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Similarly, enrichment could potentially reduce between-individual and between-laboratory variability by removing the range of variation introduced by abnormal physiology, thereby enhancing experimental reliability and replicability Figure 1. Therefore, far from introducing another source of variability into experiments, enrichment could instead 1 help address the potential effects of abnormal behavior on experimental outcomes, 2 reduce variability, and 3 improve validity.
Hypothetical data set illustrating the general hypothesis of this article. Note that none of the animals show any abnormal behavior. The gray box denotes the range of physiological variation that can be considered normal, and should be the target range for a valid study. Only a few individuals are within the normal range, hence, any experiment performed with this population will have poor validity. The increase in physiological variation induced by captivity will decrease the reliability of any experiment affected by the physiological measure, and will increase the number of individuals needed to achieve sufficient statistical power.
Abnormal behavior therefore serves as a marker of abnormal physiology. Abnormal behavior is not a necessary component of the argument that enriched animals may be more physiologically normal i. Rather than a general review of enrichment and its effects on experimental outcomes or individual variability, a specific corner of this broader issue is explored in the ensuing discussion. This article focuses on abnormal repetitive behavior ARB 1 , which because of its close connection to brain function, provides a specific example where these hypotheses may in fact bear weight; where a complete testable argument can be formulated; where potential effects on experimental outcomes can be predicted; and where areas for further study are clear.
For a broader review of the potential effects of enrichment on experimental outcomes, the reader is directed to other articles in this issue of ILAR Journal e. ARBs are defined as behaviors that are inappropriate, repetitive and unvarying in either goal or motor pattern Garner ; Turner These categories are aptly illustrated by common ARBs seen in mice. Unlike a stereotypy, each episode of plucking behavior is flexible and goal directed Sarna et al. Prevalences of the behaviors described above can be extremely frequent under standard housing conditions.
Barbering is less ubiquitous across mouse strains. For a detailed, recent review and to understand the relationship of ARB to experimental outcomes, the reader is referred to Garner The control of behavior by the brain is divided between two systems.
The first system selects and sequences individual responses on the basis of external e. This goal selection system influences behavior by priming and editing the selections made by the response selection system.
For example, when playing poker, I might bet very differently on the same hand depending on what other players have bet, on whether I am planning to bluff, and on what I know about the other players. The goal selection system is required to make these kinds of decisions, while the response selection system is responsible for initiating the actual movements involved in playing the game.
The goal selection system is involved in suppressing such automatic movements in particular circumstances e. The brain is an expensive organ to maintain, and it is designed with very little redundancy. As a result, every area of the brain performs a different job, and if a particular area is damaged i. The response selection system described above is distributed across a series of brain areas called the basal ganglia motor system.
As an example, when a patient is asked the name of his or her father, the patient might respond correctly, but then when asked to name other members of the family, might continue to respond with the father's name. In contrast, the goal selection system is distributed across the prefrontal corticostriatal loop, a series of brain areas.
In this instance, when a patient is asked to name the suit of each card turned face up from a deck of playing cards the patient responds correctly as each card is turned over whereas with recurrent perseveration, the patient would have incorrectly repeated the suit named on previous cards. However, when the patient is then asked to stop naming the suit and to state the value of the card e.
Several authors have argued that ARB in human patients is intimately related to perseveration, whereby ARB is the day-to-day expression of a deficit in behavioral control, and perseveration is the quantified experimental measure of the same deficit e. These predictions have been met in autism by correlating the severity of a patient's ARB with his or her performance on neuropsychological tasks that measure perseveration Turner Thus, ARB does indeed appear to be related to perseveration in humans, thereby raising the possibility that the same mechanisms underlie animal ARB.
The involvement of executive i. Furthermore, the hypothesis is directly testable by extrapolation from human studies. To test the hypothesis described above, colleagues and I have assessed the correlation of stereotypy with recurrent perseveration. In earlier experiments, we used extinction learning as a measure of recurrent perseveration. We taught animals a simple spatial discrimination in a two choice maze, or in a touch-screen operant; and when this simple task was learned, we ceased to reward the correct response.
Extinction learning is complete when the animal ceases responding to the previously rewarded side of the maze or computer screen and returns to choosing both options at random. Recurrent perseveration is apparent when the animal inappropriately persists in choosing the option that was previously rewarded.
Using this simple paradigm, we demonstrated that stereotypies are indeed correlated with recurrent perseveration and hence basal ganglia motor system function in bank voles Garner and Mason , blue tits, and marsh tits Garner et al.
This result has been replicated by other researchers with the same paradigm in Asiatic black bears and Malayan sun bears Vickery and Mason , Extinction learning, however, is affected by processes other than extinction. Although we addressed these issues using internal controls in our earlier experiments, in an effort to improve the replication of the human data, we proceeded in later experiments to modify the two choice gambling task for use with animals.
The sequence of choices made by the subject is recorded and quantified for repetitiveness using information theory or Markov chain analysis for introductions to these methods, see Attneave ; Martin and Bateson Using this paradigm, we again confirmed the correlation of stereotypy and recurrent perseveration in blue tits Garner et al. We further modified this task to avoid superstitious conditioning and developing side bias, so that the probability of being rewarded on each side of the maze or computer screen decreases the more that side is chosen.
Using this bias-corrected gambling task, we have confirmed the correlation of recurrent perseveration and stereotypy in parrots Garner et al. Consistent with these findings, evidence is growing that a range of neurophysiological changes in the basal ganglia motor system may be involved in stereotypy e. We have begun working on the neuropsychological basis of barbering in mice. This task has been adapted successfully for use in primates Dias et al.
The task and its use in animals are discussed in detail elsewhere Garner Colleagues and I have found that barbers i. In addition, we found that stereotypy and barbering, stereotypy and stuck-in-set perseveration, and barbering and recurrent perseveration were all uncorrelated, confirming the specificity of the association of particular forms of perseveration with particular forms of ARB. The question then arises regarding how this association between ARB and perseveration might affect experimental outcomes.
In the foregoing text, perseveration is emphasized because it is an unequivocal indicator of the function of the systems controlling the selection and sequencing of behavior. However, disruption to these systems also affects many other aspects of behavior. Manipulations such as isolation rearing Jones et al. To confirm that the correlation of recurrent perseveration and stereotypy that we have observed does indeed reflect the function of the response selection system, we have also looked for the presence of these secondary indicators.
Animals treated with amphetamine show a rapid increase in the rate they switch between behaviors, which precedes the performance of amphetamine-induced stereotypy Lyon and Robbins Initially, it might seem paradoxical that rapid switching between behaviors should be associated with stereotypy; however, this phenomenon parallels the distracted switching between goals that is associated with stuck-in-set perseveration Norman and Shallice In both cases, perseveration and switching are consequences of a failure to inhibit behavior.
Thus, recurrent perseveration and stereotypy can be seen as the failure to inhibit a response once it is completed, and switching inappropriately between behaviors can be seen as a failure to inhibit a new behavior before the current response is completed. Accordingly, recurrent perseveration and stereotypy should be correlated with the spontaneous rate at which animals switch between all behaviors in the home cage.
We have confirmed this prediction in bank voles Garner and Mason In blue tits, marsh tits Garner et al. Similarly, in schizophrenia, some authors e. Thus, the commonality of this result is currently unclear. The disinhibition of behavior that leads to high rates of behavioral switching in amphetamine-treated animals also induces hyperactivity Lyon and Robbins Similarly, animals reared in isolation have been observed to be hyperactive Einon and Morgan Accordingly, we found correlations between activity, behavioral switching, stereotypy, and perseveration in bank voles Garner and Mason Other authors e.
Amphetamine-treated animals not only make perseverative choices but also fail to suppress rapid responding to stimuli when it becomes inappropriate Robbins When we examined the latency to respond to the two choices presented in an extinction task in bank voles, we found that stereotypy was correlated with persistent rapid responding Garner and Mason We found stereotypy in parrots similarly correlated with perseveration and inappropriate rapid responding Garner et al.
Perseveration involves a failure of behavioral control, not of cognition, will, or knowledge. Thus, perseverative human patients often report that they select incorrect perseverative responses despite knowing what the correct response should be and trying to make it e. Voles generally showed extinction of choices before they showed extinction of rapid responding, so we examined the degree to which each vole persisted in rapid responding at the point where it was choosing both sides of the maze equally.
Accordingly, we found that stereotypy was correlated with a greater persistence of rapid responding at the point where choices indicated acquisition of the extinction task, which in turn indicated a greater knowledge-action dissociation. All of the data from bank voles were collected on the same individuals, therefore we were able to intercorrelate each of the measures discussed above.
If stereotypy is truly a product of a disinhibition of behavioral control, then each and every one of the measures described above should correlate with each and every other measure, as indeed we found Garner and Mason Table 1. In other experiments, however, these relationships have been less consistent than the relationship between stereotypy and perseveration e.
Nevertheless, the general disinhibition of behavior that underlies stereotypy has the potential to affect a wide range of behavioral measures. Indeed, almost every widely used high-throughput behavioral task is potentially affected by one of the correlates of stereotypy, as detailed in Table 2.
Intercorrelation of stereotypy and measures indicative of disinhibition of response selection in bank voles a b. Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents. Behav Brain Res — Partial correlation coefficients were controlled for the various internal controls in each measure. The p value of each is also given.
This pattern of data indicates a single underlying causal factor consistent with disinhibition of response selection. Potential impact of demonstrated correlates of stereotypy on commonly used behavioral measures in ethology, experimental psychology, and high-throughput phenotyping. The species in which the correlate has been demonstrated are indicated. See text for details. Thus, whether or not stereotypy is related to physiological differences e. For example, in the food storing literature, a common paradigm is to pilfer the animal's food stores, and to examine its behavioral response.
The goal is to learn whether it gives up food storing i. The chosen strategy, in theory, provides a great deal of information about the design and function of food storing behavior Lucas and Zielinski ; Lucas et al. Unfortunately, however, when we examined the response of food storing marsh tits to pilfering, we found that the responses depended on their stereotypy level.
Birds with high levels of stereotypy persisted with food storing, and birds with low levels of stereotypy gave up food storing Garner et al. The disinhibition of response selection that appears to underlie stereotypy can and does affect experimental outcomes such as extinction learning, home cage activity, response latencies, and behavioral switching. Whether this phenomenon has a major impact on many of the other commonly used measures listed in Table 2 remains to be tested and is a subject of our ongoing research.
Even if and when all of the effects hypothesized in Table 2 are observed, their meaning for scientific validity actually depends on a second issue—whether the level of brain function correlated with stereotypy is abnormal or simply a natural extreme that is expressed as an abnormal behavior in captivity. In other words, the question is whether stereotypy and barbering are malfunctional or maladaptive behaviors.
In the case of stereotypies induced by isolation rearing or amphetamine-induced stereotypies, we presume that the observed range of brain function is abnormal and that stereotypy is a malfunctional behavior. However, this presumption does not mean that all stereotypies, for example, indicate abnormal brain function.
For example, obsessive and compulsive symptoms in obsessive compulsive disorder are correlated with abnormal brain metabolism Baxter et al. Yet compulsive behavior cannot be taken blindly as an indicator of brain dysfunction because, as another example, subclinical levels of compulsive behavior remain correlated to neuropsychological measures of stuck-in-set-perseveration in healthy individuals within the normal range of brain function Zohar et al.
It is critically important to disentangle this issue of ARB in laboratory animals for the following reasons: If stereotypies and barbering are maladaptive behaviors, then 1 animals showing ARB simply express a normal extreme of brain function strangely in captivity; 2 the range of variation seen in our behavioral tests can be considered normal, and we do not need to worry about the scientific consequences of ARB.
If, however, ARBs are malfunctional, then 1 ARB is the product of abnormal extremes of brain function; 2 this abnormal brain function is a major source of excessive and uncontrolled variation, and we really do need to worry about scientific consequences. These possibilities are illustrated in Figure 2. Two different explanations for the relationship between recurrent perseveration and stereotypy.
No stereotypy is observed. In this case, stereotypy would be an example of a maladaptive behavior. In this case, stereotypy is a malfunctional behavior that indicates abnormal brain function. Nonstereotypic individuals should show levels of perseveration within the normal range, whereas stereotypic individuals would show a completely different range of perseveration, separated from the normal range.
To date there is little direct evidence related to the distinction described above, but a very tentative picture does appear to be emerging in which many, if not most, examples of ARB appear to be malfunctional behaviors indicative of abnormal levels of perseveration. The following lines of circumstantial evidence together argue that most stereotypies probably involve abnormal brain function Garner and Mason :. Stereotypies often lead to self-injury e.
Stereotypies appear not to develop in wild-caught adults, requiring instead an early critical period in captivity Callard et al. Stereotypies are thought to become increasingly resistant to enrichment as the animal ages, although only a few demonstrated examples have been reported e. The only direct experimental evidence as to whether stereotypies are malfunctional or maladaptive comes from our work in songbirds. Midway through these experiments, we moved the birds to outside aviaries as part of routine husbandry for their yearly molt.
When we returned them to their standard cages, we observed a reduction in stereotypy. Thus, this period of aviary housing served as a period of enrichment. For each bird, we maintained a stereotypy and a perseveration score from before and after the period of aviary housing. We then performed a meta-analysis wherein we normalized i. The change in recurrent perseveration during aviary housing correlated with the change in stereotypy Garner et al.
This result is consistent with the level of perseveration seen before aviary housing i. However, these data should be interpreted cautiously because the experiment was essentially unintentional. Although the case can be made that the level of perseveration associated with stereotypy may be abnormal, this conclusion is extremely preliminary. Different answers to this central question almost certainly depend on the species, time in captivity, severity and type of stressor to which the animal is exposed, and type of stereotypy.
The ultimate determination will be made in future work, but it is an empirical issue that can be assessed readily. We also are addressing this central question alongside current work of investigating the relationships between ARB, perseveration, and commonly used behavioral tests. To that end, we are investigating the effects of enrichment on stereotypy, perseveration, and experimental outcomes. If the level of perseveration observed in stereotypic animals is in fact normal, then enrichments that reduce stereotypy should not affect perseveration and should not reduce variability in experimental outcomes.
Alternatively, if the level of perseveration seen in stereotypic animals is abnormal, then enrichment should reduce perseveration and reduce variability in experimental outcomes. Most importantly, the level of perseveration seen in nonstereotypic individuals should be the same in both enriched and unenriched animals.
In this article, a discussion of the mouse enrichment literature has been avoided for three reasons: 1 Other articles in this ILAR Journal issue address rodent enrichment directly e. For instance, although toys and abstract stimulation may be biologically relevant for primates, the same stimulation is not necessarily appropriate for mice Olsson and Dahlborn To date, the only device that does appear to be ubiquitously enriching to mice of different sexes, group sizes, and strains is nesting material Olsson and Dahlborn Although shelters and complex cages may benefit some mice, these items may induce territoriality and hence become deleterious to others especially group-housed males Olsson and Dahlborn The following key conclusions are based on the information reviewed and discussed above:.
Clear evidence exists that the brain mechanisms that produce ARBs also affect measures in behavioral experiments. Enrichment might improve the validity, reliability, and replicability of behavioral experiment. Conclusive empirical work has yet to be completed. In other words, in the particular example of the effects of ARB and enrichment on behavioral experiments, good welfare probably is good science; however, a good welfare scientist would wait for more data before arguing conclusively for the scientific benefits of enrichment.
Conclusion 3 can be further divided into three key unresolved issues: a whether or not the differences in brain function seen in animals performing ARB are abnormal; b which common behavioral paradigms are affected by ARB; and c whether or not enrichment does improve the quality of behavioral data. Despite the wide literature on the effects of enrichment on the mean outcome of various measures, few studies have tested specifically for effects on the variability of these measures though see, e.
In addition, few have tested for relationships between ARB and behavioral experimental outcomes. Finally, the effects of enrichment on between-laboratory variability or for that matter the relative importance of within- and between-laboratory effects on variability are unclear—although recent work is beginning to explore this issue Wolfer et al. Nevertheless, each of these issues can be answered empirically, and given the relationship of ARB to behavioral mechanisms discussed in detail above, its effects on other behavioral measures can be predicted directly.
Thus, the interrelationships between ARB, brain function, enrichment, and potentially other behavioral measures provide a powerful system for exploring the argument that good welfare is good science. Conclusion 3 is probably frustrating to many readers who are looking for scientific reasons that support or refute the enrichment of laboratory animals. In the meantime, as we await the results of additional studies, considering the following pragmatic questions may perhaps provide some perspective on the enrichment debate.
Objecting to enrichment because of its possible negative effects on scientific outcomes involves an implicit assumption—that enrichment has a greater potential negative effect on experimental outcomes than other sources of variability in the housing of laboratory animals. Therefore, 2 Is it reasonable to argue that providing a mouse with nesting material will perturb its physiology more than many other common laboratory provisions and decisions e.
Many of the ideas in this article grew from conversations with Drs. The article also benefited from the comments of three anonymous referees. Work on this manuscript was supported by Purdue Agricultural Experiment Station grant — Attneave F.
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Barbering fur and whisker trimming by laboratory mice as a model of human trichotillomania and obsessive-compulsive spectrum disorders. Comp Med 54 : — Behavioral rigidity and rule-learning deficits following isolation-rearing in the rat—Neurochemical correlates. Behav Brain Res 43 : 35 — Latham N Mason G.
From house mouse to mouse house: The behavioural biology of free-living Mus musculus and its implications for laboratory housing. Appl Anim Behav Sci 86 : — Long-term effects of early social isolation in Macaca mulatta: Changes in dopamine receptor function following apomorphine challenge. For a historic account of significance testing, see Huberty A frequentist subscribes to the long run relative frequency interpretation of probability.
This is defined as the limiting frequency with which that outcome appears in a long series of similar events. Dice, coins and shuffled playing cards can be used to generate random variables; therefore, they have a frequency distribution, and thus the frequency definition of probability theory can be used. Unfortunately, the frequency interpretation can only be used in cases such as these. The Bayesian interpretation of probability can be used in any situation. Why should we choose between just two hypotheses, and why can't we put a probability on a hypothesis?
A typical null hypothesis, that two populations means are equal, is daft: they will almost never be exactly equal. What does it mean to accept and reject a hypothesis? If a significance level is used to decide whether a null hypothesis is true or not, note that the level, such as 0. Almost all prior information is ignored and no opportunity is given to incorporate what we already know. The subjective elements of classical statistics, such as the choice of null hypothesis, determining the outcome space, the appropriate significance level and the dependence of significant tests on the stopping rule are all swept under the carpet.
Bayesian methods put them where we can see them - in the prior. With little loss of generality, let us consider a simple problem of inference. Assume that we have a large population with known mean and one sample. All of this makes up our evidence, E. Our hypothesis, H, is that the sample came from a different population one with a different mean.
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