Paper presented at the 14th International Meeting of the International Huntington Association held in Denmark 2001

Understanding Challenging Behaviour in Huntington's Disease
Julie Snowden
Cerebral Function Unit, Greater Manchester Neuroscience Centre, Hope Hospital, Salford, M6 8HD, UK.

The need for recognition of problem behaviours
Changes in behaviour are a central feature of Huntington's disease (HD), which arise because of physical changes in the affect person's brain. Behavioural changes are often the most distressing part of the condition and create the greatest challenge for carers. Nevertheless, they have been relatively neglected by medical professionals and researchers and are often poorly understood. One reason is that they are less obvious than involuntary movements and may not be apparent during the brief period of a clinic visit. Moreover, problem behaviours are most likely to occur in the home and to be directed towards those family members and carers to whom the person with HD is closest, not towards relative strangers. Thus, behavioural problems are likely to be underestimated by outsiders.

Health professionals are, however, at last beginning to realise the enormous impact on families of behavioural symptoms. If new treatments for HD are to be successful they will need to benefit the behavioural aspects of the condition as well as the movement disorder, which means that it is increasingly important that we should understand why those behavioural changes occur. So how can we unravel the different components of behaviour?

HD is often said to give rise to a triad of symptoms: a disorder of movement, together with changes in intellect and in mood. Both the intellectual and the mood changes are likely to contribute to how a person behaves. How people behave reflects the way that they think (cognition) and how they feel (emotions). To understand HD behaviour it is necessary to understand how the structural changes in the brain alter both thinking and emotions.

Cognitive changes in HD are specific and predictable
The cognitive changes in HD are very often described as a dementia. Usage of the term dementia is unfortunate since it is very often taken to mean a generalised impairment, the implication being that mental abilities are impaired in a global and diffuse way. People with HD do not have global intellectual impairment. There are good reasons why that is so. Degenerative diseases that affect the brain, such as HD, do not damage the entire brain in a non-specific way. Rather they preferentially damage and disrupt the function of certain parts of the brain while other parts of the brain continue to function well. Since different parts of the brain serve different functions, the type of mental change that a person has will be characteristic for a particular disease and will be governed by the regions of the brain preferentially involved. Thus, mental changes are both specific and predictable.

Brain changes in HD
HD particularly affects deep structures within the brain, known as the striatum, which are important for the control of movement. These deep structures have connections to the cerebral cortex (the outer covering of the brain) and in particular to the front parts of brain (frontal lobes). Many of the cognitive changes in HD are a direct result of impaired functioning of these specific brain circuits, which link the striatum to the frontal lobes.

Functions of different brain regions
So what do the different parts of the brain do? The more posterior parts of the brain are important for making sense of what is perceived through the senses. They are important for processing visual information and being able to recognise what one sees: for example, recognising that a chair is a chair, and knowing whether two chairs look the same or different. The posterior parts of the brain are important too for processing auditory information: in converting sounds of words into meaning. Thus, they are necessary for recognising that the sound d-o-g refers to the four-footed animal that barks and not for example, to the bird that flies in the sky or the fish swimming in the sea. The ability to process and interpret what is perceived through the senses can be thought of as the tools or building blocks of thought. These building blocks, which provide the foundation of cognition, are preserved in HD. They may, however, be impaired in other brain disorders. A person who has Alzheimer's disease or who had had a stroke may have difficulty recognising objects and other visual stimuli. They may also have difficulty understanding what words mean. The reason is that those conditions can affect the parts of the brain important for these fundamental information processing skills.

If the posterior parts of the brain are important for the tools of thought, for recognising what we see and hear, what is the role of anterior (front) parts of the brain, which are damaged in HD? The front parts are the "captain of the ship". Imagine on a ship there are a variety of instruments, used for navigation and for communication. They are like our instruments or tools of thought. However, even when those instruments are all in working order, the ship does not function on its own. It needs a captain to plan and organise the journey, to attend to the instrument panels and communication systems, abstract out relevant information and ignore what is not relevant, to check incoming information and to have the flexibility to alter a course of action if circumstances change. The captain has a supervisory function, in regulating and controlling what happens. The front parts of the brain are important for those same functions and they are sometimes referred to as the executive or supervisory system of the brain. These regions are necessary for planning, forward-thinking, goal-directed behaviour, for the ability to organise behaviour, attend to what's relevant and ignore what is not relevant, to monitor and check performance, and to adapt behaviour to altered circumstances and different social situations. It is in these areas of cognition that people with HD have particular difficulties.

Clinical assessment of cognitive skills
People who attend an HD clinic may sometimes be asked to undergo psychological tests. The tests typically tap a range of cognitive abilities and are designed to identify the sorts of difficulties in thinking that the person has. This information is helpful both in understanding the person better and in monitoring change. As new treatments for HD become available it will increasingly become essential information for evaluating the benefits of those treatments. It is by means of these cognitive tests that it has been possible to identify the characteristic pattern of difficulties in people with HD; the problems in planning, structuring and organisational skills, in attention and attentional switching, and in mental flexibility.

The Impact of cognitive change on Behaviour
Initiative and Drive
The ability to plan and think ahead is an important motivator of behaviour. We think of tasks that need to be done and why we should do them now. That is, we are stimulated into action. Since the capacity for forward thinking is impaired in HD, it means that people with HD become essentially passive. They react to things that happen, but do not actively initiate activities. They are reactive but not proactive. One common characteristic is that people with HD may seem content to do nothing. If left to their own devices, they might lie in bed all day or sit watching television. This can, of course, be exasperating to a busy partner, who may resent the fact that all duties and responsibilities fall on them. However, the person with HD is not being lazy. The brain changes in HD mean that there is a loss of drive and initiative, so that the person cannot self-motivate. The stimulus needs to come from outside rather than within. Doing tasks together can be helpful since the activities of the partner acts as a stimulus to the person with HD.

Thinking ahead
The ability to think forward means that we sacrifice short-term rewards for longer-term goals. An obvious example is that young people study for exams even though they would prefer to be socialising with friends, because they think that it will be beneficial to their future prospects. We don't, as a rule, spend all our monthly salary on an expensive luxury, because we know that we will need money to buy food over the next month. That is, we are able to see the future consequences of a course of action and we modify our behaviour accordingly. If the capacity for thinking forward is lost as in HD, then the person does not see future consequences, and behaviour is governed much more by immediate needs and desires rather than longer-term goals. The person with HD may seem to want immediate gratification. The person is not being deliberately demanding. It is just that they are no longer able to think long-term.

It is important to recognise this characteristic because it has implications for our interactions with people with HD. Imagine, for example, that a friend invites you to go shopping that afternoon, and that you answer "no". There may be multiple reasons influencing your decision: you do not want to be in crowded stores on a fine day, you are saving for your holiday and do not want to be tempted to spend money, you ought to attend to tasks at home. There would be no point in your friend inviting you again after ten minutes, because all those reasons would still apply. For someone with HD, the response "no" may be much more short-term. It may mean that the person does not feel like moving from their chair at that moment, or wants to continue watching the current television programme. In ten minutes, the situation could change. It is not that the person with HD is being awkward or fickle. It is that decisions are based much more on immediate than long-term considerations.

Organisational skills
Our activities involve organisation and ordering. In the office, we might, for example, file away papers relating to one task, before getting out of the filing cabinet papers relating to another task, so that the two sets of material do not become muddled. We prioritise things that we need to do so that we can meet deadlines. People with HD have difficulty with organisation and sequencing, so that their performance can often seem disorganised. This can represent a problem in the early stages of HD when people are still at work. The person with HD will not have forgotten how to do their job, but performance may be lowered because of difficulty in organising the work efficiently.

Attention
People with HD have difficulty doing two things at once. Many of the things that we do each day that we take for granted involve coping with multiple tasks simultaneously. For example, when driving a car, we carry out the mechanics of driving, whilst also attending to road signs and conversing with a fellow passenger. We carry out these tasks as relatively automatic routines. To understand the difficulty encountered by people with HD, think back to the experience of being a learner driver. You may remember a time when you needed to concentrate so much on the mechanics of driving, such as steering, changing gear and signalling that you did not notice road signs and traffic. You may have found it difficult to hold a conversation while driving. That is, your attentional resources were overloaded. The situation is similar in HD. Activities that we take to be relatively automatic, such as walking and talking require more conscious attention for people with HD, so their attention system is easily overloaded.

Aside from overload, there is another reason why people have more difficulty carrying out two tasks; difficulty in switching of attention. Under normal circumstances, one of the reasons that we are able to deal with multiple tasks, even those that require conscious attention, is that we can switch attention between tasks. We can, for example, switch attention momentarily away from a television programme in order to answer a question and revert back to the programme without difficulty. A person with HD has difficulty doing so. The practical implication is that people should try to avoid where possible placing multiple simultaneous demands on someone with HD. One thing at a time is best. It is worth keeping in mind that tasks that seem easy to us, such as answering a question while watching television may actually be difficult for someone with HD.

Self-monitoring and awareness
People with HD have difficulty in monitoring and checking aspects of performance, so they may not be aware of errors that are apparent to others. The impression given to an employer when someone is in the early stages of HD may be that the person has become careless. That is not the case. It is simply that the person is no longer able to carry out efficiently the monitoring programme that would keep errors in check. It is worth bearing this difficulty in self-monitoring in mind when individuals with HD declare that there is nothing wrong with them. They may genuinely be unaware of the changes that are so evident to others.

Mental flexibility
Loss of mental flexibility means that people with HD may seem rather rigid in their behaviour. They may like their own routine, and seem unwilling to try anything new. They may seem poorly adaptable to changed circumstances and new situations. From a management point of view the implication is that changes, wherever possible should be introduced gradually. It is better that the person with HD is told of prospective changes in advance and has time to get used to them rather than have them imposed abruptly.

HD patients have difficulty seeing things from alternative perspectives. This inevitably has an impact on inter-personal relationships. The person with HD may sometimes seem thoughtless and selfish. However, they are not being intentionally uncaring. To have sympathy or empathy with other people one needs to be able to see things from the other persons point of view, to appreciate the other person's own needs and feelings. In HD the brain, changes may prevent them from seeing things from another perspective and appreciating the needs and feelings of others.

Mood changes in HD
There are a number of emotional changes that may occur in HD. People with HD may show irritability and feelings of anxiety and agitation. They may be emotionally volatile, seeming to flare up and losing their temper for no apparent reason. Depressive symptoms may also occur. In the later stages of HD, people may show emotional blunting with a loss of the emotional warmth and range of emotional expression that they demonstrated before they became ill. One can think of these mood changes as separate from the cognition-based behavioural changes described above. Nevertheless, it may well be that there are interactions between the two. Suppose for example that a person with HD loses his/her temper when asked a question while watching television. The person is showing the volatility and loss of emotional control, which are mood-based changes of HD. However, the person is being asked to do something that is actually rather difficult for someone with HD - switching attention from one task to another. The feeling of irritability might stem from the fact that the person finds it hard to switch attention efficiently away from the television to the conversation at hand and then back to the television. It is easy to interpret emotional outbursts in people with HD as "out of the blue" or "over nothing". It is worth bearing in mind that what may seem trivial to us may actually be a difficult task for some one with HD. It may be that cognitive demands are being placed on the person with which he/she is unable to cope and that this is the basis for the outburst. Regardless of the cause it is better to avoid confrontation in response to an outburst. It can be difficult for people with HD to see another person's point of view and to follow their reasoned argument even during periods of calm. They will certainly have difficulty doing so during periods of high emotion.

The frequency of behavioural problems in HD
Behavioural changes vary in severity in different people. For some people they may pose few practical problems whereas for others they create major problems in management. Also, some behavioural problems are more common than others. We have developed in Manchester a questionnaire of Problem Behaviours for use with HD patients and their carers. The questionnaire taps a range of aspects of behaviour including drive and initiative, quality of task performance, the ability to persevere on tasks, judgement, self care, thoughtfulness towards others, mental flexibility, social awareness, emotional warmth, temper control. We found that some behavioural changes are reported very commonly: in up to 80% of people who attended our regional HD clinic. These symptoms include loss of drive and initiative, reduced efficiency of task performance, impaired judgement, mental inflexibility and self-centredness. Since many of the people who attend the clinic are still in the early stages of HD, the high frequency of those symptoms suggest that they are likely to be fundamental to the disease process. Mood changes such as irritability and emotional volatility and depressive symptoms are also relatively common, being reported in up to 50% of individuals. Frank psychotic symptoms such as delusions and hallucinations are only rarely reported. This suggests that these latter symptoms are not an intrinsic or inevitable part of HD. It may be that HD has the effect of increasing the likelihood of such symptoms in people who have a prior susceptibility.

Cognition-based versus mood-based behaviours
It has been implied earlier that some behavioural changes are the consequence of cognitive difficulties (cognition-based behaviours), whereas others reflect a person's mood (mood-based behaviours). If that assumption is correct then it would be anticipated that so called cognition-based behaviours should correlate with cognitive change (i.e. the presence and severity of one should predict the other). However, if mood changes have separate underlying mechanisms, then there ought to be a much less well-defined relationship. This is exactly what occurs. Behaviour changes fall into distinct, identifiable behavioural clusters. Behavioural changes relative to drive, initiative, perseverance and judgement (i.e. behaviours that we would anticipate intuitively to be cognition-based) do indeed show a strong relationship to actual cognitive test scores. In contrast, mood changes such as depression and irritability show no statistical relationship to the severity of cognitive disorder.

Behavioural changes and stage of HD
Cognition-based behaviours such as loss of drive and initiative and poor perseverance show a systematic worsening over the course of HD. This suggests that these aspects of behaviour are fundamental to the disease process. In contrast, mood changes do not show such a systematic worsening. It appears that HD predisposes people to certain mood changes such as depression, with the result that the incidence is greater than in the general population. However, such mood changes, if they occur, may present themselves at any stage of the illness. Bouts of depression may occur with apparent randomness and then resolve. Irritability may peak and then decline. Mood changes are amenable to treatment. People with HD can benefit significantly from standard medical treatments for depression, anxiety and irritability, thus improving quality of life both for suffers and their families.

Effects of disease versus reaction to disease
It is sometimes questioned whether the behavioural changes in HD, particularly those relating to mood, are an inherent part of the disease process (i.e. a result of the physical changes that take place in the brain) or a secondary reaction to having a distressing and debilitating condition. The foregoing sections place a great deal of emphasis on changes that are part of HD and result in structural brain changes. That emphasis is deliberate, because understanding what the disease does to the person is essential to understanding the person with HD. However, that is not to say that there are not also reactive components. People with HD have life changes imposed on them: they may lose their job, their social life, their mobility and their independence. Their symptoms may be misinterpreted. They may, later in the disease, have difficulty communicating their needs and wishes. It is not surprising that there are times when people with HD show irritability and frustration. Often, behaviour is not just the direct effect of HD or just a reaction to it. It is a combination of the two. This is well illustrated by an incident involving a man with HD. As he was walking along he was stopped by the police and accused of being drunk. As he was entirely sober the man felt insulted and outraged, hit the policeman who then arrested him on a charge of assault. Many people with HD have parallel experiences in which their symptoms are misinterpreted by others. The man's feelings of anger can be seen as an understandable reaction, and it is a feeling that most people would share. Nevertheless, in a comparable situation most people who do not have HD would immediately be aware of the potential repercussions of hitting a policeman and realise that it would not be in their best interests to do so. They would, moreover, have the capability of suppressing their feelings of outrage. The man with HD could neither foresee the consequences of his actions, nor could he keep his feelings of anger in check. Those features are the direct effects of HD.

Conclusion
HD can be a destructive condition, because it may lead to behavioural problems that damage social and family relationships. It is, however, the disease and not the person that is at fault. People with HD are not being deliberately thoughtless, awkward and uncaring. It is the disease that gives rise to changes in behaviour, over which the person with HD has no control. There are not easy answers to behavioural problems. However, understanding why people with HD behave in the way that they do is important, since it may provide clues to circumventing problems. At the very least, understanding behaviour is a step towards better understanding of the person with HD, placing families and carers in a better position to provide optimum support and care.