SENSORY, EMOTIONAL, AND SOCIAL  DEVELOPMENT OF THE  YOUNG DOG                                             By Dr. Joël Dehasse, Behaviorist Veterinarian                                                          Version 1.1 - 6 Feb.97                            Dr. Joël Dehasse 3 ave du Cosmonaute 1150 Brussels - Belgium
This article has been published extensively, with images and charts, in The Bulletin for Veterinary Clinical Ethology, Vol.2, n°1-2, pp 6-29, 1994 (Brussels). In our Western culture, the relation between humans and dogs is played out in a historical and socio-economic context that fosters the emergence of behavioral dysfunctions in animals (the discrepancy between the imagined dog and reality). Many behavioral problems in dogs arise from a failure to recognize social and environmental constraints during their growth. In this article we shall briefly trace these phases of a dog's social and behavioral ontogeny and epigenesis. We shall also point out the risk factors that can undermine the harmonious interaction between humans and their dogs.
                               THE MAIN PHASES IN NEUROLOGICAL DEVELOPMENT Like humans, dogs belong to a species that matures slowly after birth: the new-born is not completely developed and is incapable of surviving on its own. This implies a structured and caring parental environment (caring for the young), reflexes that orient the young puppy to its parents, and the existence of optimal, even crucial, periods in the development of the animal's nervous system. The growth of the nervous system underlies behavioral epigenesis. The immaturity of the nervous system at birth is obvious: Cragg (1975) calculated that in cats the number of synapses per cortical neuron grows from a few hundred to nearly 12,000 in the 10th to 35th day after birth (in Changeux, 1983). Various measurements (volume, weight, percentage of dry matter, oxygen consumption) of the brain show that growth is rapid until the 6-7th week when development suddenly slackens considerably. The number of brain cells and their myelination reaches full adult maturity at 4 weeks. It is worth mentioning that the brain is totally unmyelinated at birth, except for the trigeminal nerve and the non-acoustic part of the auditory nerve which correspond to the new-born's orientation reflexes (Herman 1958, in Scott & Fuller 1965). The motor cortex is the more developed at birth. The occipital cortex, however, then grows more rapidly than the motor and frontal lobes; it also contains several immature neuroblasts that reach full development only around 3 weeks of age (Fox, 1965). Behavioural epigenesis (ethogenesis) is linked to the way neuronal connections are organised (theory of selective stabilization). The development of the neuronal networks is a characteristic process: "the phase of synaptic redundancy followed by a phase of regression in the axonal and dendritic branches is a critical period of development... The redundancy is temporary. Active nerve endings are eliminated all the while the nervous system itself is expanding... This neuronal hecatomb is part of the normal development. ... The hypothesis that spontaneous, and later evoked, nervous activity contributes to the development of neural networks and synapses appears to be plausible" (Changeux, 1983). Behavioural epigenesis is influenced by environmental factors, by the surroundings. Activity regulates neuronal development. In a now classic experiment (by Weisel and Hubel from 1963, in Changeux 1983) with monkeys, noticeable visual defects were caused when one eye was sewn shut during the first six weeks of life; the problems were reversible if the eye was re-opened after three weeks' time. The same experiment on adult monkeys showed no effect on vision. Similar experiments on cats show there is a sensitive period for visual development between 3 and 7 weeks of age, and incapacity to recover vision after three months (Weisel and Hubel, in Vastrade, 1987). "There is a critical period during which the abnormal functioning of a system causes irreversible lesions." (Changeux, 1983). According to Klosovskii (1963), puppies and kittens that undergo periods of forced rotation for several days have vestibular neurons that are larger than those of animals that have not received this stimulus (in Fox: 1965). *In rodents, postnatal temporary occlusion of the ears leads to subsequent difficulties to locate sounds in space and to reduction of discrimination of auditive patterns (Caston: 1993). In rodents always, precocious exposition to other species odors eases future interspecific socialization (decrease in aggressions, lowering of corticosteroïds hormones) (Caston: 1993). * This reflects Cyrulnik's (1991) remarks that the brain becomes atrophied when [an animal] is raised in sensorial isolation, and it develops more than average in an environment of hyperstimulation in noise, affectivity, odors, tastes, sight, etc.... Neurobiological studies have showed that prolonged precocious isolation was responsible for long-lasting structural or functional cerebral modifications. Isolation leads to a diminution of the dendritic network in the monkey frontal cortex; it also induces a reversible diminution of the activity of the mesocorticofrontal dopaminergic pathways (with hyperreactivity to stress), associated with a slight increase of the activity of the mesolimbic and nigrostriatal dopaminergic pathways (Verdoux and Bourgeois: 1991). Development thus seems to come about in stages; although these stages are possibly nothing more than a "simplified classification system where the classifier traces a straight line through a continuum" (Bateson, 1981). Pampiglione (1963) observed marked changes in EEG patterns at 7-8 days, 5-6 weeks (reaching adult levels), and 4-5 months (Fox, 1965). According to Charles and Fuller (1956) (in Scott and Fuller: 1965) the alpha rhythm that appears at 21 days signals an activation of the sense of sight. Scott (1958, 1962) (in Scott and Fuller: 1965, and Fox: 1965) speaks of several stages of neurological, reflexive and behavioral development that are particularly didactic: neonatal (0-14 days), transitional (14-21 days, starting when the eyes open and ending when the animal starts on hearing a noise), socialization (21-70 days) and juvenile (70 days and older). These periods overlap considerably. Since these stages are still used in the literature, they are worth mentioning. We recommend reading Vastrade (1986), Markwell & Thorne (1987), and Nott (1992) for an overview, or Scott and Fuller (1965) or Fox (1965) for a more in-depth study. In conclusion: behavioral patterns develop over successive phases, according to internal and external factors that interact in a complex and continuous manner. As Cyrulnik wrote, "the World of each animal is built around the double constraint of genetics and development".
                                                                  THE CONCEPT OF SENSITIVE PERIODS Bateson (1981) has described the developing individual as a train with its windows closed - at a certain point (maturing) the windows open and the traveler is encouraged to study the information passing by outside. Depending on the information presented (learning), he/she either continues (motivation) or stops (habituation, impregnation, or self-limitation) looking out the open window. In other cases the windows close when a new point is reached. This notion of learning in phases has various names: sensitive period, critical moment, optimal period, vulnerable point, crucial stage, susceptible period, and so on. A sensitive period is a point in the maturing process when events are susceptible to leaving long-term effects, or a period when learning is easier and knowledge gained is stored in the long-term memory. During the sensitive period, a small number of determining experiences have major effects (or damages) on future behavior. The sensitive period is preceded and followed by periods of lower sensitivity, and the transition is gradual. The notion of sensitive period is used in the place of critical period because the former extends over a longer period of time. Ducklings become attached to their mother between the 13th and 16th hour of life (Hess 1959, in Cyrulnik 1989), it takes 5 minutes of contact during the first hour after birth for a she-goat to become attached to the odor of her kid (Bateson, 1981), and a ewe needs contact within 4 hours after the birth of her lamb. Without this contact the mother will reject her young in the last two cases (Collias, 1956, in Scott and Fuller, 1965). These very short periods justify the term critical. Since puppies do not have such short periods of facilitated learning, we will use the term sensitive period. I was one of the people who helped spread this concept in French-speaking countries (Dehasse and De Buyser: 1983, 1989, 1991) by emphasizing on several occasions that the sensitive period in the behavioral epigenesis in puppies extended from 3 weeks to 3 months of age. The duration of this sensitive period had to be verified by delving into the literature on experiments in this realm and clinical review.                                                                                       THE PRENATAL PERIOD Pregnant rats that have been placed under stress or injected with ACTH or adrenaline give birth to young rats that are emotive and perform less well than a control group. (These young rats are raised by another mother that has not been placed under stress to preclude the possibility of postnatal maternal influence.) (Fox, 1978) In a similar vein, when a pregnant animal is petted her litter is more docile (Denenberg and Whimbey 1963, in Fox 1978). This effect, called the "gentling", "petting" or "caress" effect, can be prolonged by caresses to the new-born. According to Fox (1975, in Fox 1978) this activates the parasympathetic system, facilitating relaxation, digestion and emotional attachment, and thus socialization as well. Experiments by Cyrulnik with cats have shown that attachment depends on the cholinergic system; anti-cholinergics block the attachment process. The object of attachment is a being whose presence soothes and whose absence causes distress, who possess the signs of familiarization; a "reference being" (Eibl-Eibesfeldt 1984). This is probably linked to the social species' innate need for contact. A dog's tactile capacities develop before birth, and it is possible that it already becomes used to contact in the uterus, when the mother is petted. Puppies manipulated this way show a greater tolerance to touching than dogs born of a mother who was not petted. In rats, once again, manipulation (contact, exposure to cold, etc.) at a young age or before birth (manipulation of the pregnant mother) gives greater resistance to stress (cold, hunger) and disease (implanted tumors). This phenotypical effect is transmitted non-genetically for several generations (Denenberg and Rosenberg, in Fox 1978). These experiments enable us to deduce that when a gestating pet is given a friendly and caring human environment (with affectionate physical contact), the domestication and emotional balance of her offspring is facilitated, as compared with an environment where there is no contact and interaction with people.                                                                                   THE NEONATAL PERIOD We will only say a few words about this period, which arbitrarily ranges from birth to the opening of the eyes at approximately 13 days. Superficial, limited observation of the new-born puppy could lead one to believe it did not even belong to the canine species: awkward, dragging itself around, oriented to contact, the mother's teats and the smell of milk, yapping in distress when isolated, cold, hungry or in pain, and having only a limited capacity to keep itself warm and to learn. The new-born puppy is a completely dependent being, and apparently hardly influenceable psychologically in classical conditioning tests. As such this phase holds only minor interest in our study. It is possible, however, that the future holds surprising discoveries about the epigenetic importance of this neonatal period, especially as concerns the "manipulation" effect on neuro-hormonal development.                                                                         THE IDENTIFICATION PHASE At birth the puppy has not an innate recognition of members of its species; in a way it does not know it is a dog. This must be learned! Through species identification a puppy is able to recognize its parents (filial imprinting), and develop preferential intraspecific social relations (fraternal imprinting) and the relations (sexual imprinting) which mean the survival of the species (filial and sexual imprinting). An animal that is badly imprinted is lost for the species. Here are a few examples: Christy, a female puppy, was raised in complete isolation from other dogs by the "colony" of students at the Jackson Laboratory. At 9 weeks she was introduced to other dogs: the adults growled at her but showed no further signs of aggression and the puppies (litter-mates) began to play-fight and she responded. In 4 days time her behavior was indistinguishable from that of the other puppies (Scott and Fuller, 1965). Note that, unlike goats and sheep, adult dogs show no parental rejection of their young! A fox terrier puppy (male) raised in complete isolation and introduced to other dogs at 16 weeks displayed inhibited behavior and was attacked by the other puppies that were normally socialized. He was placed with other dogs also raised in isolation; the dogs lived alongside each other, without aggression but also without interaction (Fisher, 1955 in Scott and Fuller, 1965). Dogs raised in isolation and placed in contact with others of their species at 16 weeks are attacked and rejected. When the experimenters mime play-fights against these same dogs, they are able to recover a positive dog-dog interaction and complete integration in the same pack within a few days (Fuller, 1961 in Scott and Fuller, 1965). Male chihuahuas raised by cats until 16 weeks of age demonstrate preference for the presence of cats, and submission - or fear - in the presence of dogs (they also show no reaction to their reflection in a mirror). When they are placed with other dogs at 16 weeks, they recover intraspecies socialization in two weeks; they now prefer dogs to cats and react to images of themselves in a mirror (Fox, 1971, in Pieters 1984). On the other hand, puppies raised in a family from 4 weeks of age (becoming used to dogs, cats and/or children), without renewed contact with the laboratory dogs, show greater familiarity with people than with dogs. An adult sheltie (who had lived with a cat and two children) showed sexual attraction for the cat and attacked all dogs (male and female alike); a beagle became "attached" to a vacuum cleaner bag; a basenji (who lived with a female dog) became a delinquent stray who attacked other dogs  (Scott and Fuller, 1965). Clinical practice shows that when a puppy is acquired at 6 weeks this is already a handicap in developing its adult social and sexual preferences. We should also mention that the first signs of humping (pre-imitation of future sexual behavior) appear as early as 3 to 4 weeks (Scott and Fuller, 1965). This behavior is provoked by pressing on the sternum or the stomach. It is possible that this is a factor in sexual imprinting, but it has yet to be proven. To my knowledge, no statistical studies have been made on dogs raised in isolation, covering a broad range of breeds (for ethical reasons?), which means that crucial experimental data are lacking. Our knowledge is partially extrapolated from ethology studies in birds. Among birds, imprinting lasts throughout parental care and this period is shortened when there is a danger of mixing species. Preference is given to visual and auditory imprinting whose effects last almost a whole lifetime. With mixed imprinting, there is a preference (innate predisposition?) for one's own species over a neighboring species, and for this species over a more distant one (such as humans). In conclusion, species identification (filial, fraternal and sexual imprinting) is acquired during a sensitive phase of development, and depends on "play-fighting" among puppies (litter-mates). This begins about the third (3±½) week and ends somewhere between 11 and 17 weeks (12±5), when the dogs loose their ability to play with unfamiliar dogs and become "serious" in defending their group. In the absence of siblings, a puppy establishes identification through care-giving, care-searching and/or playful interaction with its parents or other dogs. This interaction must last until at least, if not beyond, the 6th week. The presence of other species during this period does not hamper identification with one's own species. The end of this phase varies depending on factors that are internal (breed, line of descendants, individual) and external (behavior of the mother, other dogs, quality of the surroundings). A stressful environment (feral dog) will close this phase ahead of time (probably around 7 to 9 weeks). This type of learning presents several characteristics: it is stable, rigid and persistent (sometimes for life); it is easily acquired; sexual imprinting occurs on supra-individual and supra-breed characteristics, which permits species generalization; filial imprinting (attachment) seems to be more discriminating and is limited to parents; fraternal imprinting is the basis of sociability; attachment is an interactive process. Risk factors They are similar to those found among birds. The total absence of other dogs (own species) between 3 and 12±5 weeks fosters identification with another species that is closest (in general humans, but occasionally cats, rabbits, etc.) or an appropriate substitute (stuffed animal, vacuum cleaner bag, etc.). This identification is persistent, occasionally for life. In adults this leads to: Courting behavior and attempts to copulate with the identification species (despite activation by pheromones of one's own species), no behavior of this type or else awkward attempts with a sexual partner of the same species, Social preference for the identification species, Rejection (flight or fight) of one's own species (including mirror images). The relative absence of other dogs between 3 and 12±5 weeks leads to relative, total or no handicaps depending on circumstances: possible recovery of the dog's species identity at 9 weeks when it plays with other puppies, attachment to the identification species and disinterest or aggression towards canines, despite the (almost) normal capacity to reproduce, etc. The imprinting effects of a mirror placed in the surroundings of a puppy isolated from other puppies have not been studied (to my knowledge). Since no interaction is possible with a mirror image, this seems to be a poor substitute for suitable "imprinting".
                                                                  RISK FACTORS There can be several risks involved in acquiring a puppy as a pet: The human desire to give and receive attention is opposed to the normal (agonistic) parental behavior to wean the puppy, detach oneself and encourage autonomy. The result can be attachment, even hyper-attachment, later engendering a separation anxiety syndrome. The human tends to fear for the puppy's health and thus pays particular attention to its appetite, watching it while it eats, indulging it when it begs, worrying about finicky appetites or loss of appetite, varying food, and hand-feeding, which become invested with the social symbol of dominance. The anthropomorphic tendency of a human-dog relationship to develop into that of parent-child, or parent-baby postpones the puppy's training towards adulthood at 5-10 months as well as the order-obedience relationship that is part of hierarchization. This delay can foster sociopathy and certainly does not facilitate obedience. Furthermore the lack of rituals lead to their malfunction, and even changes in their significance: if a dog in a submissive posture is petted (positive reinforcement) it will adopt this posture more often in the search for attention. The master then obeys by petting it. The relationship risks reverting to one with a demanding-dominant dog and a obedient-submissive owner. Dogs have a cynomorphic approach to the human-dog relationship, seeing it first as one between puppy-adult dog, then as an interaction between pack-mates (pre-adult-adult). A dog views human behavior through the social lens of its own species and attempts to gain privileges as high as possible on the hierarchical scale. These risks are avoided when dog owners behave in a way that can be assimilated to the parent-dog relationship. It is clear how the Western world's custom of acquiring pets favors the emergence of hyper-attachment and sociopathies (dog as a toy, an object (a live teddy bear), a substitute for children, a catalyser for social reactions, spoiled dog, etc.).                         THE COGNITIVE SENSATION-RATIONALIZATION PHASE IN PRE-PUBERTY In clinical practice we have observed cases where phobic behavior (both towards the dog's immediate surroundings and towards humans with which the dog has little contact) and anxiety develop in pre-puberty. This occasionally leads to an anxiety syndrome which I call "anticipated defense behavior" (Dehasse, 1990a). A Bernese sheep-dog (raised in Belgium) developed intermittent anxiety (with pathological anticipations) around the age of 6 months, despite a social and sensorial enrichment between 3 weeks and 4 months. Her sister acquired the same tendency in a completely different environment (Netherlands), as did her brother (in Switzerland). A family of briards (Brie sheep-dogs) displayed the same tendency, despite differences in the surroundings in which they were raised. This enables us to propose two hypotheses: the hypothesis of inherited temperament and that of the phase of pre-puberty sensitization. A bibliographic study confirms there is a phylogenetic and/or epigenetic tendency for pre-puberty sensitization. Fox (1978) studied primary and secondary socialization in wild dogs and other canines that were raised in identical environments and had daily contact with the trainer and intermittent contact with unfamiliar humans. The wild canines all remained attached to the trainer, at least until they reached maturity, and then became less tolerant to contact with or proximity to the trainer all the while welcoming him with appeasement postures (whereas in the beginning he was welcomed with active postures: jumping, licking, nudging). Wariness of strangers develops: quickly in the solitary species (from 4 months in foxes), later in species of average sociability (around 1 year for jackals and coyotes), and much later in social species such as wolves (between 6 and 18 months) or dogs (beagle, pointer or Chihuahua - between 1 and 2 years). There is a correlation in canines between wariness and the arrival of puberty (10 months in the coyote, 2 years in the wolf), except in foxes (wariness largely precedes puberty) and dogs (wariness follows puberty which appears around 6 months). In dogs, precocious neutering can delay or preclude the emergence of wariness towards strangers (Brunner, 1968, in Fox, 1978), which could possibly confirm the tendency's hormonal cause. It is Fox's opinion that domestication led to a dissociation between gonadal maturing (precocity) and maturing of the central nervous system (late). Figures given for dogs, however, are hardly conclusive. We all know how the age of puberty, temperament, emotivity, sociability etc. can vary among breeds and individuals. It is thus normal to see the appearance of wariness towards strangers (or the unknown) or a loss of certain social experience and sensorial references between 4 months (as in foxes) and 2 years (as in wolves). This can also be compared to the development of so-called territorial aggressivity. Woolpy (1968, in Fox, 1975) accustomed adult wild wolves to contact with humans in 6 months' time; he then isolated them somewhat from humans: in this case they retained their socialization experience. He also accustomed wolf cubs to humans, then isolated them: in this case there was de-socialization (instability of precocious socialization). Young animals need continuous reinforcement. The same holds for dogs: when a normally socialized puppy is isolated from humans and placed in a kennel from 3-4 months of age to 6-8 months he becomes fearful in the presence of humans, even the trainer. Woolpy's interpretation (for wolves) is that socialization is limited by fear of the unknown. Although the behavioral signs are precocious, the subjective element evolves gradually over a year (at least). Thus before socialization can be acquired, the subjective (cognitive) element of fear must first mature. In other words, fear of the unknown has both an emotional and behavioral phase (starting around 5 weeks) and a cognitive phase (near puberty). It is my hypothesis that an optimal period of attraction-habituation (acquiring sensorial and emotion homeostasic referentials) closes with an emotional and behavioral phase of aversion-fear of the unknown (5-14 weeks). There follows a vulnerable period of cognitive sensitization at pre-puberty or puberty during which minor trauma can occasionally entrench wariness or fear, (ill)adaptations, and cognitive and emotional distortions that are undesirable in a dog living among humans in a city environment. Risk factors Sensitization (and the often indissociable generalization) is the process that engenders wariness, fear, phobia and anxiety. The cognitive process it entails leads to a dog's anticipating harmful situations that exist only in its mind (in a way, fear of being attacked) and thus behavioral strategies (defense mechanisms: flight, aggression, inhibition). It is at this sensitive age that dogs often begin group training courses. It is imperative for the training environment to be controlled to ensure the dog does not suffer any psychological trauma. At pre-puberty, however, dogs emit pheromones that activate demonstrations of authority by the group's dominant dogs. It is best to begin group courses around 3 months of age, so that the dogs can become familiar with each other and hierarchies before puberty.                                                                        PUBERTY AND HEIRARCHY Dogs are social animals that need company, living in a hierarchical pack (or family-pack). In clinical practice we continually observe cases of conflicts (competitive aggression) at puberty, and later in adulthood. These conflicts revolve around access to the opposite sex (intra- or interspecific), but they can also arise over occupation of certain areas of the group's common space (in the house in cases of conflicts with the dog's owners, and rarely outdoors), in particular feeding and sleeping areas. Our hypothesis is the following: an optimal period of intraspecific socialization (identification) is followed by several crucial periods of hierarchization that occur in successive phases: food, territory, socio-sexual at puberty and maturity.  Pageat (1984) demonstrated the existence of a triple surge of social aggressivity in dogs (male spaniels): the first peaks around 4-5 months with the dog returning to normal around 6-6½ months, when it begins obedience lessons (the owners assert their dominance); the second surge coincides with the production of sexual steroids (±5 months); the third corresponds to a "second attempt to obtain reproduction rights" and only occurs in dogs who are allowed to live in the house. Pageat explains this as follows: in a dog-pack, adolescent males at puberty are pushed to the fringe of the group (by the alpha male and the other older males). The third aggressivity surge does not appear at this time. This is because in a group, the dominant members react and put the young dog in its place each time it tries to compete aggressively, barring its access (satellisation) to socially invested areas and sexual partners. If the dominant members fail to react, aggressivity is reinforced and the young dog rises in hierarchy. In Fox's experiment (1975) with various wild and domesticated canines, there was a surge in aggressivity in male jackals and wolves at the onset of puberty which increased until it peaked at 2 years. Aggressivity was directed toward males (canines and humans). Note that canines are perfectly capable of distinguishing the sex of humans, even when they are dressed alike; this is probably through their sense of smell. Fox also pointed out that competitive aggressivity may not appear in wolves (males as well as females) until 4-5 years of age (maturity). We have seen that hierarchization occurs during a first "food" phase between puppies (from 5 weeks and is practically established, depending on the breed, between 3 to 12 months), then between adults and puppies (around 4 ± ½ months). This phase corresponds to the first surge of social aggressivity identified by Pageat. The second phase of hierarchization, puberty, is sexual, social and zonal-spatial. The young dog develops an interest for the opposite sex and for areas occupied by the dominant members, who react by pushing the adolescent to the fringe of the group. The process is complex: sexual pheromones are awakened at puberty, activating "desire" (Vincent, 1986), the dog exhibits courting behavior and is rejected outright by the dominant member of the same sex, the only one of the group with the right to exhibit his/her sexuality openly. The adolescent is pushed from areas occupied by the dominant members (high-placed positions, controlling passages, preferential sleeping areas, etc.). It no longer has the right to greetings, licking and other social attentions given by the other dogs. This is why this phase is social, spatial and sexual. This phase is generally accompanied by territorial defense behavior. In some breeds it occurs earlier, appearing from 2 months. In females, progesterone favors territorial defense behavior, just as it favors whelping and pseudocyesis. A third phase of hierarchization occurs at maturity (adulthood), an age that varies in dogs depending on the breed (from 8 months to 3 years). It reproduces the same characteristics as the second phase, only this time with all the weapons, strength and passions of a mature adult. Risk factors If adolescent dogs do not undergo hierarchization-satellisation, they gain hierarchy - access to the privileges of the dominant member. The dog's relation with its master thus becomes ambivalent, with conflicting messages: demands (dominance) - tolerance (submission). The lack of comprehensible appeasement rituals favors attitudes of competitive aggression (sociopathy) or substituting behavior (sometimes self-directed).                                                       DISCUSSION AND CONCLUSIONS No quantitative studies have been made on intra-breed variability, and inter-breed studies have only concerned a few family lines in selected breeds. It is thus impossible to form conclusions based on breed in view of the number of dog breeds identified up to now (more than 200). Furthermore, the studies we have cited have never been conducted on a large number of animals. The results mentioned are thus qualitative and speculative, as are the dates and periods. Nevertheless, a dog's ethogenesis evolves in (at least) three overlapping phases, each related to a particular system: the neuro-vegetative (neuro-glandular) - 1 to 7 weeks, the emotional (limbic) system - 3 ± ½ to 12 ± 5 weeks, and the cognitive system (cortex) - 5 ± 1 to 18 ± 10 months).
                              THE DIFFERENT PHASES OF DEVELOPMENT Neuro-vegetative from -4 (before birth) to +7 weeks Imprinting-Identification from 3±½ to 12±5 weeks Filial, fraternal and sexual imprinting Intraspecific sociability Emotional-Relational from 3±½ to 12±2 weeks Socialization - Thymostasis - Conditioning, etc. Cognitive 5±1 to 18±10 months Hierarchization - Rationalization - Territorialisation
Each phase presents a series of risks that can undermine the dog-dog and dog-human relationship. A dog's epigenesis engenders multiple temperaments that can be partially foreseen by controlling its environmental stimuli. One factor favorable to emotional and relational well-balance of a dog that must live with humans in a city context is enrichment in the breeding environment.   It is the breeder's role is to ensure temperamental selection and to enrich the development environment (under veterinary guidance). The role of the veterinarian is essential because he/she sees the animal from 6 to 16 weeks for its vaccinations. He/she thus theoretically has several occasions to assess the puppies' early emotional and behavioral development and can recommend preventive measures and training techniques. The media can also play a role in educating potential dog owners to adapt their relational needs to the dog's ecological and social reality, rather than their own personal wishes. The trainer must not only inculcate the bases for instrumental learning, he/she must also take advantage of having a group of dogs to continue their socialization and avoid de-socialization, both towards other dogs and towards humans. Dog owners must find adequate counseling to prevent multiple relational (systemic) and behavioral dysfunctions in their dogs. But they must first be aware of the problem and know where to go for advice. It is up to the veterinarian to inform them!
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