An introduction to developmental problems in puppy hood

Breed effects

Selective breeding has resulted in genotypic differences and phenotypic differences that have produced an array of breed differences within the single species Canis familiaris.

Although originally intended to enable the selection of dogs with specific abilities such as hunting and herding, most differences also show themselves in anatomical traits affecting ears, tails and noses. These anatomical changes have not altered behaviours associated with self preservation or sexual behaviour, which remain common to all breeds (Lindsay, 2000), but some traits have resulted in anatomical changes that make canine communication and signalling difficult for both canines and humans to read. The positions of ears and the facial expression of dogs are particularly important in signalling the progression of emotional changes. The position of the tail is also indicative of emotional state. The effectiveness of such communication tools can be compromised by breed characteristics such as ears that are incapable of standing erect, brachycephalic conformations that reveal teeth, hair that covers eyes, tails that are constantly held erect, piloerection along the backbone.

Brain receptor sensitivity

Both genetics and inheritance affect brain receptor sensitivity, and traits such as fearfulness and anxiety may be partially inherited (Mills, 2005). Differences in emotional thresholds can be affected by a limbic/autonomic inheritance present at birth (Lindsay, 2000), and the dog's general emotional reactivity or threshold to stimulation will be a pre-disposing factor towards the development of behaviour problems. Many studies have shown emotional extremes involving anxiety and fear are highly hereditable (Thorne, 1944), and such dogs are much more sensitive to environmental stimulation and this sensitivity can be difficult to alter despite the influence of learning in later life.

Breed and behaviour

Breed standards have developed that not only specify the type of work that the dog should be able to perform, but also desired behavioural traits such as ‘wary’, ‘cautious’ or ‘reserved’. Strong genetic links to emotionality leading to behaviour problems have been demonstrated in specific lines of certain breeds of dogs (Podeberscek and Serpell, 1996 and 1997) and to the symptoms of anxiety and fear (Scott and Fuller, 1960; Scherrer et al, 2000).

Inherited temperament traits influence the way dogs learn and how they are most effectively trained, and various behavioural profiles have been prepared to assist potential dog owners in selecting a breed that is compatible with their lifestyle (e.g. Scott and Fuller, 1965 and Hart and Hart, 1985); the Waltham Centre for Pet Nutrition has a counselling service assisting potential owners in finding the ideal companion. All of these scientific and applied activities are based on the assumption that a considerable portion of a dog's behaviour is affected by inherited tendencies and traits.

Breed effects relating to species-specific responses

Although not completely reliable due to the potential for individual variation in the species-specific response following from opportunities to learn about the result of responses, breeding is likely to dictate the initial expression of a dog's species-specific response. In the presence of a fear-inducing stimulus and with sufficient behavioural freedom to do so, dogs of most breeds would respond by fleeing from the stimulus. However this is not the case for all breeds. The development of specific breeds for specific purposes may have interfered with the species-specific response, as is the case with terrier breeds that have been specifically bred to initiate aggression on threat, and with the beagle that is unusual in its tendency to freeze when threatened (Scott and Fuller, 1965). This genetic pre-disposition to express a specific response when faced with challenging situations can make it extremely difficult for a dog (e.g. terrier) to respond in a manner that the general public may consider socially appropriate.

Stimuli that may induce emotions such as fear or anxiety in the dog

As already alluded to, anxious or fearful responses are not always learned or acquired through experience. Fear is often evoked by unconditioned aversive stimuli that have evolutionary significance, known as innate fear stimuli. Different species show biological preparedness to different sets of such stimuli. For dogs, innate fear stimuli include pain, rapid stimulus change, loud noises and other intense sensory stimulation, sudden movements, heights, isolation, fire, water, and unfamiliar environmental and social situations (i.e. novel environmental or social stimuli such as unknown people). This latter trigger may appear incongruous for a social species but there is a tendency to forget that within a ‘natural’ dog group the social composition would remain fairly constant throughout an individual dog's life.

Natural triggers of fear are associated with imminent threat and evoke preparatory physiological arousal mediating species-specific escape responses.

Inter-uterine influences on puppy behaviour

Sex hormones

At the stage of foetal development when the central nervous system is most sensitive to androgens, testo-sterone is only produced by male foetuses and causes masculinisation of their brains. It has been found that in litter-bearing species, such as the dog, some female foetuses may become exposed to testosterone, particularly if the foetus lies between two males in the uterine horn. Testosterone may diffuse through the amniotic membranes or enter the foetal blood circulation (vom Saal, 1989) causing similar developmental changes in the female brain as those occurring in the surrounding males. These masculinised or androgenised females may show more male-like behaviour than non-masculinised females, including an increased tendency to exhibit aggression (Beach, 1974; Brain and Haug, 1992; Overall, 1995), also leg-lifting to urinate. Foetal androgenisation may increase the incidence in the development of resource-based aggression in bitches after spaying (Voith and Borchelt, 1982; Warnes, 2005) once the ameliorating effects of oestrogen and progesterone are reduced. There may be a gradation of masculinisation depending on the level of exposure to testosterone (Overall, 1995)

It has also been suggested that male puppies, positioned in utero between other male puppies, may be exposed to increased levels of testosterone that enhance the development of primary sexually dimorphic behaviours such as rough play and increased activity. Punishment of such seemingly excessive behavioural displays may lead to owners inadvertently initiating a motivation for defensive behaviour in the young dog, leading to unintended learned associations.

Postnatal changes

The dam and nest

There are some anecdotal reports that the mother may play an important role in the regulation of aggressive behaviour through the exercise of early discipline (Lindsay, 2000). It is also widely accepted that modelling and observational learning occurs so that the mother's emotional tone and reactivity may encourage similar reactions in puppies. The mother's negative reactions to social contacts or events may be the result of heredity, her own personal history, or a combination of both and impressionable puppies are at considerable risk of internalising her attitude during the socialisation period as well as before birth (Thompson, 1957). It is a common belief (Lindsay, 2000) that puppies reflect more of the mother's emotionality than the father's and prenatal and postnatal influences probably exert a more significant influence than sex-linkage in these apparent differences.

The influence of the dam's emotionality, both during and post pregnancy, on the developing emotional baseline of the puppies enhances the necessity for breeders (both professional and hobbyists) to ensure that potential mothers are capable of coping with potential emotionally arousing circumstances and that their environment is managed to reduce potential stressors. The stability of the social environment in which pregnant females live is critical for their offsprings' social behaviour later in life (Kaiser and Sacher, 2005).

The nest environment is in itself important to the emotional development of the puppy. Environments that are lacking in resources such as toys can have a two-fold negative effect on the puppies' developing behavioural repertoire. Barren nest sites enhance the salience of the mother as she is the only stimulus, social or otherwise, within the environment (Figure 2). This can lead to puppies finding it extremely difficult to cope with the environmental and social changes that occur as they enter their new home, enhancing the likelihood of distress, associated learning and separation problems. Barren early environments also pre-dispose puppies to competitive and resource holding behaviours, as if insufficient in number, those distracting items that are placed in the nest area become a focus for competitive behaviours rather than enhancing appropriate social behaviour including shared social play.

Distress and impulsivity

Some external influences may have long-term effects on learning, emotionality and general adaptability despite the neonatal state of the puppy (between birth and 12 days). Early neonatal handling for as little as 3 minutes per day and exposure to mild environmental stressors such as slight changes in ambient temperature and gentle movement may have positive effects on a puppy's later emotional reactivity and mature learning and problem solving abilities (Morton, 1968). Animals left undisturbed during neonatal development have been found to be consistently more emotionally reactive as adults (Danenberg, 1964).

Perinatal brain plasticity increases the vulnerability to early adverse experiences, thus leading to abnormal development and behaviour (Anand and Scalzo, 2000). These changes may promote anxiety, altered pain sensitivity, stress disorders, hyperactivity/attention deficit disorder and are likely to lead to impaired social skills. Studies such as those undertaken in altricial species by de Kloet et al (2005) suggest that adverse conditions during early life are a risk factor for stress-related diseases (Figure 3) such as depression and post-traumatic stress disorder, and that adverse early experiences trigger immediate changes in the stress system that may permanently alter the brain and behaviour.

Socialisation

The development of a dog's social behaviour unfolds according to a genetically programmed timetable (Scott and Fuller, 1965) and this developmental process has a permanent influence on the behavioural adjustment of the dog (Lindsay, 2000). During the brief period between 3 to between 12 and 16 weeks (depending on breed) the average puppy will learn more than during the remaining course of its life, forming a lasting emotional and cognitive scheme of the social and physical environment. These early experiences produce the range of how and what the dog is prepared to experience and learn in the future.

Much of what is learned during this early period is lasting, providing the foundation for adult behaviour patterns and problems (Fox, 1969) including aversions, social affinities, patterns of active and passive agonistic behaviour, reactions to separation and other emotionally provocative situations, approach-avoidance patterns, patterns of exploratory behaviour and functional fear and avoidance responses — all of which have direct relevance to the development of the dog's behavioural repertoire, including the use of aggression.

A common source of anxiety, fearfulness and aggression is a lack of adequate socialisation and social referencing to the complexities of the social mix and diversity of stimuli in the environment in which the adult dog will have to live (McCune et al, 1995). Domesticity demands that the dog must display considerable social flexibility and the opportunity to learn about this generally occurs at 7 weeks plus as the puppy enters its new home. However, observation of livestock guarding dogs and their ability to form strong inter-specific relationships with species on which a less socialised dog would predate (Coppinger, 2002) and research on sensitive periods in behavioural development (Pluijmakers et al, 2003) would suggest that the learning that occurs between 3-6 weeks is essential if the dog is to become socially competent with a species other than its own. It may also be best to initiate environmental referencing during this period when puppies are more outgoing and less fearful than older puppies.

Social and environmental referencing

Between the ages of 3 and 16 weeks, access to an environment that is rich and diverse is essential for future emotional stability (Thompson and Heron, 1954). Although it is hoped that the breeding environment provides puppies with opportunities for exploratory behaviour they must also be exposed to the environment within which they will spend most of their life; this includes exposure to traffic and the sound of domestic appliances and routines.

Careful environmental exposure carried out systematically through gradual and incremental increases in intensity and duration, allows a puppy to habituate to potentially fear-eliciting stimuli. Classical conditioning, using an appetitive unconditioned stimulus associated with neutral stimuli such as being handled or placed on tables, can further enhance the animal's resistance to developing fear responses later in life.

Dishabituation

Social and environmental referencing occurs through a process of learning known as habituation. During habituation an animal learns to accept environmental and social stimuli that are found within the environment and the process will occur naturally on gentle exposure to stimuli that do not become associated with emotional arousal. As the puppy is more likely to be in a para-sympathetic state prior to 6 to 8 weeks of age, this process occurs most easily at this time.

However despite exposure to a wide range of social and environmental stimuli associated with the domestic environment, puppies that fail to continue experiencing regular exposure to such stimuli may become dishabituated and respond on subsequent exposure as though habituation had never occurred. The process of dishabituation is further enhanced by concurrent emotions of anxiety or fear. Consequently puppies that experience periods of environmental or social isolation on rehoming in combination with stress, e.g. if they are unable to continue exposure to the environment due to illness or kennelling, are particularly susceptible to dishabituation (Sherman and Mills, 2008).

Maturation and hormonal effects

Increased competitiveness and aggression is often associated with the hormonal changes occurring at puberty and these may lower the threshold for frustration and consequently for aggression, particularly for sex-related behaviour patterns such as aggression towards other dogs. It is interesting to note that as oestrus is approached, circulating testosterone in female dogs reaches plasma levels comparable to those in male dogs (Olson et al, 1984). Despite their recognised role in regulating the expression of intraspecific aggression, there is as yet no reliable research to implicate the direct role of sexual hormones in aggression towards humans or other species, with the possible exception of testosterone which has been frequently quoted as an aggression facilitating hormone (Lindsay, 2001). Although the general ineffectiveness of castration of male dogs in controlling aggressive behaviour may put this opinion in question. Behaviours associated with maintaining access to and control over resources may also increase as the young dog approaches sexual maturity (Overall, 1995, 1997, and 2003a and b).

Learning

Controlled studies (Scott and Fuller, 1965) show that puppies between the ages of 3 to 16 weeks are able learners and at no other time in the dog's life will it be more receptive to training, functioning at a nearly adult level in terms of learning ability. But although the puppy's ability to concentrate on tasks continues to increase, by 16 weeks the ease with which they learn begins to decline. This is probably due to previous learning beginning to interfere with new learning. This further emphasises the importance of the nature and quality of the puppy's early experience of its social and physical environment if aggressive behaviour is to be avoided.

Survival depends on an animal learning from past experiences, adjusting its behaviour appropriately to current circumstances, and forming reliable predictions about similar situations in the future. Consequently, learning has an important role in the development of anxieties and fears. There is a temptation to consider behaviour as either innate or learned; however, learning cooperates with innate mechanisms to ensure that organisms are well adapted to the environment in which they must survive.

Classical conditioning and chaining

Anxiety and fear are learned through classical conditioning. Learning that is classically conditioned involves an involuntary or reflex response and it does not rely on the presence of external reward. An example within the veterinary practice would be where a dog has learned to become fearful (unconditioned response) when given pain through being injected (unconditional stimulus). The sound of a syringe or needle packet being opened may become the conditioned stimulus (CS), leading to signs of fear before the injection is given. As learning is intended to maintain the safety of the individual, the animal will quickly chain events backwards from the original CS to other preceding, predictive stimuli to which the animal may also show the conditioned response of fear. In this case the chain could begin with a drawer opening, but on the next occasion when being placed on the examination table, then the dog may show signs of fear towards a person in a white coat in the examination room. This may then generalise to anyone in a white coat and even to anyone wearing white.

If the original stimuli are sufficiently salient or if the animal is already in a state of emotional arousal or anxiety before the presentation of the stimuli, classical associations may be learned in a single exposure (Lindsay, 2000).

Training

Most of what a dog does can be interpreted in terms of innate behavioural predispositions manifested under the influence of learning (Lindsay, 2000). As long as the dog exhibits sufficient variability and flexibility in its innately prepared and instinctive behaviour, that behaviour can be modified through training.

The success of training is likely to be dependent on the dog's previous learning opportunities, the motivation to perform the new skills in preference to previous responses (which may be coping strategies that the dog considers to be necessary within the circumstances), the method of training used and the context in which the trained behaviour is requested. Training may not automatically control a dog's behaviour in a specific context until the dog has had opportunities to become competent in performing the behaviour, to discriminate the cue from background stimuli, by generalising the behaviour to a variety of contexts, including within that specific environment.

Frustration

Frustration, or failure to gain access to the expected reward, is a common factor in mammalian emotions and frequently results in distress.

Many behaviourists believe that hand-reared puppies are particularly prone to this problem due to a failure to go through a normal weaning process that involves the puppies learning that the immediate satiation of a need for resources is not guaranteed. However, puppies do not have to be hand reared to miss this stage in their social learning — puppies that go straight from feeding on their mother to semi-solid food (possibly supplemented with occasional opportunities for suckling) effectively fail to experience periods of having to ‘do without’.

Some puppies enter their new home without experiencing a previous need to engage enhanced emotional activity in response to a delayed response to their perception of their needs (frustration). Initially many owners will pander to the puppy's every need, but they eventually fail to be present at the initiation of ‘need’, inadvertently initiating incidents of frustration.

At such times, frustration bursts of puppy activity aimed at gaining access to a resource that is perceived to be required to satiate the puppy's ‘need’ will be initiated. If owners comply with the puppy's requirements the behaviours associated with the frustration burst will be reinforced for future use. If owners fail to comply, the associated distress my result in an escalation of behaviour and possibly aggression. As with all aggressive incidents in puppies, the manner in which the owner handles such outbursts may have a permanent effect on pet-owner relationships and any attempt by owners to use aversive control techniques will merely enhance the puppy's perception of threat and the need for defensive behaviour (Arhanta et al, 2010).

Fear, anxiety and the environment

Both fear (a stress initiating negative emotional response to a specific stimulus) and anxiety (a stress initiating emotional response associated with an anticipatory state) produce a need within the individual to create an area of safety around it (Appleby, 1997). A fearful or anxious dog will signal that it is uncomfortable with the proximity of a stimulus by initially barking and if this is not successful by growling and eventually biting. A failure to reduce the degree of stimulation will escalate the signalling and possibly teach the dog that the initial stages of this sequence are pointless as only snapping or biting actually achieves the dog's intended result of removing the problem stimulus (Askew, 1996).

The interaction between emotional responses such as fear and anxiety and the resulting behaviour is influenced by:

For each individual the breed, sex, age, experience during sensitive periods for learning, previous learning experiences, physical and social contexts in which the behaviour occurs, opportunities for generalisation and reinforcement and the consequence of the behaviour for the individual will all play a role in the development of fear or anxiety.

Anxiety, fear and separation problems

Fone and Porkess (2008) suggested that exposing mammals to early-life adverse events, including maternal separation or social isolation, profoundly affects brain development and adult behaviour. In addition, anxiety and fear may enhance the salience of the presence of an attachment figure, as puppies find that ‘coping’ is easier at such times. As a con-sequence, adverse events not only enhance fear and anxiety in an increasing array of situations, but they also predispose the young dog to distress and to separation-related problems (Appleby and Pluijmakers, 2004).

Distress and impulsivity

Impulsivity is a common factor in puppy behaviour — the inability to understand the likely outcome of behaviours — a particular problem when puppies have not yet learned the capacity for self control. However, not all puppies learn to control their excessive out-bursts of behaviour and impulsivity in adult dogs may result from brain changes that occur early in life as a result of early stress.

Human psychiatric studies show that early abusive experiences can create brain changes resulting in the impulsivity associated with adult psychiatric conditions. These patients cannot be cured, but they can be helped to manage these behaviours — to identify triggers and to avoid them. However, it is impossible to create such learning in a non-human animal. You cannot teach a dog to stop being impulsive; it is the responsibility of the owner to recognise trigger factors and environments and to manage them appropriately so that the dog does not experience the need to engage in impulsivity.