Complexity of Early Environment

An animal’s central nervous system only develops its genetically predetermined functions if exposed to appropriate environmental stimulation, especially early in life. A restricted environment early in life results in an animal with abnormal sensory perception. The animal may not be able to perceive stimuli to which it was not exposed during development. An animal reared in a restrictive environment will also be emotionally unstable. A restricted early environment also may result in reduced learning ability and trainability, thus an interesting, stimulating early environment must be provided. It is also important that the early environment be predictable and consistent. If not, the animal will not only be frustrated and under stress, but it will also learn that its behavior has no impact on what is happening around it. Such animals will be in a state of learned helplessness and are exceedingly hard to train later.

Effect of Neonatal Stress

Some degree of stress (e.g., handling or cold temperature) in a dog’s neonatal period may accelerate growth, reduce emotionality later in life, increase social status, and promote resistance to some diseases. Handling sessions from the first days of a puppy’s life are recommended because they not only expose the puppy to a mild stress but also facilitate socialization when the puppy gets older. In addition to handling sessions, puppies may be removed from the nest (best while someone else walks the mother) and placed singly on a cool vinyl floor for a brief time (30 seconds) before being put back into the warm nest. Flashing lights, noises, and motions have also been used as mild stress. The Army’s super-dog program used slow, refrigerated centrifuges to apply a mild stress. If done in the first few (3) days after birth when the hypothalamic-pituitary-adrenal (HPA) axis develops, the expected result is reduced behavioral and physiologic reaction to chronic stress, an increased physiologic reaction to acute stress, and reduced emotionality of the adult dog. Chronic stress is caused by unavoidable and long-lasting aversive conditions. Since they are unavoidable, the stress reaction does not result in coping and drains the animal’s resources. In humans, such chronic stress causes stomach ulcers and other health impairments. A strong reaction to acute stress, however, is desirable. If an animal is exposed to a sudden, intense, and potentially damaging stimulus, it may save its life to mobilize all its resources to escape. Thus a reduced reaction to chronic stress and an increased reaction to acute stress are both beneficial.

Mild early stress also results in increased resistance to some diseases, a more stable and less emotional temperament, and increased learning ability and trainability.

Sensitive Periods of Development

It is well documented that there are “sensitive periods” in the behavioral development of the dog. These are periods of development during which certain experiences are needed to achieve normal development. Lack of these experiences during these sensitive periods may have lifelong irreversible effects. For example, between 4 and 12 weeks of age, a puppy learns how a social partner looks. During this time, the brain develops a sort of filter system in the visual cortex, which becomes sensitized to the shapes of the social partners of the puppy. In the wolf, these would be adult wolves and other pups; in the dog, they include humans and other pets. This filter system ensures that certain neurons in the visual brain are only activated when the puppy sees a social partner. After 12 weeks, it is difficult to further modify this system so that the puppy will not learn (or only learn with difficulty) to accept previously unknown species as social partners.

The recognition of critical periods in canine behavioral development may be one of the most important discoveries about dogs. By controlling the puppy’s environment during its early life, we can influence the emotionality, temperament, sociability, confidence, and learning ability of the dog. Early and appropriate intervention can result in the dog being more adaptable, easier to train, and physically and emotionally healthier.

The exact time course of development varies between authors (and probably between dogs to some degree!), since the sensitive periods do not start and end abruptly, but rather, they phase in and out gradually. The development of puppies has been divided into the periods seen in Table 13-1.

TABLE 13-1 Periods of development in puppies

Period	Age
Fetal period	up to birth
Neonatal period	0 days to 10 days
Transition period	11 days to 21 days
Socialization period	3 to 12 (or 14) weeks
Fear period	Around 8 to 10 weeks
Juvenile period	3 months to puberty
Second fear period(s)?	3 weeks duration between 4 and 11 months?
Adolescent period	Puberty to social maturity

Fetal Period (Up to Birth)

Shortly before parturition, the male fetus produces a burst of testosterone, which has an organizational effect on the brain of the male fetus: it masculinizes and defeminizes the brain (Box 13-1). Masculinization results in the organization of typical male behavior such as roaming, urine marking, inter-male aggression, and male sexual behavior. Castration is usually successful in reducing these behaviors but does not entirely eliminate them. The effectiveness of castration in altering these behaviors is individually very variable. Defeminization results in the destruction of the mechanism that results in cyclical sexual behavior in females (intact male dogs do not have an estrus cycle and are always ready to breed) and eliminates the predisposition to show female sexual behavior. A male dog castrated after birth when given estrogen will show male and not female sexual and social behavior.

BOX 13-1 Fetal period: up to birth

During the fetal period, the male brain is defeminized and masculinized. This process determines gender differences in behavior.

The priming of the fetal male brain is irreversible and affects all behavior that is gender-dimorphic, including various types of aggression, even in the castrated dog. Therefore a castrated male dog is still very much male; a spayed female dog is still very much female.

Neonatal Period (0 Days to 10 Days)

A puppy is born both blind and deaf but is capable of whining to attract attention from its mother (Box 13-2). It is born with the senses of balance, taste, smell, touch, and temperature. Until 3 weeks of age, the puppy is not able to urinate and defecate spontaneously and depends on stimulation (licking) by the mother to fulfill these functions. Its nervous system is poorly developed: for the first 3 days of age it has “flexor dominance” (i.e., it curls up when you pick it up by the head) and from day 4 to day 21, it has “extensor dominance” (i.e., it stretches when you pick it up). Although puppies depend on the mother for thermoregulation, they are born with a sense of temperature and will root against a warm object. Newborn puppies will also move against the grain of the hair of their mother so they will get closer to the udder and also turn or move toward the side they are touched on. From about 2 to 3 days of age, a puppy is able to crawl by throwing its head from side to side, using its nose as a sensory touch and temperature probe. All of the puppy’s behaviors are designed to get it back into the heap of littermates and to the udder.

BOX 13-2 Neonatal period: days 0 to 10

The puppy is blind and deaf and completely dependent on mother for thermoregulation, food, and elimination.

The senses of balance, touch, smell, and taste and sensitivity to temperature are already developed.

Mild stress of the neonatal dog, such as induced by handling or placing the puppy on a cool surface, increases the puppy’s ability to cope with stress later in life.

Already during this early stage, human contact and handling are important as environmental enrichment and for inducing a mild stress. As mentioned, a mild stress can also be imposed by removing the puppy from the nest for a brief period (30 seconds) and placing it on a cool surface such as a vinyl floor. This may allow the animal to better cope with stress, be more trainable, and be more emotionally stable later in life.

Puppies may vocalize when hurt, cold, or uncomfortable or when they lose contact with the littermates or the mother. However, most bitches will not react to these vocalizations. Learning with positive reinforcement is already possible, although the puppies’ responses are very limited. Conditioned aversion has also been achieved in very young puppies.

Transition Period (11 Days to 21 Days)

Puppies are born in a very early stage of development. Such animals are called “altricial.” In the transitional period, a puppy catches up with those animals that are born in a much more developed state, such as foals or calves, which are examples of “precocial” animals. The puppy begins to develop its senses, gains control over thermoregulation, and at the end of the transitional period, becomes able to eliminate spontaneously (and the mother stops eating its stool) (Box 13-3). From this point on, the puppies should have the possibility to leave the nest site to eliminate. Puppies thwarted from doing so may become almost impossible to house train.

BOX 13-3 Transition period: days 11 to 21

During this time, the puppy begins to develop its senses of vision and of hearing. Therefore a complex environment should be provided to allow optimal development of the nervous system. From 3 weeks on, the puppy can already be desensitized to potentially frightening sights and sounds.

The development of vision and hearing makes the puppy more reactive to environmental stimuli. Since the puppy is also able to habituate to stimuli and still profits from environmental complexity for normal neurological development, the provision of sensory, visual, and auditory stimuli is very important. This can be done through handling; placing the puppies for short periods into a playpen with toys, platforms, tunnels, and so on (under supervision!); and playing commercially available recordings of various noises. Puppies will also begin to play-fight and are better able to learn, especially with positive reinforcement.

At around 3 weeks of age, the mother and/or father may start to regurgitate food for the puppies. However, probably as a result of domestication, not all dogs will do that. The puppies will solicit food regurgitation by pushing their noses into the corners of the parents’ mouths, a behavior that later develops into appeasement behavior. At this time, it is appropriate to begin feeding solid food to puppies.

Socialization Period (4 to 12 or 14 Weeks)

The socialization period has been subdivided into a period of primary socialization, normally to conspecifics (earlier on in the socialization period), and secondary socialization to other species (later in the socialization period) (Box 13-4). Social play is the most prominent behavioral aspect of this period. During the primary socialization period, a puppy learns to interact appropriately with other puppies, to read canine body language, about bite inhibition, and to fit into a social group. During secondary socialization, the puppy learns to predict actions of members of other species and to interact with them successfully.

BOX 13-4 Socialization period: weeks 4 to 12 or 14

Socialization to dogs and to people has to occur during this time. If this opportunity is missed, the puppy will most likely always be fearful of dogs and/or humans.

During the socialization period, the puppy should also be exposed to all situations that it is likely to encounter during its life. The best prevention of behavior problems is to take the puppy to puppy classes during that time.

During the socialization period, the puppy can already learn some commands. It should learn a biting inhibition and start to learn to fit into a social group.

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