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An evolutionary approach
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An evolutionary approach to the analysis, assessment and treatment of behaviour
problems in companion animals
*Dr. Daniel Mills dmills@lincoln.ac.uk,
Gill Sheppard
* Author for all correspondence
The nature of behaviour and behaviour problems
Understanding the nature of behaviour problems is essential to developing a
rational basis for their treatment. Behaviour problems arise as a result of an
interaction between factors relating to the current environment and developmental
factors within a patient of a given state. Not all behaviour problems represent
dysfunctional, abnormal or maladaptive behaviour since "the problem is the
not the animal’s behaviour per se but rather the problem that this behaviour poses
for its owner" (Askew 1996). Broadly speaking behaviour problems may
be divided into behaviours which are adaptive but inconvenient for the owner,
those which are derived from attempts to behave in an adaptive way in a suboptimal
environment and those which are truly maladaptive e.g. seizure activity.
The causes of behaviour may be investigated at a proximate or ultimate level
(Mayr 1961). Proximate explanations relate to the environmental stimuli and mechanisms
within the individual which bring about the physical expression of the behaviour;
they describe the pathological and aetiological processes with which veterinary
surgeons are familiar in normal clinical practice. The ultimate explanations describe
why such proximate processes should come about; they explain the function or adaptiveness
of the processes. Tinbergen (1963) suggested that a full explanation of behaviour
was to be found at four distinguishable but complementary levels: phylogeny (evolutionary
history), ontogeny (development within an individual), mechanism and adaptive
value. This paradigm has now become a central tenet to ethology. Unfortunately,
within the field of animal behaviour therapy, there has tended at times to be
a fragmentation of this unifying model with emphasis being given to particular
levels according to the philosophical standpoint of the therapist, which may be
medical, psychological or more purely ethological. Clinical ethologists tend not
to adhere rigidly to a single model as it is generally accepted that internal
and external causes interact in the development of a disorder. However, one type
of cause does tend to be emphasised at the expense of other possible explanations.
(Sheppard & Mills 1998).
Ethological explanations which focus on the ultimate factors governing behaviour
are widely used for the category of problems which consist of adaptive, species
typical behaviours which are inconvenient for the owner, like urine spraying in
cats and hierarchical aggression in dogs (Borchelt and Voith 1982). However the
potential for an ultimate analysis of behaviour problems which have traditionally
been thought of as psychopathologies, is a much more recent phenomenon. These
problems tend to be analysed from a behavioural or medical perspective which concentrates
on proximate explanations of behaviour (Mills 1997).
Criticisms of existing models
Many of the difficulties that are faced in investigations of psychological
problems in animals have been apparent for much longer in the field of human psychiatry.
Kraepelin proposed the first comprehensive system for the classification of
mental disorders in 1896 and his view still holds enormous influence in the field.
His beliefs are the core of the biomedical model and its associated problems.
He suggested that psychological disturbances represented a pathology in much the
same way as physical problems, and that diagnosis should be based on the description
of symptoms. This view rapidly gained popularity as his work was soon supported
by the experiments of Krafft-Ebing (1897) who demonstrated that mental illness
could have an infectious cause, in the case of syphilis (Rosenhan and Seligman
1995).
Emphasis on the description of symptoms is the main feature of the Diagnostic
and Statistical Manual of Mental Disorders (4th edition). This is atheoretical
with regard to the aetiology and development of disorders and was developed to
facilitate clinical practice and communication, with clinical utility its highest
priority (American Psychiatric Association, 1994). Individuals are categorised
within the same diagnostic group on the basis of similarity in signs and symptoms.
Descriptive criteria determine diagnoses, resulting in a classification system
that is mostly based on superficial similarities in signs and symptoms. The system
may provide precise criteria for diagnoses but not precise boundaries. Diagnoses
can be based on meeting a certain number (but not necessarily all) of a list of
criteria. For example, dysthymic disorder requires the presence of two symptoms
from a list of six. The diagnostic categories may thus ignore and conceal important
individual biological differences between patients with the same diagnosis (Dubovsky
and Butler, 1995).
DSM-IV is based on the classical nosological approach and leads to explanations
of disorders being sought in terms of:
Clusters of co-occurring signs and symptoms
The definition of disorder
Biological markers and causes
Some authors (e.g Maas and Katz, 1992) have suggested that the classical nosological
approach has been a hindrance to investigations to identify specific causes of
psychiatric disorders; a field which has produced a very low return for the amount
of research invested into it. The problems that have emerged may be due to an
incompatibility between the nature of psychiatric disorders and the form of nosological
categories (Clark et al, 1995).
The nosological approach aims to develop a series of categorical diagnoses
that are mutually exclusive and jointly exhaustive (Goldberg and Huxley, 1992).
Since disorders are viewed as discrete entities with discrete bases that are usually
assumed to be biological (Kendell, 1982), most research aims to identify specific
brain dysfunctions as causal factors. However, psychiatric disorders are not discrete
in nature; symptoms are not all-or-nothing phenomena. They occur with varying
degrees of severity and appear to exist on a continuum, blending with normal behaviour.
Categories impose arbitrary and imprecise boundaries on such a continuum and may
overlap or leave gaps that are not covered by the diagnoses. This creates difficulties
in fitting clinical presentations to diagnostic criteria. It may also result in
diagnostic categories that reflect quantitative differences rather than qualitative
ones. Additional categories may increase the coverage of the continuum and decrease
the likelihood of gaps alternatively they may be used to create smaller categories
and more specific diagnostic criteria. However, additional categories increase
the likelihood that diagnoses overlap, resulting in comorbidity when only one
disorder is present (Frances et al, 1991). They also increase the difficulty in
categorising borderline cases that do not fit easily into a diagnostic group.
Despite many years of refinement, DSM-IV still requires "dustbin categories"
to ensure that all clinical presentations can be accommodated within the classification
system. For example, "depressive disorder not otherwise specified" is
a category that can include all of the possible clinical presentations of depression
that do not fit elsewhere. Thus the categories of DSM-IV do not reflect discrete
biological processes.
Investigations of the aetiology of psychiatric disorders tend to assume that
diagnostic categories are valid. It is more likely that such categories have only
face-validity and investigations of these diagnostic groups are unlikely to identify
causes of disorders.
It is likely that disorders exist as dimensions that reflect the interaction
of multiple factors rather than the action of a single discrete cause. The growing
acceptance that disorders occur on dimensions is indicated by the increased use
of terms such as "spectrum" and "continuum" in psychiatric
literature.
The rise of behavioural psychopharmacology has offered the possibility of using
pharmacological probes to help elucidate the biological bases of various disorders.
The inferences drawn from such experiments must be made with caution and cannot
easily be used to form a nosological framework. Response to treatment does not
necessarily correlate with a change in the causal mechanism of the problem (Lader
1991). Treatment may be only symptomatic and thus indirectly supportive of the
pathological organ. Lader (1991) illustrates this point well by reference to the
use of diuretics to treat congestive heart failure. Understanding the action of
diuretics on the kidney, does not help us to understand the processes behind the
failing heart. Similarly, heavy sedation may prevent a problem response from occurring
without addressing the mechanism behind the behaviour (Cooper and Mills 1997).
By way of a more subtle example of this logical fallacy, benzodiazepines were
the standard anxiolytic against which newer preparations are assessed, but there
is no evidence that there is a specific benzodiazepine receptor with a specifically
anxiolytic function (Petersen et al 1986), rather it has a more general effect
on the chloride ionophores of inhibitory GABA receptors. Many other compounds,
like tricyclic antidepressants and monoamine oxidase inhibitors (Shader and Greenblatt
1983), which do not act through benzodiazepine receptors also have anxiolytic
properties. Psychological phenomena, including disturbances, tend to be the product
of a dynamic interaction between several central systems which result in a co-ordinated
response. Until the neurophysiological mechanisms behind a condition are fully
elucidated we must consider the possibility that response to a particular type
of antidepressant, antipsychotic or anxiolytic may be operating at only a phenomenological
and not necessarily a specific mechanistic level. The doses of drugs prescribed
and the systemic levels which result, are also many times in excess of any natural
biological level. It is then to be expected that their effects will extend beyond
the specificity of any known drug-receptor interaction. In this context, the action
of drugs may be far from correcting any supposed biochemical imbalance underlying
the problem, but rather chemically flooding the system to oppose a behavioural
tendency. In which case drug therapy is again not treating the cause but rather
stimulating a system which will mask the symptoms. It is not surprising therefore
that treatments are not specific to one disorder but are partially effective across
a range of disorders. None are consistently effective in the treatment of a diagnostic
group, no matter how narrowly it is defined (Kendell, 1989). Other concerns relating
to the use of the pharmacological approach to understand the biology of psychological
problems relate to the lack of a predictable relationship between disorder and
treatment response and prognosis. Thus the diagnosis is of limited value to the
choice of treatment and predicted prognosis (Clark et al, 1995).
Since psychological disorders in animals appear to share a similar inherent
structure and mechanism to human psychiatric disorders, it is likely that investigations
of the former will be equally unsuccessful unless a more appropriate approach
is rationalised.
A proximate factor is not necessarily a primary cause. A neurophysiological
change that accompanies a disorder may be a response to another neurochemical
change or a response to an environmental event. For example, Raleigh, McGuire,
Brammer and Yuwiler (1984) investigated the association between social status
and serotonin levels in vervet monkeys. High-ranking male vervet monkeys have
serotonin levels that are, on average, almost twice as high as those of low-ranking
males. A high-ranking male that is displaced displays behaviours that appear similar
to those associated with depression in humans, and serotonin levels decline to
that of a low-ranking male. In this example the neurophysiological change follows
the environmental event.
Behaviour problems consist of clusters of behaviours and emotional states,
most of which are not specific to one disorder. If proximate causes are identified
they could be associated with one or more signs and may also be associated with
other disorders. The neurological processes underlying such general states as
depression, anxiety or phobic responses could be normal adaptive mechanisms rather
than a pathological process in the normal sense of the word. For example, fearful
behaviour in a dog is regarded as a disorder if it is too prolonged, too frequent
or occurs in the absence of an appropriate trigger. The difference between "normal"
and "abnormal" is subjective with such an approach and unsatisfactory
as a foundation for a clinical science (Mills 1997).
Mechanistic investigation is in danger of identifying the normal mechanism
that instigates a fear response as opposed to the primary cause of what makes
it inappropriate, which may relate to endogenous or exogenous individual factors.
The evolutionary approach
Biomedical and pharmacological models of psychological problems emphasise the
internal causes of disorders; by contrast, the behavioural and sociocultural models
emphasise external causes. In any case, each model implicates a specific type
of proximate cause in the development of behaviour problems and provides explanations
on that basis alone. Proximate explanations that give equal consideration to the
influences of internal and external factors have greater value but cannot provide
a full understanding of the causes of a disorder, as they do not evaluate the
potential role of ultimate factors involved. The importance of ultimate factors
such as function in the classification and treatment of ethological behaviour
problems is well recognised, and the evolutionary approach to psychiatry extends
this to psychological phenomena. The different levels of explanation proposed
by Tinbergen (1963) are interdependent in the construction of a paradigm for assessing
behaviour problems and so should have equal consideration. An evolutionary framework
enables us to integrate these different factors in a coherent manner and on a
sound basis, since the theory of evolution is the central tenet of biology.
The evolutionary approach to psychological change focuses attention on the
interactions of an animal with its environment and investigates their potential
functional value as well as the nature, source and degree of any perceived suboptimality.
Two stages of psychological evaluation can be recognised:
evaluation of the functional value at an evolutionary level of the psychological
process being evoked
evaluation of the functional capacity in situ of the process involved
The adaptive value of the processes of fear and anxiety in helping an animal
avoid or prepare for a noxious event are obvious, but other psychological processes
which may also feature as "psychological problems" may also have adaptive
value. Price et al (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. In these circumstances, a depressive response assists an
individual in deferring attacks from higher ranking individuals and helps in the
recruitment of social support from other members of the group, thus minimising
the impact of defeat and maximising the coping potential of the individual. However,
depression when alone might suggest a different function, such as withdrawal from
uncontrollably oppressive features of the environment (McGuire and Troisi 1998).
Behavioural and emotional responses are often considered to be disorders when
responses are too intense, too prolonged, too frequent or when they appear to
occur in the absence of an appropriate triggering stimulus. These responses could
however be adaptive in other contexts such as alternative genetic combinations,
different stages of the animal’s development, the opposite , or alternative
environments (Nesse and Williams, 1997). In which case the behaviour and psychological
processes behind it cannot be considered pathological. Normal population variation
means that individuals in a given population differ in the degree of baseline
optimality of specific traits. This is the raw material for natural selection
and evolution proceeds as a result. The sensitivity of different systems may need
to vary for optimal adaptation in different environments; consider the cosseted
pet with its feral neighbour for an extreme contrast. If suboptimality is due
to a mismatch between the animal’s adaptive range and the environment in which
it is placed the prognosis for psychological recovery is better than when there
is a genuine dysfunction of the trait. In the latter case, there is a real neurological
disturbance and the prognosis is considered much poorer (McGuire and Troisi 1998)
When a large proportion of functional capacities are highly flexible an individual
can adjust to and live successfully in a wider range of environments than when
functional capacities are more limited. However, the latter does not necessarily
exhibit any behavioural disturbance. For example, a dog with limited functional
capacities may be able to live in a quiet, rural environment without displaying
any signs of a behaviour problem, but in a noisy inner city area it may be unable
to adjust so well. This does not inevitably lead to any form of pathology but
it may lead to behaviour problems associated with a specific psychological state.
We can identify the two categories of response described above. Firstly the dog
may use unacceptable or concerning strategies to control its environment and help
it to cope. This might include increased aggression to repel strangers or a depressive
withdrawal. If this is identified, functional treatment should not seek to control
the behaviour per se but rather address the problem of compromised adaptability
which has led to it. Alternatively the mismatch between the animal and its environment
may be addressed in order to help the dog to cope in a more acceptable way. Even
if the pathways involved in the control of the behaviour become sensitised and
the response generalised to a wider range of stimuli, it still maintains a functional
form and so is not considered pathological.
If the situation is so prolonged or intense that it exhausts or defeats the
coping mechanisms, then we may start to see a truly dysfunctional behaviour. In
this case we have a genuine psychopathology, with the behaviour no longer structured
in a functional way. Prognosis in these cases is poor.
Thus disorders may represent attempts to behave adaptively in the face of limitations
and in other contexts be signs of an overtaxing of these and a true dysfunction.
The evolutionary approach is not a radical departure from that used currently
by other clinicians but provides further information for the management of cases
where psychological factors are significant. It is to be hoped that with this
approach a functional ethogram can be constructed against which an objective assessment
of behavioural pathology can be made. The approach has also helped in owner counselling
and a more rational application of psychopharmacolgy. For example, Mrs W. contacted
the Animal Behaviour Clinic for advice concerning her two neutered male Border
Terriers who had started fighting each other since they were nine months old,
some six months previous. The smaller dog (R) apparently initiated the attacks
despite being consistently defeated by its larger sibling (H). These would tend
to occur only when the dogs were on the lead. After a fight R would withdraw from
H, but stay within sight of the owner and appear "depressed". The owner
admitted to feeling sorry for R and was wondering whether or not he should be
rehomed, as she felt he no longer enjoyed life. Traditional treatment strategies
emphasise the need to reinforce the dominant and subordinate dogs’ positions but
this is difficult for owners to implement when they already feel guilty about
the subordinate’s quality of life. Alternatively, antidepressants may be considered
to improve the well-being of the subordinate dog. However, in this case, when
it was explained that the depressed behaviour was most probably functioning as
a care-soliciting behaviour designed to recruit owner support which maintained
instability in the unit, which was leading to these fights, the owner quickly
complied with the treatment strategy proposed. R was ignored whenever he showed
the depressed response and the owner made sure that H was never compromised in
the presence of the other dog, for example by being on the lead when R was free.
The owner was encouraged to allow the dogs to play competitive games like tug’o’war,
since H reliably won these by virtue of his size. After two weeks, there had been
only one fight, when H was startled whilst on his lead. The owner responded as
directed after the dogs had been separated and 8 months later there have been
no further fights. The owner also noted a marked improvement in the mood of the
R within these first weeks. In this case an evolutionary approach also predicts
that pharmacological intervention would be contraindicated, as serotonin re-uptake
inhibitors suppress submissive behaviour (McGuire and Troisi 1998). Thus treatment
of the depression would probably extend the range of situations when fights were
instigated. Whilst the evolutionary approach may not alter the treatment offered
in this particular type of case it provides a much more satisfactory explanation
of the situation than any behavioural or medical model. It helped improve owner
compliance and avoided the potential misapplication of pharmacotherapy. The pattern
of response seen in R, has since been noted in several other cases of sibling
competition seen by the author, and these cases have been managed equally effectively.
It is accepted that further research is necessary in order to investigate the
hypotheses that such an approach generates about the nature of the psychological
state of patients with supposed psychological disturbance. However, it is suggested
that this approach has the potential to explain the success and limitations of
the systems adopted and proposed by different experts within the field.
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