Dogs and cats show large individual differences in their response to stress, and these are partly related to early-life environment. Early development of dogs and cats include four phases: prenatal, neonatal, transition, and socialization. During these phases, the handling of puppies or kittens and the characteristics of the environment in which they live have a very pronounced and long-lasting effect on their behavior. Consequently, an incorrect handling of puppies and kittens could lead to behavioral problems with poor prognosis. The most common behavioral problems associated to inadequate management early in life include the inability to cope with stressful situations, poor social skills, fear-related problems, aggressive behavior, and house-soiling problems.^1,2

Research done in a variety of species has shown that animals born to mothers that have suffered stress during pregnancy are likely to be more easily stressed as adults.³ Other changes in the offspring due to stress of the dam during pregnancy are increased serum testosterone, decreased serotonin concentration, and changes in sexual behavior.⁴ Therefore, providing a non-stressful environment for the dam is important, and this would require, among other things, adequate feeding, thermal comfort, and a dry and clean resting area.

During the first fifteen days after birth (neonatal period), kittens and puppies are blind and deaf, and therefore their sensory world is very limited. Tactile stimuli play a very important role in this phase for at least two reasons. First, as the sense of touch is already functional immediately after birth (and even before), it provides an essential mechanism of interaction between the animal and its environment. Second, the development of the skin and skin receptors (including tactile receptors) is closely related to the development of the central nervous system (CNS). It is well known that adequate tactile stimulation during this period results in animals being more able to adjust the intensity of their stress response to the relevance of the stressor. This adequate tactile stimulation is usually provided by the dam when licking the pup. However, when the mother shows poor maternal behavior or in the case of orphan puppies or kittens, it is important to provide additional tactile stimulation during the neonatal period. It has been suggested that 5 minutes per day of gentle strokes⁵ would be adequate. The effect of neonatal stimulation on the stress response is caused by molecular and cellular changes in the CNS. In particular, tactile stimuli during the neonatal period result in an increased concentration of glucocorticoid receptors in the frontal cortex and the hippocampus. This, in turn, increases the negative feedback of glucocorticoids on the stress response.

The importance of the socialization period cannot be overemphasized, and it is now widely accepted that dogs and cats should be exposed during this period to conspecifics, adult humans, infants, and any stimuli that they are likely to encounter later on in life. Two additional facts should be highlighted in this respect. First, exposing puppies and kittens to many different stimuli early in life not only reduces their fear of those particular stimuli, but also their general fearfulness. Second, most of the vaccination plans end at 3 months of age. As the socialization period of dogs also ends at roughly 3 months of age, it is important that, in order to minimize the risk of infectious diseases, stimuli are presented to the animal in a safe environment. Puppy socialization classes, where stimuli are presented in a controlled manner and in a clean environment, reduce the likelihood of behavioral problems later on in life.

Weaning age has a long-lasting effect on behavior, and research has shown that early weaning may result in lower tolerance to frustration. Frustration has a key role in the development of behavioral problems, especially aggression-related behaviors and compulsive disorders. From a practical viewpoint, frustration can be prevented through three strategies. First, the interaction between the mother and its offspring, particularly at weaning, results in the offspring becoming more tolerant to frustration. Then, if at all possible, it is important that puppies and kittens are not removed from their mothers before the natural weaning process has taken place. Second, it is very important to advise the owner to interact with the dog or cat by following consistent and predictable rules, as lack of predictability has been identified as a major source of stress. Third, the frustration threshold can be increased using basic learning methods (such as classical and operant conditioning), even when the animal is adult.

The stress response is triggered when animals are unable to predict and control their environment.⁶ Setting consistent rules, so that the expectations of the animals are met, increases the predictability of their environment.^7,8 This includes having routines in the dog or cat daily activity and interaction with the owner and, secondly, using rewards in a consistent manner. For example, playtime can be signalled to the animals by showing a cue immediately before the activity will start. When doing so, it is important to avoid an excessive time lapse between the signalling cue and the actual start of the activity, as otherwise frustration may occur. A very important aspect is that all family members should be encouraged to use rewards as consistently as possible. Indeed, oftentimes given behavior is encouraged by a member of the family and punished by others. This management inconsistency may lead to frustration and should therefore be avoided, as frustration is one of the most important causes of behavioral problems in dogs and cats.

Several studies have shown that environmental enrichment reduces stress. One of the main goals of environmental enrichment is to allow animals to express their natural behavior, or at least parts of it. When planning an environmental enrichment program, the behavioral biology of the species has to be taken into account. In particular, it is important to know the behaviors that have a strong motivation or that contribute to positive emotional states, as they should be encouraged. Providing a safe area is another goal of the enrichment programs.

In cats, enriched environments should include a sufficient number of adequate resting and hiding places, water bowls, and litter trays. Additionally, toys that trigger hunting behavior can also be used. It has been suggested that, when doing so, it is convenient that the cat can end up catching the "prey" in order to avoid frustration. A safe area allows cats to control or avoid stressful events.

In dogs, environmental enrichment should mainly consider three different aspects. First, it is essential to provide enough positive social contact with other dogs or with humans. Second, it is also important to use environmental enrichment items that stimulate exploratory and foraging behavior, as well as cognitive skills. Finally, providing a safe area, as in cats, may also be useful.

References

1.  Arai S, Ohtani N, Ohta M. Importance of bringing dogs in contact with children during their socialization period for better behavior. J Vet Med Sci. 2011;73(6):747–752.

2.  Boxall J, Heath S, Bate S, Brautigam J. Modern concepts of socialisation for dogs: implications for their behaviour, welfare and use in scientific procedures Altern Lab Anim. 2004;32 Suppl 2:81–93.

3.  Dickerson PA, Lally BE, Gunnel E, Birkle DL, Salm AK. Early emergence of increased fearful behavior in prenatally stressed rats. Physiol Behav. 2005;86(4):586–593.

4.  Kaiser S, Sachser N. Social stress during pregnancy and lactation affects in guinea pigs the male offsprings' endocrine status and infantilizes their behaviour. Psychoneuroendocrinology. 2001;26:503–519.

5.  Gazzano A, Mariti C, Notari L, Sighieri C, McBride EA. Effects of early gentling and early environment on emotional development of puppies. Appl Anim Behav Sci. 2008;110(3):294–304.

6.  Weiss JM. Somatic effects of predictable and unpredictable shock. Psychosom Med. 1970;32:397–408.

7.  Fontayne R, Vervliet B, Hermans D, Baeyens F, Vansteenwegen D. Reducing chronic anxiety by making the threatening event predictable: an experimental approach. Behav Res Ther. 2009;47:830–839.

8.  Grillon C, Baas JP, Lissek S, Smith K, Milstein J. Anxious responses to predictable and unpredictable aversive events. Behav Neurosci. 2004;118(5):916–924.