David Appleby and Jolanda Pluijmakers
Although the modern dog successfully fulfils the role of companion, society places pressure upon it to meet its expectations about its behaviour and yet that same society frequently leaves them ill equipped to achieve these ideals. As a consequence of this failure many dogs are unable to cope with everyday situations without resorting to avoidance or defensive behaviour. The welfare of these dogs is at risk. They cannot relax and enjoy life, they feel threatened by everyday events and are susceptible to stress and disease. As a consequence they are less likely to make rewarding pets and are at risk of being abandoned, re-homed or euthanased.
A review of cases by the Association of Pet Behaviour Counsellors showed that aggression motivated by fear towards people (25%) and dogs (15%) were the most common reasons why dogs were referred for treatment by their vets. Fears and phobias, such as in response to sounds, was the reason why a further 8% of the cases analysed were referred. These figures probably represent the tip of the iceberg because many dogs display problem behaviour related to fear whose owners don’t seek help from a behaviour counsellor.
A dog’s temperament and character is dependent upon genetic and environmental factors. The extent of the influence of each is not clear, the old ‘nature-nurture’ argument. This is not the impasse that is often implied because it is safe to say that genetics govern the potentials the dog can achieve and experience and resultant learning shape behaviour and determines whether those potentials are realised. This shaping occurs throughout the dog’s lifetime but there is a biologically pre-programmed period in early life during which simple exposure to things or experience of interacting with them has greater influence on the development of emotional states and behaviour than in later life. During this time, called the sensitive period, the puppy learns what to expect and how to react, resulting in a sense of control and the capacity to remain in a positive emotional state in diverse situations. This organisation of a puppy’s behaviour forms the foundation on which the development of its subsequent behaviour is based.
Current understanding of the sensitive period has its origin in research conducted in the 1950s, 60s and 70s that suggested that fear of or reducing willingness to approach unfamiliar things develops in identifiable phases between 3 to 12 – 14 weeks of age. However, the interpretation of the results may have been misleading because the researchers depended upon observing changes in behaviour in response to the presence of unfamiliar stimuli. These changes follow the development and integration of the relevant brain structures and a period of learning that results in the organisation of the puppy’s behaviour. Therefore the sensitive period may be much shorter than the researchers assumed and looking at the sensitive period from the perspective of emotional development the most important phase is between three to five weeks of age.
It might be generally accepted that, like us, animals have emotional states such as fear and anger and sadness etc., Emotions enhance an individual’s chances of survival by improving its ability to recognize events that are useful or unsafe and to make appropriate responses. Situations that create a mismatch or conflict with an individual’s interests, give rise to negative emotions such as fear that require them to act in order to cope.
Whether an emotion is experienced as negative or positive is dependent on the activity of the dog’s autonomic nervous system, which is controlled by the brain. This system is functionally divided into two parts: arousal (Sympathetic) and relaxation (Parasympathetic). These have mutually exclusive actions. Conditions of stress trigger activity in the Sympathetic Autonomic Nervous System that has an emergency function, preparing the body for action. The effect includes increased heart rate, increasing blood supply to the muscles, heart and lungs, increased respiration and bowel movement, sometimes resulting in loss of toilet control, and chemical reactions such as the release of hormones. This activity co-occurs with negative emotional states described in humans as fear, anxiety etc. A positive emotional state (parasympathetic) has a recuperative function due to its opposite effect e.g. by restoring the blood supply and heart rate to normal.
Every individual strives to achieve and maintain emotional homeostasis, i.e. a positive emotional state. The function of emotional homeostasis is to allow an individual to deal with and adjust to the many changes that are part of everyday life. If every change in the environment caused a loss of emotional homeostasis the individual would never be able to relax and its welfare would be seriously impaired. To prevent this, a ‘picture’ of the world is formed early in life which sets the standard for situations during which they can afford to remain relaxed. Changes in the environment that deviate from this standard may cause a negative emotional state.
A dog’s capability to remain in emotional homeostasis develops throughout the sensitive period for behavioural organisation. During part of this process mental representations of stimuli are formed and associated with responses. Those associated with a positive emotional state become part of a set of animate and inanimate objects that enable it to maintain emotional homeostasis and organise its behaviour. The effect on subsequent behaviour was shown in three week old Chihuahua puppies fostered individually in litters of four week old kittens (Fox 1971). By twelve weeks of age, the cat-reared puppies preferred contact with cats over contact with other puppies that had not been fostered. Another experiment involved litters of puppies split into three groups. One group was hand-reared from three days old and received no canine contact. The second group was given equal canine and human contact. The third group only experienced other puppies and their dam. When these three groups of puppies were brought together at 12 weeks they showed a preference for puppies that had received similar rearing experience and the puppies raised in isolation from other dogs showed an overall deficit in their relations with other puppies (Fox & Stelzner 1967).
Some maintenance stimuli grow to be so important that the dog becomes dependent on their presence to maintain emotional homeostasis. This dependency can be formed to any social or non-social stimulus, as is illustrated by these experiments. Elliot and Scott (1961) found that puppies confined in a strange pen were three times more distressed than puppies confined in a familiar pen. Cairns and Werboff (1972) housed four week old puppies with adult rabbits and found that within 24 hours of cohabitation, the puppies lost emotional homeostasis when separated from their rabbit, which was expressed by intense distress vocalisations and attempts to escape and regain contact with the removed rabbit.
Dependency on social stimuli is more likely to develop than other stimuli because they provide more stimulation and easily become associated with important factors such as contact comfort, suckling or play. The duration of exposure to a stimulus and its availability are important factors in determining dependency. If a maintenance stimulus, e.g. a female owner, is present in a variety of contexts there is an increased likelihood that the dog will become dependent on her compared to other family members who are only present in some situations. A maintenance set that provides a dog with the best chance of maintaining emotional homeostasis consists of a large number of stimuli some of which are of comparable worth, which is necessary because the composition of the set alters with changes in the environment and situation the dog is in. The broader the maintenance set the more able the dog will be to cope with disruption of emotional homeostasis.
Disruption of emotional homeostasis can be caused by the loss of stimuli from the maintenance set, which leads to a feeling of reduced control. The extent to which disruption occurs increases with the importance of the lost stimulus or stimuli. For example, a puppy may whine all night after it is homed because the maintenance set it had built up at the breeder’s is totally disrupted when it is removed from its dam, littermates and the breeder’s house or kennel. Another example is provided by dogs that become so dependent on their owner’s presence that they loose behavioural organisation, manifested by an inability to stay in a positive emotional state, when left alone.
Things the dog finds frightening can also cause disruption of emotional homeostasis. These can be learnt if a stimulus becomes associated with a threatening event, such as darkened skies becoming a predictor of fireworks. Dogs may also react fearfully towards a stimulus because of its physical characteristics without having to learn that it is threatening. Examples include intense and/or sudden stimuli as gunshots, fireworks or thunderstorms. As behavioural organization increases, the presence of novel stimuli and stimuli that do not perform to expectation may lead to a negative emotional state and loss of emotional homeostasis.
The sensitive period of behavioural organisation can be divided into three stages.
A puppy’s initial maintenance set normally consists of its mother, littermates and nest-site. This is unavoidable because of the availability and salience of the stimuli and absence of opportunity to associate other stimuli with a relaxed emotional state because puppies are born deaf and blind and move in a crawl-like manner. Most of their time is spent sleeping or feeding. Although several primitive sensory and behavioural systems are present at birth, the puppy’s behaviour is largely reflexive and organized to guarantee what it needs for survival at this stage of development, such as food and adequate warmth. Neonatal puppies are incapable of controlling their body temperature internally but keep it constant by staying in close contact with their mother and littermates and they will display intense distress vocalization when separated from them, but will be content and go to sleep without the comfort of contact with them if they are warm.
Although complex learning cannot occur during the initial stage simple conditioning of touch, taste and scent stimulus-response associations are possible from the first day of life. For example, Fox (1971) placed aniseed oil on the mammary glands of a nursing bitch. Puppies exposed to the smell whilst suckling were more attracted to it away from the suckling context than those that had not had the opportunity to develop the association.
Neonatal experiences seem to have considerable effects on the development of behaviour. This appears to have been illustrated in unpublished work by De Witt, which involved half litters of newborn puppies having no direct exposure to humans whilst the remainder received a high level of human scent for half a minute immediately after birth. Subsequently both groups were isolated from human contact until tested, some at five weeks and some at seven weeks. Puppies that had been exposed to human scent had a preference for investigating people over other environmental stimuli. Unfortunately puppies that had no direct human contact showed the same preference, attributable to the fact that they were mixed with littermates from the exposed group that would have been carrying human scent on their coats. However these combined groups showed significantly greater interest in investigating people when compared to a new control group that was kept in total isolation from human scent until three weeks of age. The importance of early handling by the breeder was also shown in a study by Gazzano et al. (2008), which showed that gentle handling on a daily basis during early puppy-hood has a beneficial effect on emotional development.
A synthetic version of a maintenance stimulus called ‘Dog Appeasing Pheromone’ (DAP) is available as ADAPTIL in the form of a plug-in diffuser, useful for creating a feeling of security in the home, a spray and as a collar useful when away from home, e.g. during walks. The appeasing pheromone is produced by the sebaceous glands in an area between the mammary glands of the bitch three to five days after the puppies are born and helps to create relaxation and dependency upon her. It is suggested that the resultant positive emotional state enables the puppy to remain relaxed as it explores its environment and encounters new stimuli in the next stage and that this reassuring property persists into adulthood. The use of a diffuser may provide a puppy with a salient maintenance stimulus when it is moved to its new home.
After the opening of the eyes and around 13 (+3) days and the opening of the ear canal at approximately 18–20 days, a puppy is aware of visual and auditory stimuli. The puppy’s movements become increasingly co-ordinated and it develops the ability to run but without the grace of an adult. The ongoing development of cognition, perception and motor abilities means that puppies experience a rapid increase in stimulation and because complex learning is possible most reflexive behaviour that was displayed automatically without conscious thought is replaced by learnt responses related to environmental stimuli.
During the three to five week period puppies are at an optimum stage of development for establishing a broad maintenance set. This occurs for several reasons. Firstly they are less inclined to stay close to the maintenance stimuli they became dependent on in the initial stage (the dam, littermates etc.). In addition to their new mobility this is because what has been described as the seeking system, within the brain stimulates them to actively search and explore their environment. The second factor is that the brain over produces neurons during early development that will go to waste if they don’t get used. Although new ones are formed during learning in later life the capacity to store knowledge of the world and how to cope with it is more efficient during these important weeks. Through exposure to and interaction with their environment puppies store representations of new stimuli and variations in familiar stimuli. The third factor is that during these weeks puppies are in a biologically pre-programmed period of parasympathetic dominance, characterised by factors associated with relaxation, such as low heart rate predisposing them to have a positive emotional state. While they are in this relaxed frame of mind, puppies easily associate new stimuli with that emotional state of relaxation and they become part of a broader maintenance set.
At the start of the three and five week period, approach and investigative behaviour is directed equally to novel and familiar objects but most attention is paid to stimuli that change rapidly, such as movement and sounds. As recognition and recall memory develops and maintenance sets are refined, attention to familiar things declines. Greater attention is paid to those things that are less familiar. These trigger investigative behaviour, whereas things that are extremely unfamiliar begin to cause some minor hesitation to approach. This can be explained by the fact that when something unfamiliar occurs the puppy’s brain compares it with the representations it has stored. A successful match will result in a positive association and the further development of behavioural organisation. Failure to match during this phase of development will normally result in efforts to investigate the stimulus or event.
Preparedness to respond positively to novel stimuli during this stage was shown in a response test conducted as part of an experiment by Freedman et al. (1961). In this experiment litters of Cocker Spaniel and Beagle puppies were kept with their littermates and dam but isolated from human company except for specific periods. Pups from each litter were taken from the field for a week of socialization at two, three, seven and nine weeks of age and then returned to the field. During this week indoors pups were played with, tested and cared for daily in three half-hour periods. How avoidance behaviour develops was evident in daily 10-minute tests of the amount of time a puppy spent in physical contact with a passive, reclining experimenter. The two-week-olds were too immature to do much but sleep, eat or crawl about randomly. However, the three-week-olds were immediately attracted and spent most of the 10-minute period pawing, mouthing, and biting him and his garments. Five-week-olds exhibited wariness at first, but they became comparable to three-week-olds before the end of the first play period. In contrast seven-week-olds were frightened and wary of contacting the experimenter over the first two days, while nine-week-old pups exhibited these reactions over the first three days. Puppies tested at 14-weeks that did not receive any exposure to people were fearful and remained so even after several weeks of petting.
Experiments have also been designed to reveal a puppy’s response to inanimate objects, for example, puppies housed in conditions devoid of objects were placed in a test area with various articles for just half an hour at five, eight, twelve and sixteen weeks. These puppies were found to increase their exploration as they grew older and developed a preference for more complex things. However, puppies first tested when they were over eight weeks tended to withdraw from the items and those not tested until twelve or sixteen weeks old frequently became catatonic with fear (Fox 1978).
During the three to five week period dependency on maintenance stimuli for emotional homeostasis develops very rapidly and becomes progressively important for behavioural organisation. Search behaviour for missing social or non-social maintenance stimuli starts to appear. Little by little evaluation of contexts also starts to occur. In practice this means that to increase the chance of a puppy accepting unfamiliar stimuli without causing loss of emotional homeostasis novel stimuli should be introduced in a familiar environment so the puppy can rely on its existing maintenance set. It also means that a puppy has to be exposed to a great amount and variety of animate and inanimate stimuli and it will benefit from being regularly moved to locations where unfamiliar types of stimulation and variations of familiar stimuli exist. This is at a time when the puppy is in the care of the breeder and therefore this responsibility falls to them.
After the rapid developmental changes in the brain, nervous system and behaviour in the previous stage, from five to six weeks development continues at a more gradual rate. The ‘natural relaxed frame of mind’ is lost and replaced by a period of high heart rate and sympathetic dominance from week five to a peak at seven/eight weeks followed by gradual decline.
The increasing maturation and integration of various brain structures during the five to seven week period increases the potential for a reaction to novelty. Things the puppy has not had a chance to develop a positive emotional response to now have an increased likelihood of triggering fear, which may be displayed as either avoidance behaviour, fear or fear aggression. An example of this was shown in experiments where puppies exposed to video images between 3 and 5 weeks showed reduced fearfulness in a novel environment in the presence of items similar to those they had seen on the videos when compared to puppies that had not seen the videos (Pluijmakers et al 2010).
Although the puppy has established a broader maintenance set and behavioural organization to the known environment, the composition of stimuli in it can change through the availability and importance of other things it encounters. In general things that are moderately different or unpredictable will still cause exploration and a preference for investigating novel stimuli and locations over those that are familiar continues, so long as contextual factors are reassuring. However, the introduction of novelty becomes more likely to upset than to benefit the system. The amount and nature of previous experience increasingly determines whether the puppy shows fearful responses and the capability to control its environment and thus maintain behavioural organization becomes very important. If a dog does not have a sense of control it may easily learn fears or develop what, from our perspective, may seem to be inappropriate and unpredictable behaviour in response to unfamiliar or aversive stimuli. Once developed these responses may generalise to other things and situations.
During this stage puppies should be given plenty of opportunity and time to become familiar with new things and build up their confidence to approach and investigate them. Giving them the chance to do this at their own pace allows them to control their emotional state, which they can exercise by governing their approach, withdrawal and wait and see responses. If they stay relaxed the stimulus will eventually be associated with a positive experience. Conversely, forcing a puppy to approach will have the opposite effect because a sense of loss of control will cause anxiety or fear, resulting in a negative association.
To maximise the chance of the puppy forming a suitable maintenance set and coping with the world beyond the breeder’s environment puppies should be homed as soon as it is allowed. The younger the puppy the easier it will be for it to add new stimuli it encounters to its maintenance set, which helps to reduce the risk of the development of fear related problems. After the age of 7 to 8 weeks, when the puppy’s representation of the world is, for the most part, formed this becomes increasingly difficult, but definitely not impossible. Obviously, the opposite is true and the later broadening of the maintenance set starts the less likelihood of developing sound temperament there is and starting from scratch at 12 to 14 weeks is likely to present new owners with extreme difficulties. Of course, change is possible but prevention is better than cure. After they are obtained and have received their initial vac cinations the process of exposing puppies to as many different stimuli and environments as possible to build up their confidence should continue. This process has to be repeated until at least six months and probably a year to prevent behavioural organisation regressing.
From 1959 practical application of the research into the effect of early experience was conducted with over 24,000 puppies by Guide Dogs for the Blind Association in the UK. This work is ongoing but was reported on in 1991. The qualities required of a potential guide dog, the training of which starts at around 12 months, include confidence and low reactivity to normal stimuli. Until 1956 the GDBA relied on the donation of adult dogs to maintain their stock and the success rate of those accepted into training and becoming guide dogs fluctuated between nine and eleven percent. In an attempt to improve the success rate puppies were purchased and placed in private homes between ten and twelve weeks of age or even later but it did not significantly improve.
In 1959 the GDBA started managing the gene pool with its own breeding scheme. The puppies were raised in kennels and placed in the urban homes of puppy walkers after first vaccination at six weeks. Systematic exposure to the environment in the area around the puppy walker’s home commenced immediately and continued until the puppies were returned for training. Annual success rates between 75 and 80 percent became common with some variation between breeds.
Dogs that exhibit avoidance, or aggressive behaviour related to fear could be more likely to have a history of limited early experience than dogs displaying other types of behaviour problem. This theory was tested by Appleby, Bradshaw & Casey in 2002 when the early experience of 820 dogs referred by veterinary surgeons to one pet behaviour counsellor (D. Appleby) were compared. The results suggest that there is a relationship between a dog’s early environment and the development of fear-related behaviour problems. Living in a domestic environment at the breeder’s and experience of urban life after vaccination appears to reduce the probability that the dog will develop avoidance behaviour or aggression in response to unfamiliar people. Interestingly, there was a significant relationship between the dogs that had been reared in a non-domestic maternal environment, such as a barn, shed or kennel and aggressive behaviour when examined by the vets in later life. A possible explanation is that for puppies that have not had the diversity of experience available in a domestic environment the first experience of visiting the vet, which normally occurs within two days of being obtained, is likely to be traumatic resulting in an association between the vet and fear and defensive behaviour during later consultations.
Whereas, in this study, homing before 8 weeks appeared to reduce the risk of fear related behaviours in adult dogs whose breeders did not raise them in a domestic environment, a study of adult dogs whose breeders raised them in domestic environments suggests that homing after 8 weeks is associated with higher instances of problematic behaviour towards both familiar and unfamiliar people and unfamiliar dogs. (Appleby et al. 2013). It also showed that homing at 8 weeks is associated with less risk of these adult problem behaviours than homing before 8 weeks.
The importance of exposing puppies to unfamiliar stimuli gradually also applies to teaching them to adapt to changes in their maintenance set when left alone. Elliot and Scott (1961) found that puppies that are not exposed to separation experiences early in life have an extreme reaction to them in later life. They divided some puppies into four groups and exposed them on a weekly basis to separation in a strange pen. They repeated this until the age of 12 weeks. Puppies of group four were not exposed to separation experiences until they were tested for the first time at 12 weeks. These puppies panicked and were unable to cope whereas the other groups, especially the group that started having this experience at three weeks, had learned to adjust more effectively. Care should be taken to develop a puppy’s capacity to cope with segregation gradually. Young puppies have a strong need for close social contact. This need is first satisfied by its mother and littermates and later by its owners. Locking a puppy in a room on its first night in its new home, after its previously established maintenance set has been removed, and letting it cry until it is worn out is not good for its welfare. It could sensitise it so that it reacts negatively when left alone on future occasions, increasing the potential for separation problems such as destructiveness, vocalisations and elimination. New owners can gradually accustom their puppy to being on its own by getting it used to an indoor kennel and placing this next to their bed and gradually moving the kennel away from the bedroom once the puppy has learnt to settle at night or they can sleep near the puppy downstairs for the first few nights, gradually withdrawing their presence once the puppy has adapted to its new environment.
Maturation and integration of structures in the brain makes more detailed information processing possible resulting in changes in behaviour and an increase in emotionality. Once the naturally predisposed period of parasympathetic dominance and positive emotional state has declined and the maintenance set has been formed, unfamiliar stimuli encountered may cause a negative emotional state. The characteristics of these stimuli and the characteristics of the maintenance set will determine the extent to which arousal and disruption of behaviour occurs. The more effective the maintenance set the better able to cope with disruption of emotional homeo stasis the dog will be. The presence of an effective maintenance set also increases the individual’s confidence to explore and broaden it. It follows that a failure to develop an adequate maintenance set during the period of parasympathetic dominance between three to five weeks and beyond should have a detrimental effect on the development of subsequent behaviour the dog’s welfare and there is an increase in the potential for behavioural disorders to develop.