ILAR Journal Online, Volume 34(3) 1992: ILAR's Fortieth Anniversary

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ILAR Journal V34(3) 1992 [FORMERLY ILAR NEWS]
ILAR's Fortieth Anniversary

Letters

The Controlled Water Access Paradigm
Robert Desimone, Carl Olson, and Roger Erickson

Robert Desimone, Ph.D. is chief of the Section on Behavioral Neurophysiology, Laboratory of Neuropsychology, National Institute of Mental Health; Carl Olson, Ph.D. is a visiting professor in the Laboratory of Sensorimotor Research. National Eye Institute. Roger Erickson, Ph.D. is a senior staff fellow with the Laboratory of Neurophysiology, National Institute of Mental Health.

A Note To Our Readers:

The following contribution, The Controlled Water Access Paradigm, was submitted in response to Prolonged Water Deprivation: A Case Study (ILAR News 33[3]:48-52, 1991), by F. Barbara Orlans. It is followed by a rejoinder from Dr. Orlans.

In considering Prolonged Water Deprivation: A Case Study for publication, the ILAR News Editorial Panel understood the term "case study" used by Dr. Orlans to mean an account of a single institutional animal care and use committee's (IACUC's) deliberations concerning a single protocol. However, as Dr. Orlans acknowledges in her rejoinder, "certain additions were made (thus making it a 'composite')''. It is ILAR's editorial policy to use the term "case study" only when referring to a true record of circumstances surrounding a single event.

ILAR News strives to stimulate discussion within IACUCs by providing material from a variety of sources. Contributions such as these are not intended to be used as policy or precedent. The opinions expressed in author-attributed articles in ILAR News do not necessarily reflect those of ILAR or the National Research Council, National Academy of Sciences.

--The ILAR News Editorial Panel

Introduction

In many studies of perception, memory, and other higher functions, monkeys are trained to perform challenging tasks for reward. A standard procedure for producing motivation in these tasks has been to limit access to water before each training session and then to deliver water or fruit juice as a reward. Studies utilizing this technique have shed significant light on the workings of the central nervous system. It has recently been suggested by Dr. Barbara Orlans (1991) that institutional animal care and use committees (IACUCs) should reject protocols involving this procedure. We here critically examine the arguments leading to that position and conclude that the controlled water access paradigm, as now widely used in behavioral and neuroscience laboratories, is humane and scientifically justifiable.

The arguments marshalled by Dr. Orlans arose from an analysis of what was presented as a case study. A case study should describe a single series of events that actually occurred. When we contacted Dr. Orlans to verify that the article was indeed based on a real case, she stated that the article described a "composite" of cases. A composite description, in which events can be freely selected and blended, is not a case study. The article is, in fact, an opinion piece, and Dr. Orlans should have labeled it as such.

Despite the mislabeling of the article as a case study, it is important to examine the reasoning by which the composite IACUC decided to reject the paradigm. In the following comments, we focus on the three major claims presented in the article, namely, that the paradigm is (1) officially discouraged, (2) unnecessary, and (3) inhumane. We shall show that none of these claims is correct.

Official Policies

Dr. Orlans states that the committee, in searching for policies that might provide guidance, found that some discouraged and others prohibited the restriction of water intake outside training sessions. This claim is misleading for two reasons.

First, it does not reflect guidelines that actually govern animal research in the United States. The Animal Welfare regulations of the U.S. Department of Agriculture, and the Public Health Service Policy on the Humane Care and Use of Laboratory Animals, which do govern research in this country, do not prohibit the paradigm. On the contrary, it is accepted as a standard technique in guidelines promulgated by an NIH-sponsored workshop of nationally recognized veterinarians and scientists concerned with animal welfare issues in the neurosciences. These guidelines state: "when a liquid is used as a reward, the behavioral task is often the only time the animal is allowed access to liquids" (Van Sluyters and Oberdorfer, 1991, p. 39).

Second, in citing foreign policies that purportedly prohibit the technique, Dr. Orlans has taken statements out of context. She states that "perhaps the most uncompromising policy of all those encountered is that of the Biological Council (1987) in the United Kingdom" and goes on to quote a passage stating that "water should always be available to all animals." She concludes: "under these guidelines, the protocol could not be approved." However, the passage quoted is located in a section of the guidelines concerned with animal husbandry issues and is not from the section on research protocols. In fact, water restriction as a motivational procedure is not mentioned in the guidelines. Moreover, we have confirmed by contacting colleagues in England that Home Office approval has been granted to procedures involving the controlled water access paradigm.

In citing another supposed example of a policy that would prohibit water restriction, Dr. Orlans states: "the national standards of Canada allow no waivers. The Guide to the Care and Use of Experimental Animals of the Canadian Council on Animal Care unreservedly states, 'Water deprivation should be used only when thirst is the specific subject of the study'. However, this statement is not the whole story. The Canadian Guide addresses the issue of thirst as a motivator in a later section not mentioned by Dr. Orlans. This section, developed in consultation with the Canadian Psychological Association, is worth quoting despite its length because of its clear exposition of the reasoning underlying water restriction procedures (CCAC, 1980, p. 114):

Psychologists incorporate and manipulate motivational variables in their research for three somewhat dissimilar reasons. The first is when the subject of study is the motivational system in question, e.g., the control of feeding or drinking behavior. In such a context, it is obvious to all why an animal might be on a water or food restricted regimen. The second is when the motivational system in question is being used as a model for other appetitive or aversive motivational systems, as discussed [in an earlier section]. The third reason, and one that is often not well appreciated by those outside the discipline, is that such manipulation represents an effective means of facilitating the controlled study of phenomena only indirectly related to the motivational manipulation. Behavior that is oriented towards obtaining access to food and water, or escaping or avoiding an aversive event, can form the basis of sound inferences about nonmotivational processes associated with, for example, learning, memory or perception.

It is clear from this passage that the Canadian Guide recognizes water restriction as an acceptable procedure for producing motivation even in experiments where thirst is not the specific subject under study. Dr. Harry Rowsell, former executive director of the Canadian Council on Animal Care, in Ottawa, Ontario, has confirmed to us that the sentence quoted by Dr. Orlans is inconsistent with the other policies of the Canadian Council on Animal Care and that IACUCs in Canada do permit water restriction as a motivational technique.

Finally, as a further precedent for rejecting the protocol, Dr. Orlans cites a study (Dresser, 1989) in which IACUCs, presented with a hypothetical proposal involving water restriction, raised questions about it. But this proposal involved procedures markedly different from those employed in the standard form of the paradigm. The monkeys were to be restrained in chairs continuously for up to 8 weeks, subjected to intermittent blood sampling, and given access to fluid for only 30 minutes per day (not as a motivational procedure but in order to produce arousal), in a study that had not undergone scientific review. It is clear that the committee members' responses to this hypothetical protocol should not be interpreted as a general rejection of controlled water access.

Necessity of Controlled Access

A second critical claim presented by Dr. Orlans is that restriction of neither food nor water is necessary for motivating monkeys to perform tasks. She states that the committee, through consulting unidentified experts, "learned that given free access to water and food, animals will work well for rewards of high preference food or drinks that are not part of their normal laboratory fare." This statement requires major qualification. In our experience, the willingness of monkeys to perform a task for a high preference food or drink depends on both the animal and the task. Some monkeys, without prior restriction of intake, will perform an easy task for extra treats such as raisins or a highly preferred juice; however, even when given a preferred food or juice, most monkeys will perform a challenging task only when working for some portion of their daily food or fluid requirement. Without knowing the details of the behavioral task, the requirements of the research, the number of daily behavioral trials required for adequate statistical analysis, and the behavioral results from using different types of fluids, it is impossible to evaluate whether restriction is necessary. In the case described by Dr. Orlans, the investigator asserted that adequate data collection in the context of his behavioral paradigm required controlled access, and no evidence to the contrary is described.

Animal Welfare

The third critical claim presented by Dr. Orlans is that the controlled water access paradigm causes suffering. In considering this issue, one should note at the outset that monkeys are not deprived of their daily fluid requirements. Rather, in the standard form of this procedure, animals are trained to meet their full daily fluid needs during the testing session, which typically lasts 2-8 hours. Food and treats such as raisins, peanuts, and "monkey chewles" are also typically offered during the session. Monkeys normally work until satiated but those that fail to earn the necessary quantity of fluid are given a supplement at the end of the session. In many protocols, the animals are given periodic "vacations", in which they have free access to water and/or supplemental fruit with high water content. An essential part of this procedure is careful daily monitoring of the animal's health by the investigator, veterinarians, and animal care staff.

Dr. Orlans cites unnamed primatologists as informing the committee that procedures such as these would cause distress to monkeys. To check the validity of this claim, we contacted two primatologists who have studied primate behavior in the wild (Dr. Stuart Altmann, University of Chicago, Department of Ecology and Evolution; and Dr. Donald Lindburg, Center for Reproduction of Endangered Species, Zoological Society of San Diego). According to both of them, access to water once a day is not uncommon for wild monkeys, particularly during dry seasons; thus, the paradigm is not outside the range of natural conditions. Dr. Stuart Altmann, who has observed the drinking patterns of baboons (Altmann and Altmann, 1970), states: "at Amboseli, baboons occasionally go an entire day without water, when the nature of their day range precludes drinking." Based on his observations, Altmann believes that experienced monkeys adapt to restricted periods of water availability, and thus tolerate periods without water much better than would naive animals suddenly deprived of water. He speculates that "experienced baboons 'tank up', just as experienced human hikers do before a long trek without water in an arid area." Dr. Donald Lindburg, who has studied the drinking patterns of rhesus monkeys (Lindburg, 1977), states: "as conditions began to dry out and daily temperatures to rise, the troops would travel distances of 1-2 miles on a daily basis to visit a water source" and expresses the opinion that "a laboratory macaque living indoors at moderate air temperature could do quite well on access to water once or twice daily." These comments are supported by additional published observations. According to Hall (1965), patas monkeys inhabit areas of West Africa that are completely devoid of water during the dry season. On infrequent visits to water holes, individual animals have 10-30 seconds' access to water under the watchful eye of an adult male on the lookout for predators. He concludes that "wild groups are habituated to a low level of water intake." Dr. Orlans reports that giving fluids drop by drop may be stressful to the animal, but this also has parallels in the wild. In the Kuiseb Canyon of South West Africa, for example, baboons dig holes down to the water table, slowly sucking up the water that seeps into the hole (Hamilton, et al., 1976).

The notion that animals in laboratories should be shielded from all of the stresses, strains, and challenges faced by animals in the wild may be well intentioned; however, it is misguided. The NIH intramural IACUC guidelines for water restriction acknowledge that engaging monkeys in complex behavioral tasks for fluid rewards may actually improve their psychological well being. In addition to the challenge of the task itself, the change of environment and the daily social interaction with familiar human caretakers are themselves enriching. Furthermore, as described above, it is far from unnatural for monkeys in the wild to forage, solve problems, travel long distances, avoid predators, and otherwise labor for their food and water.

Conclusion

The three critical arguments that Dr. Orlans presents against controlled water access are based on erroneous claims. Contrary to the arguments presented by Dr. Orlans, this approach is permitted by the regulations that govern animal research, is necessary in many cases, and is humane. It has been in wide use, with institutional approval and in accord with regulations of the United States, Canada, and Great Britain, for over 20 years and is a continuing source of major advances in the understanding of behavior and the brain. IACUCs considering protocols that incorporate controlled water access should not reject them out of hand, but should consider them on their individual merits. Scientifically worthy and humanely designed protocols involving controlled access to fluids can and should be approved.

Acknowledgments

We are indebted to Drs. Stuart Altmann, Donald Lindburg, and Harry Rowsell for valuable discussions and for permission to cite unpublished data and opinions.

References

Altmann, S. and J. Altmann. 1970. Baboon Ecology: African Field Research. Chicago: University of Chicago Press.

Biological Council, The. 1987. Guidelines on the Use of Living Animals in Scientific Investigations. London: The Biological Council.

CCAC (Canadian Council on Animal Care). 1980. Guide to the Care and Use of Experimental Animals. Volume 1. Ottawa, Ontario: Canadian Council on Animal Care. (Available from: CCAC, 1105-151 Slater Street, Ottawa, Ontario KIP 5H3, Canada.)

Dresser, R. 1989. Developing standards in animal research review. Am. J. Vet. Med. Assoc. 194(9):1184-1191.

Hall, K. R.L. 1965. Behaviour and ecology of the wild Paras monkey, Erythrocebus patas, in Uganda. J. Zool. 148:15-87.

Hamilton, W. J., R. E. Buskirk, and W. H. Buskirk. 1976. Defense of space and resources by chacma (Papio Ursinus) baboon troops in an African desert and swamp. Ecology 57:1264-1272.

Lindburg, D.G. 1977. Feeding behaviour and diet of rhesus monkeys (Macaca mulatta) in a siwalik forest in north India. Pp. 223-249 in Primate Ecology: Studies of Feeding and Ranging Behaviour in Lemur, Monkeys, and Apes, T. H. Clutton-Brock, ed. New York: Academic Press.

Orlans, B. 1991. Prolonged water deprivation: A case study in decision making by an IACUC. ILAR News, 33(3):48-52.

Van Sluyters, R. C., and M. D. Oberdorfer, eds. 1991. Preparation and Maintenance of Higher Mammals During Neuroscience Experiments: Report of a National Institutes of Health Workshop. U.S. Department of Health and Human Services Public Health Service, National Institutes of Health (NIH publication 91-3207).