Veterinary Clinical Ethology
Concepts, History, Terminology and Future.

Gill Sheppard, Dr. Daniel Mills dmills@lincoln.ac.uk

Introduction

The practice of veterinary clinical ethology represents the application of a mosaic of science and practical skill; with the art of animal behaviour therapy being as old as civilisation itself and the science being born out of this practical experience and the importation of ideas from related sciences. It is only in the last couple of decades that clinical ethology has developed its own specific scientific agenda, (see Tuber, Hothersall and Voith, 1974). Not until 1997, did the various national veterinary interest groups make a concerted effort to host a truly global conference (Mills, Heath and Harrington, 1997). Perhaps this more than any other initiative has focused people’s attention on how the science has radiated in different ways in different cultures. Understanding the history of applied clinical ethology can therefore provide some explanation of the fragmented approach that has developed in the study of companion animal behaviour disorders. Different schools have emerged in different areas of the world, each emphasising its own theoretical traditions. Thus contrasting approaches have emerged influencing not only the terminology used but also the related classification of disorders and hypotheses generated about their aetiology. This paper seeks to examine and explain this phenomenon with a view to placing markers on the common road ahead.

Concepts and philosophies

The role of the environment and training has always been recognised in the modification of the behaviour of animals and this is one of the fundamental tenets of behaviourism. This philosophy dominated Anglo-American academic psychology up until the mid 1960s, and formed the cornerstone of the early therapeutic regimens for companion animals in these countries. It is typified by Barbara Woodhouse’s assertion that there are "No bad dogs" (Woodhouse, 1978). The behavioural model regards the behavioural signs and symptoms as the problem to be addressed. Diagnoses may not need to be made. Maladaptive learning or an absence of learning is assumed to be the cause and new learning is regarded as the appropriate treatment. Thus the cause of the problem is identified as something that is external to the animal. Behavioural methods are widely used to treat disorders but are usually used in conjunction with other methods. Dog-trainers still concentrate largely on the behavioural approach.

However, at the same time, some in these countries recognised that behaviour problem management was more than simply training and looked towards the medical models in psychiatry for further explanation. This approach considered not only the role of underlying physiology on behaviour but also the potential of central nervous system dysfunction. The early signs of a move towards a medical model of behaviour problems can be seen in 1975 by Bill Campell’s still relevant text "Behavior Problems in Dogs".

The medical model regards behaviour problems as signs and symptoms of an underlying tissue pathology and implies that the animal’s disorder has an internal cause. Such causes may include genes, disease, neuroanatomy or biochemistry of the brain. The medical model tends to emphasise physical treatments such as medication. More recently scientists like Overall (1997) have been champions of this cause, by proposing a whole taxonomy of behaviour problems in dogs and cats based on the approach used by the American Psychiatric Association for its Diagnostic and Statistical Manual (1994). Accompanying this shift is a move towards diagnostic rather than descriptive terminology. Thus various forms of stereotyped behaviour have become "obsessive compulsive disorders" (Luescher, McKeown and Halip, 1991).

On mainland Europe the value of psychiatry to the field was similarly recognised and employed in its own traditional way. Here there was an immediate emphasis on the potential value of psychopharmacology (Lapras, 1977 cited by Voith, 1991) and this continues today particularly within the French speaking community (Pageat, 1995). This group perhaps more than any other, has moved rapidly to incorporate the language of diagnostic psychiatry into the field. However the psychiatric traditions of France are somewhat different to other countries, being based on a combination of psychoanalytic- existentialistic philosophy and psychopathology (Gelder, Gath and Mayou, 1989) and so this has led to some confusion. Thus American researchers refer to cognitive dysfunction in the ageing dog as a suitable model of pre-Alzheimer changes in humans based on a combination of neuropathological and behavioural evidence (Cummings, Head, Ruehl, Milgram and Cotman, 1996). However Pageat (1995) and Bourdin (1997) refer to involutive depression to describe a condition with a similar signalment, behavioural signs and treatment. However Pageat (1995) emphasises the similarity between these behaviours and those expressed by puppies in a way which appears reminiscent of the regression referred to by psychoanalysts. Further evidence for this philosophical influence comes from the high value placed on items like oral exploratory behaviour in the scale developed by Pageat for the Evaluation of a Dog’s Emotional Disorder (EDED). The importance of such behaviours has not been previously recorded in the Anglo-American literature, but the use of this scale is now being more widely encouraged (Pobel, 1997).

Most clinical ethologists tend not to adhere rigidly to either a medical or behavioural model as it is generally recognized that internal and external factors contribute to the development of a behaviour disorder. Neither model, unless modified, is adequate to explain the full range of disorders that exist. Whilst the French-speaking veterinary community appear to have established the discipline well within its own profession, the British have encountered more difficulty. This probably reflects the fact that trainers, psychologists and animals scientists have led the development of the field in the U.K. with little liaison with human psychiatristry by the profession.

Taxonomy

Traditionally, function has been strongly emphasised in the classification of behaviour disorders (eg. Borchelt and Voith, 1982) as the same symptom may indicate different treatments according to its function. For example the dog that bites an advancing hand in order to protect a painful lesion requires a different treatment to the dog in the same situation which is motivated by social dominance. The functional approach can accommodate external and internal causal factors but a coherent and verifiable framework is required to integrate these elements. Without such a framework this approach often leads to multiple diagnoses, which raises questions over its validity (Mills, 1997).

The contrasting approaches that have emerged have resulted in classificatory systems that emphasise different aspects of behaviour disorders. Such emphasis can be limiting if other possible interpretations of behaviour are overlooked. However, despite the differences that have emerged, none of these approaches are necessarily incorrect.

Tinbergen (1963) identified four different types of response that may be given when asking about the origins of an animal’s behaviour. These responses may refer to the mechanism (i.e. the integration of biochemistry, physiology and anatomy), ontogeny (i.e. the developmental history within the individual), function (survival value) or evolution of the behaviour. Function and evolution are often referred to as ultimate causes while proximate mechanism and ontogeny may be considered to be proximate explanations (Alcock, 1993).

These four different types of response demonstrate how the same behaviour may be explained differently, according to which approach is adopted. The medical model and the behavioural model emphasise different proximate causes whereas classifications based on function place greater emphasis on ultimate causes. Individually, each of these approaches has value but only provides a narrow view of a particular behaviour. A neurophysiological change that is associated with a behaviour disorder is not necessarily the primary cause. It could be a response to other neurochemical changes or a response to environmental events (for a good example of this pheonomenon see Ray and Sapolsky, 1992). In order to view the behaviour as a whole it is necessary to consider all four of the possible causal explanations that Tinbergen highlighted.

A coherent framework is needed to integrate the different approaches that are currently in use and to direct research into the "gestalt" of behaviour problems. An evolutionary model could provide a suitable structure.

McGuire and Troisi (1998) have proposed the adoption of such an approach in human psychopathology as more traditional models have proved inadequate. Reference to both proximate and ultimate factors in the explication of a behaviour problem are not new as the numerous references to dominance aggression associated with the natural hierarchy of the pack can testify (eg. Borchelt and Voith, 1996; Askew, 1996). Nor is the idea that behaviour and psychological problems result from an incongruity between the adaptations possessed by an animal and the domestic environment in which it is kept (Fraser, Weary, Pajor and Milligan, 1997). However an evolutionary model, such as that proposed by McGuire and Troisi (1998) illustrates how these ideas and the observations of the different clinical ethologists can be universally integrated. It also puts the supposed disorder or mental disease state into a more rational biological setting.

Using an evolutionary approach a behaviour disorder can be viewed as a mismatch between an animal’s adaptations and its current environment. Such a mismatch may occur in companion animals if an inappropriate environment is provided, as most individuals will continue to operate in a proximate way according to the phylogenic physiological and behavioural rules of thumb which have been adaptive in an ultimate sense. The problem may then manifest itself as an inappropriate behaviour or the consequences of a lack of the necessary adaptations. A mismatch may also occur in a favourable environment as a result of an animal's impaired adaptability and functionality. However, behaviour that indicates such impairment is likely to have fitness benefits in other contexts. These different contexts could include alternative genetic combinations, different stages of the individual's development, the opposite sex, or alternative environments (Nesse and Williams, 1997). For example, fearful behaviour in a pet dog could be viewed as evidence of a disorder in the domestic environment. However, such behaviour is likely to be adaptive in a more extreme and dangerous environment such as that in which the animal evolved or that in which a feral animal lives. It would also be adaptive in a different genetic combination if such a combination resulted in a level of caution that was suited to its current circumstances. This approach encourages the examination of not only the animal's behaviour but also the context in which it occurs.

In psychiatry this approach has been used to challenge traditional functional interpretations of syndromes such as depression. For example, Price, Sloman, Gardner, Gilbert and Rohde (1997) hypothesise that depressive states are adaptive mechanisms that enable individuals to cope with defeat in social competition and to adjust to a low social rank.

A mismatch between an animal's adaptations and its current environment indicates the presence of a suboptimal trait, a dysfunctional state or a combination of these factors. A suboptimal trait is a phenotypic feature which results from interactions between the genotype and the developmental environment (epigenesis). Examples of such a traits could include low basal serotonin levels which may predispose an individual to depression or an ectopic ureter which means the animal is unable to avoid house soiling in the domestic environment. A dysfunctional state is a proximate change in a trait which may occur due to biological changes and/or environmental circumstances. Such states might include the anxiety produced by the impending departure of an owner of a dog with a separation problem or that produced by a brain lesion.

Suboptimal traits are likely to be more resistant to proximate treatment regimes than dysfunctional states but may respond to ultimate treatments such as selective breeding programmes. Thus suboptimality and dysfunctionality may affect treatment response which, in turn, may influence prognosis. The presence of both a suboptimal trait and a dysfunctional state may indicate a different prognosis than either factor alone. Physiological measures may help elucidate a biological marker of the problem but, without additional information, will not often distinguish between the suboptimal and dysfunctional. This will come from an evaluation of proximate states, traits and events (including environmental factors), the ultimate functioning of the behaviour systems of the individual and the relationships between these factors.

Detailed analysis of deviations in the normal functioning of behaviour systems will provide a complete picture of the clinical case. Behaviour systems can be divided into the following key components: the underlying motivation-goal; the processing of incoming information; the programme for the execution of the behaviour; the functional capacity of the programme (McGuire and Troisi, 1998). Behaviour disorders may be associated with compromised functional capacities which can result from dysfunction or suboptimality in other key components. Functional capacities may also be suboptimal or dysfunctional in their own right. A detailed analysis can identify in which component(s) the problem originates and whether suboptimality or dysfunctionality is implicated. In psychiatry this approach is claimed to be more useful than diagnoses based on DSM-IV for predicting treatment response and prognosis (McGuire and Troisi, 1998). An investigation of this nature is more likely to identify primary causes than is research that concentrates on specific proximate factors like neurotransmitter level.

An evolutionary approach can also direct research into considering ultimate factors which will enable knowledge of proximate causes to be fully utilised in both diagnosis and treatment. Thus when depression is viewed primarily as a psychopathology, emphasis naturally falls on correcting the underlying proximate neurochemical imbalance. However, when its value as an ultimately derived adaptive response to loss of status or resource is recognised (Nesse and Williams, 1995) the focus shifts away from treating the "disorder" per se and towards treating the proximate and ultimate factors affecting the individual. Since treatment becomes holistic and individually focused rather than condition based, it is likely to be more efficient.

Terminology

The different approaches to behaviour disorders have also produced a lack of agreement on terminology, as different authors have adopted different terminology or have applied different definitions to terms that are commonly used.

The use of psychiatric terms which refer to the cognitive status of the animal patient (eg. by Pageat, 1995 and Overall, 1997) has yet to be validated. Such use of this terminology either requires inferences about an animal’s thoughts or the acceptance of new diagnostic criteria for its application in this field. However, the existence of a long-standing definition for a term, such as obsessive-compulsive disorder, is likely to result in inappropriate assumptions being made about animals with this diagnosis.

It is not unusual for animals to be used to provide models for human psychopathology but certain criteria have to be fulfilled in order to promote validity. Stein, Dodman, Borchelt and Hollander (1994) recommend the use of pharmacological methods to compare the underlying neurobiology of human conditions with that of other animals. They also recognised the relevance of comparing the evolutionary origins of a behaviour. They concluded that "further empirical research is necessary to establish the relevance of veterinary disorders to psychiatry". Similar caution should be exercised if human psychopathology is to be used to provide models for animal behaviour disorders.

A descriptive approach is more objective as disorders are grouped according to similarities in signs and symptoms. However, problems have resulted from the use of this approach in DSM-IV (American Psychiatric Association, 1994). Similarities in signs and symptoms may reflect the presence of a single disorder or may be due to superficial similarities between two different disorders. Such superficial similarities do not necessarily imply that aetiology, underlying mechanisms, treatment response or prognosis will also be similar. For example, a dog that constantly licks at its paw in a repetitive manner may be displaying a displacement behaviour or may be responding to localised arthritis or an allergy.

A descriptive approach may also lead to the splitting of groups on the basis of superficial differences, resulting in two or more diagnoses when only one disorder is present. Differences between categories may be quantitative rather than qualitative, particularly if the same treatment is indicated by both diagnoses. For example, Odendaal (1997) differentiates between stereotypical behaviour and compulsive behaviour in his classification system. Such a distinction may result in more diagnoses than necessary. It may also encourage the adoption of a "shifting" classification, with new diagnostic categories being added, when a patient does not fit into a predefined category, without consideration of the validity of a new category of disorder.

Excessive splitting of groups may also occur due to individual differences in the behavioural expression of a disorder. The environment has an important role in shaping behavioural responses and variation in environments may result in inter-individual variation in species-typical behaviours. Behavioural signs and symptoms of disorders may be similarly effected resulting in animals with the same disorder receiving different diagnoses. Much has been written about classification problems that result from the use of a descriptive approach (for example see, Clark, Watson and Reynolds, 1995).

Classification systems should be based on more than the behavioural signs and symptoms that are displayed. It is also necessary to investigate the proximate and ultimate origins of the behaviour and consider treatment response and prognosis within this framework. It is unlikely that all of this information will be available but that which is should be utilised in order to develop valid terminology.

Future

The different approaches that have been adopted in veterinary clinical ethology have resulted in a field that is fragmented. The evolutionary model could unify and integrate these approaches in order to utilise the full range of knowledge that is available. It will also enable us to clarify what is known and identify areas of uncertainty in order to direct future research. This will provide a sound basis that will enable the field to develop and progress

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