Abstract
Stereotypic behaviors are one of the more common behavior problems seen in captive wild animals. For years it was believed that these behaviors were primarily a result of barren captive environments. However, it has been noted in many instances that simply improving the environment did not always completely stop the behavior. Much research followed that focused on the treatment of stereotypic behavior with environmental enrichment before we even had a very good understanding of what caused the behaviors. The biggest question remains today: why do some animals perform stereotypies and others in the very same environment do not? More recent research has given us some insight into the complex variety of factors associated with the development of stereotypic behaviors as well as the possible neurobiologic basis of the behaviors.
Stereotypies have been defined as invariant, repetitive behavior patterns without obvious goal or function.13 They typically develop from normal motor patterns, such as those associated with foraging, grooming, or eating. In the beginning, there may be some variation in the behaviors but with time, they become more fixed and inflexible. Stereotypic behaviors can vary dramatically between species and individuals within a species.
Interestingly, for a behavior that is defined as “without function or cause” much of the research has focused on looking for the cause of stereotypies. One hypothesis that has arisen suggests that stereotypies develop as a strategy to help animals cope with an adverse environment. Early studies focused on the self reinforcing aspect of the behaviors. It was hypothesized that the behaviors led to the release of endogenous opioids and individuals performing the stereotypies were self-narcotizing. Some studies have demonstrated that opioid antagonists do in fact disrupt the performance of stereotypies in some animals. Other studies have led to ambiguous results with some researchers concluding that “there is no evidence that performance of stereotypies results in increased opioid activity.”17 Overall there is no evidence that all stereotypies help animals to cope.17,22
The one common unifying feature among animals exhibiting stereotypic behaviors is the presence of frustration: frustration that appears to arise due to the thwarting of very highly motivated behaviors.3,17 The possibility that the environmental constraints placed on captive animals leaves them in a constant (or at least frequent) state of high motivation, has been considered by many as the more likely cause of stereotypies.11,17,22 Motivated behaviors typically have an appetitive phase, the first phase of a behavioral series, that leads to a consummatory phase or “end act.” Motivation is in some cases controlled by negative feedback: for example, if consummation is successful (the leopard makes a kill) then the motivation to perform the appetitive behavior is decreased (the leopard stops hunting). The term “appetitive” can be applied to many behaviors, such as foraging, exploring, searching for a mate, or migrating. Motivational theories suggest that too often in captive animals, the appetitive phase of a behavior does not culminate in appropriate consummatory behavior, or the consummatory behavior does not follow a normal period of appetitive behavior. The failure of the negative feedback loops often leaves animals in a high state of motivation resulting in frustration related stress. Any number of unusual behaviors may follow.3,11,17,22 The failure of some animals to stop the behaviors even after being placed in more appropriate environments that allow them to express more of their innate behaviors, has led some to suggest that stereotypies are the equivalent of a “mental scar” and do reflect some level of brain dysfunction.11,17 Their continued presence is reflective of the frustration that occurred earlier in the individual’s history.
Increasing evidence suggests that dysfunction within the basal ganglia of the brain is the underlying source of stereotypic behaviors.5-8,12,21 Malfunction in the circuitry involving the basal ganglia and the prefrontal cortex has been shown to lead to perseveration of behavior, an inappropriate repetition of behavior and an inability to shift goals. Further, these studies suggest that stereotypies and impulsive/compulsive disorders are a result of dysfunction in two different systems within the brain and that they are two distinct classes of repetitive behaviors.5,9,12,15 Impulsive/compulsive behaviors are repetitive, but unlike stereotypies, they are goal directed and they usually vary in the form of the motor patterns. The key difference between the two is in what is repeated. With stereotypies a motor pattern is repeated, such as walking a particular route in the cage and placing each foot in the same location every time. With impulsive/compulsive behaviors, an inappropriate goal is repeated, such as plucking feathers.5 The distinction may prove critical in guiding future research and in our understanding of the prevention and treatment of these conditions.
Brain dysfunction may explain some of the mechanisms leading to repetitive behaviors but it appears that a variety of developmental and genetic factors may predispose individuals to develop the behaviors. It is notable that these factors are not necessarily the same as those environmental factors (such as barren environments) that elicit them. For example, a recent study in horses found that those animals with stereotypies had higher baseline levels of opioids than those without, suggesting some neurochemical difference in the animals that leads to the development of the behavior.1
Studies of the genetic basis of stereotypies are also offering some intriguing findings. There are distinct differences in the propensity to develop stereotypies within species. For example, in one species of vole, it has been found that the offspring of mothers who exhibited stereotypies had a higher incidence of stereotypies than did the offspring of the non-stereotyping mothers.18 In other rodent species, it has been shown that levels of stereotyping run in families.18,19,22
Developmental factors may also play an important role. Many studies have shown the lack of environmental complexity can be damaging, especially on young, developing animals. Animals raised in barren environments during the early weeks, months, or years of their development have fewer neurons in the brain, decreased dendritic branching and spine density, reduced synaptic connectivity and a higher incidence of stereotypies than animals raised in enriched envrionments.2,12
In addition to impoverished environments, other situations that cause severe stress, such as early or abrupt weaning, can also lead to abnormal neural development. When individuals are under extreme stress, they experience massive release of endogenous opioids. The presence of these opioids at an early age may sensitize the dopaminergic systems in the basal ganglia, possibly leading to the dysfunction that results in stereotypic behaviors.11,12,22
Research now suggests that early environmental complexity has a protective effect. This may explain why some wild caught animals exhibit fewer stereotypies in barren environments than animals born and raised in captivity. For example, a survey of adopted feral horses found that the feral horses had a much lower incidence of stereotypic behaviors than has previously been reported for other populations of horses.4 Black rhinos, bank voles, and African striped mice have all been shown to be less prone to stereotypies when wild born rather than captive born.12,18,19 In captive settings, studies have shown that exposure to more complex environments may be effective when provided at a variety of different times during development and the timing may be more important than the duration of the exposure.2,10,12,14,16,22 Studies in orange winged amazons have shown that stereotypies may be prevented and reversed by exposing them to more complex environments.14
A great deal of research has been conducted on the role of environmental enrichment in the treatment of existing stereotypies. These studies do suggest that environmental enrichment effectively decreases the performance of stereotypic behaviors by 50% in most cases. However, it is notable that most fail to completely eliminate the behaviors.20 No matter what the original cause of a stereotypy may be, repetition strengthens the behavior by sensitizing the neuronal pathways involved. Treatment plans should be initiated immediately upon discovering an animal engaging in repetitive behaviors to be most effective. Animals that have been engaging in repetitive behaviors for years, or even a few months, are unlikely to completely stop the performance of the stereotypy.
Effective enrichment must be biologically relevant for the species being enriched. Caretakers should, to whatever extent possible, consider environmental changes that: increase opportunities for the animal to express species typical behaviors, appropriately increase sensory stimulation, and remove sources of stress for the animal.20 Anything that increases an animal’s control over the environment may be stress relieving and improve the animal’s welfare. Where opportunities to modify the environment are limited or where they do not decrease the stereotypic behavior to a level that caretakers consider acceptable, pharmacologic therapy could be included in the treatment plan. Few controlled studies treating repetitive conditions in animals exist, so our knowledge is quite incomplete at this time. Tricyclic antidepressants (clomipramine in particular), the selective serotonin reuptake inhibitors, dopamine antagonists and the neuroleptics may all be effective at treating stereotypies.15 As we learn more about the neurophysiologic basis for the different repetitive behaviors, our ability to use these medications in a safe and effective way should continue to improve. Part of any treatment plan for repetitive behaviors must include systematic documentation as to how often and under what circumstances the animal performs the behavior. Only by documenting behaviors before and after different aspects of treatment have been initiated, can we truly learn what works and what doesn’t.
While much has been added to the body of knowledge regarding stereotypic behaviors, much remains to be learned. The emphasis should continue to be on prevention by providing animals with complex environments and reducing stress during sensitive developmental periods. When possible, removing stereotyping animals from a breeding pool should even be considered. Research should continue to focus on understanding the multiple factors involved in the development of these behaviors. Ultimately, our goals should be to eliminate the cause of the behaviors, rather than continuing to treat the symptoms.
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