few systematic attempts have been made to develop a peripheral theory of hunger….But the fact is that we do know a good deal about some of the peripheral signals which feed into the central nervous system feeding circuitry in a variety of animals. In view of this it would seem worthwhile to start with this information, build a simple model, see how far it can go in describing feeding behavior, and then add to it as more information becomes available. If the model does reasonably well as a first approximation, it could provide the foundation for the construction of a more complete model of feeding. This paper represents a start in this direction” (pp. 379-380).
The first part of the review was concerned with Sensory excitatory control, Gastrointestinal inhibition, and their interactions. The second part described the application of control theory to the controls of ingestion. The review closed with a word of caution: “The apparent initial success with a model such as ours can be seductive; there is a strong tendency to believe that the model really does represent reality…This attitude can make one blind to alternative, perhaps better, models. Its main contribution as we see it is that it organizes what appear to be some reasonable assumptions in such a way that specific quantitative predictions can be made. Confirmation of these predictions generates confidence in the model but by no means confirms it.”
Twenty years later, Davis reviewed the status of his model: “In summary it is clear that the model was, with a few exceptions, wrong in its specific predictions….This to me is not the least discouraging. We never expected the model to be correct in any really precise sense. It was designed to organize our thoughts about meal size and to generate predictions that could be tested in a quantifiably specific way. This has been done to some extent and the results of those tests have helped some of us pinpoint where our ideas and assumptions about the variables that control the intake of liquids by rats are wrong. The negative results have forced us to ask some questions that we might not have asked if the discrepancy between prediction and outcome were not so clearly apparent.
“The value of the model, as I see it, has been in the quantitative specificity of the predictions it made. Many were wrong, but discovering that has served the purpose of forcing revisions in the model….A major revision is the inclusion of conditioning.
“The revised model is an improvement over the original one, but like the original model, it only incorporates what Smith (1996) has called the direct controls of ingestion” (pp.168-170).
Despite the problems, Davis endorsed model building because “it provides a means by which quantitatively specific predictions about the control of meal size can be made and tested. By this process, and only by this process, can we learn where our knowledge about how the system operates is reasonably accurate and where the gaps in our knowledge are” (pp.128-129).
Davis retired from experimental research in 1999 and moved to Florida. He remained interested in his science. One of the lectures he listened to irritated him so much he wrote his last paper, The conditioned satiating effect of orosensory stimuli (Davis and Smith, 2009). “Ingesting a diet under real feeding conditions leads to the development of a classically conditioned form of satiation based on an association between gustatory stimulation and some consequence of gastrointestinal stimulation by the ingested food. This conditioned orosensory satiating effect extinguished when sham feeding occurs repeatedly without intervening real feeding tests. Thus, gustatory stimulation both stimulates and inhibits meal size….A change in meal size produced by some treatment should now include measurement of the potency of the conditioned orosensory satiating effect as well as the potencies of orosensory stimulation and postingestive negative feedback.”
This paper and the 1959 paper about Spence’s errors are bookends for his publications. It is interesting that both papers were initiated by exasperation with the scientific practice of others.
Davis and I collaborated for about 20 years. He was an ideal collaborator—tenacious, resourceful, critical, poised and funny. He had high standards that could be intimidating. His scientific goal was the mathematization of the peripheral controls of meal size. He thought that refinements of a model by iterative testing was the only way to produce scientific knowledge. Thus, he was a classical scientist, a member of an endangered species in our time.
Jim Gibbs was a good friend and close colleague of Jack for more than thirty years. At the Festschrift for Jack in May 1999, Jim raised the question of what accounted for Jack’s stream of scientific discoveries: “What is the art of finding the narrow path to discovery? It includes recognizing something that will sustain a lifetime of work, finding the right teachers, staying the course through difficulties, enjoying the talents and friendship of colleagues, acting on curiosity, trusting one’s judgment, focusing well, and digging deep” (Gibbs, 2001,p. 60). Jack walked that narrow path every day of his scientific life.
G.P. Smith, MD, New York Presbyterian Hospital