Sensory, Emotional and
Social Development of the Young Dog
© Dr. Joël Dehasse
3 avenue du Cosmonaute, B-1150 Brussels
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).
It is a long article of 72,4
K. I have not cut it in parts, so it may take some time to load.
I have removed all images and charts to facilitate loading.
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
1-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).
2-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,
3-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....
4-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).
5-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
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.)
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
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
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
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
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,
Clinical practice shows that when a puppy is acquired at 6 weeks
this is already a handicap in developing its adult social and
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.
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
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,
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".
The socialization-domestication phase
A puppy is not programmed to interact socially with another species.
Twelve thousand years of domestication, however, has shown that
this is possible. The dog's particular nature - a puppy has to
learn to identify its own species - can serve to foster socialization
with other species (called domestication when it involves interaction
Let's look at a few experimental cases:
Puppies raised in a semi-open environment in (nearly) complete
isolation from humans reacted differently towards an active unfamiliar
observer depending on their age. Each puppy was taken from the
surrounding in which it was raised, placed in contact with humans
for one week, and again tested. Fear in the presence of a human
that handled him decreased from 3 to 5 weeks, was minimal at 5
weeks, then increased again afterwards. "Recovery" (improvement
or disappearance of fear) after a week of interaction-socialization
was more efficient at 3 weeks; it was roughly the same at 5, 7
and 9 weeks (Freedman, King, Elliott, 1961, in Scott and Fuller,
A puppy - raised in the same type of surroundings - was placed
10 minutes a day with a passive observer, calmly sitting in the
room and paying no attention to the dog (Scott and Fuller, 1965):
at 3 to 5 weeks, the puppy investigated the observer openly;
at 7 weeks, it took 2 days before it investigated (2 10-minute
at 9 weeks, 3 days;
at 14 weeks it no longer investigated the observer.
At 12 weeks a puppy is easily frightened. Confinement and hand
feeding enable it to accept contact with its laboratory handler(s)
but not with strangers, and it still prefers the presence of dogs
to that of humans (Scott and Fuller, 1965).
This fearful reaction has been found in all breeds tested. When
put on the defensive a cocker's bite is "softer" than
that of other breeds tested (basenji, terrier, beagle, sheltie).
According to Fuller (1961), puppies raised in isolation in a laboratory
develop adequate socialization to humans if they receive two 20-minute
periods of human contact per week. This short contact, however,
is not enough for basenji puppies; this variability is thus truly
linked to breed (genetics) (Scott and Fuller, 1965).
In conclusion, puppies demonstrate an investigation-attraction
behavior towards the unfamiliar as soon as they are able to
express this attraction (almost adult motor capacity), in other
words at 3±½ weeks. This attraction subsides in
an almost linear manner after the fifth week until at least
9 weeks. The attraction recedes under the influence of fear
of the unknown behavior which grows after 5 weeks; the
puppy "recovers" from its initial fearful reaction instantaneously
from 3 to 5 weeks (investigation behavior effect), and then it
remains wary for longer periods as it grows older. At 12 weeks
socialization requires active manipulation (mimicking play-fights),
at 14 weeks socialization seems to be impossible.
In birds fear of the unknown is delayed when they are raised in
isolation; this phenomenon thus appears to depend on experience
rather than maturing of the nervous system (McFarland, 1981) -
one must first be able to refer to something "known"
before fearing the unknown.
An arbitrary limit can thus be set for spontaneous socialization
to another species, during a first encounter, at 12
± 2 weeks. Nothing, however, enables us to affirm
or deny that rapid habituation to close stimuli cannot be achieved
after 12 weeks.
Interspecies socialization (attachment) does not have the same
characteristics as species identification:
It is easily acquired but requires permanent reinforcement
to avoid de-socialization;
it is not generalized (generalisable) to all individuals
of the species concerned, but remains relatively limited
to the individual's characteristics. It is thus infra-species:
it is a "type" socialization (human: man, woman, adolescent,
child, baby, black, white, with/without beard, hat, white apron,
etc.). The capacity to generalize varies from one species
to another (dog and wolf, more than coyotes), breed (watchdogs
less than other dogs, according to Fox, 1978), the family line
and individual (no statistical studies available).
the threshold of socialization (number of interactions)
is variable and depends on factors that are internal (breed, individual)
or external (mother's fearful behavior, quality of the surroundings,
Domestication depends on the presence of humans between 3 and
12 ± 2 weeks in the surroundings in which a puppy develops
and this socialization must be continued throughout the animal's
life. The lack of human contact between 3 and 12 ± 2 weeks
fosters the development of fear/wariness of humans (feral dog).
The relative absence of human contact leads to relative handicaps,
such as fear/wariness/phobia towards a type of human (children,
The interactive presence of different types of humans between
3 and 12 ± 2 weeks facilitates a puppy's generalized socialization
The interactive presence of other animals leads to interspecific
socialization and attachment, and it counters predatory behavior.
Interspecific socialization counters predatory behavior towards
the type of attachment individual.
The emotional self-regulation (homeostasis) phase
Homeostasis is the ability of an organism to maintain an
equilibrium in a variable environment. Just as we have thermo-regulation
(thermal homeostasis), we can also speak of emotional and relational
homeostasis (Vincent, 1986). And we could even stretch the analogy
somewhat: the organism has a thermostat for heat regulation, and
a 'ponderostat' to maintain an ideal weight (Vincent, 1986). Likewise
for emotional and relational homeostasis we could also envisage
the existence of a "sensoriostat", "thymostat"
or "sociostat" respectively measuring a being's
sensorial perception, and emotional and social equilibrium.
Living in a group and adapting to varied environments calls for
a certain degree of emotional equilibrium (with minor fluctuations).
This adaptation is possible only through habituation (disappearance
of reactions) to certain stimuli. That this process is essentially
learned, rather than genetically acquired is a sign of the species'
ability to conquer - and adapt to - varied and new environments.
This ability is an opportunity, but also a cause for risk.
Among animals, innate fears do exist, although in dogs
they remain to be demonstrated: for example the fear of "beating"
or "gunshots" is not innate, despite various writings
along these lines. Nonetheless, you can talk about acoustic sensitivity
in individuals or breeds. This has been demonstrated in rodents:
certain strains of mice (DBJ/2J) have shown an innate
hypersensitivity to certain sound frequencies which give them
convulsions (Dantzer, 1988).
A large number of fears arise from an individual's development.
Is there a sensitive phase during which it would be easier to
establish emotional homeostasis, enabling the individual to develop
frames of reference (referential, thymostat) and
long-term habituation? The answer is "yes".
Here are a few examples:
A dog's typical reaction to an unfamiliar situation is fear: starting,
fleeing or inhibition. In a semi-open milieu, the dog tends to
flee (and is impossible to catch after the age of 4 months) (Scott
and Fuller, 1965). w w When it is
raised in isolation in a closed environment (0.2 m² cage)
the flight reaction does not develop; instead only inhibition
or fear-provoked aggression develop (Fisher, 1955; Fuller, Clark,
Walker, 1960 in Scott and Fuller, 1965).
If guide dogs for the blind are placed in a foster family at 12
weeks, they generally adapt well, but placement at 14 weeks can
prove to hinder performance in later training (Scott and Fuller,
Fox (1975) experimented with puppies placed in contact with increasingly
complex stimuli (enrichment) at 5, 8, 12 and 16 weeks:
as they grow the puppies tended to seek out complex environments.
Puppies raised in surroundings poor in stimuli ("stimulus-poor
puppies") and placed for the first time in a highly stimulating
environment at 12 or 16 weeks are inhibited (fear) and search
less complex environments. Enriched puppies are systematically
dominant in the presence of stimulus-poor dogs.
Male dogs are raised in normally lightened cages for the 10 first
months of their life, but without any contact with the outside
world (restricted sensorial situation). They are tested
at 10 months old. Their activity level is 6 times higher than
average dogs raised in normal surroundings (motor hyperexcitement).
They learn slowly and forget easily (every trial is like a new
experience). When they have learned some behavior, they reproduce
it even when the rewarding factor has been removed (lack of
the extinction process). Put in the presence of a bitch in
oestrus, they show a state of increased excitement but they direct
it towards stereotyped habitual behaviors and not towards the
stimuli coming from the bitch. (Caston: 1993). For Caston, sensorial
and social deprivation has impeached the maturation of the brain:
it can not exert an inhibitory influence on the mesencephalic
reticular formation (MRF) anymore; MRF is becoming hyperactive,
and produces unfocalised and unadaptative behaviors. This has
been verified by EEG recordings (in rabbits). In rhesus monkeys,
this deprivation syndrome leads to high level of blood
Stimulus-poor primates show a greater degree of attachment to
their mother (pathological hyper-attachment), which led Bobbitt
(1968, in Fox 1975) to propose that detachment from the mother
is a continual process linked to a young being's attachment to
the environment. This conclusion can most likely also be applied
In clinical practice we have observed dogs acquired at 3 or 4
months that had phobic behavior, whereas their siblings, acquired
at 2 months, were emotionally balanced.
I also participated in a study on the effects of a serotoninergic
psychotropic drug on the behavior of beagles raised in a kennel.
The beagles were chosen for their anxious-inhibited (depressive)
behavior. In exactly identical conditions, with limited human
contact (kennel staff) it was easy to choose 16 dogs of 8 - 13
months in which the following symptomatic behavior towards the
presence of humans could be observed:
-expectancy posture (Pageat, 1986) (locomotor inhibition,
almost crouching, tail between the legs, head extended towards
the stimulus presented),
-refusing, or cringing from, hand contact,
-lack of interest or catatonic immobility in the presence of a
colored moving object,
-inhibited movements outside the kennel (limited city noise).
In this single-breed kennel (little variation in genotype) in
a relatively deprived sensorial environment, there was a high
degree of phenotype variation with, nevertheless, a large percentage
(more than 50%) of dogs displaying inhibited behavior (more than
75% of the dogs were anxious). An overall inhibition index was
established (4 tests each rated from 1 to 6, for a total ranging
from 4 to 24 points, with 24 being the value for a normal dog).
-At the start of the experiment, all the dogs tested between 4
to 10 points.
-After 2 months they ranged from 8 to 21.
-As the effects of the psychotropic drug were not significantly
demonstrated compared to that of a placebo, the evolution towards
'normal' behavior could be imputed to the effects of the experiment
itself, since the dogs were tested every other week (5 minutes
maximum per dog) and given medicine twice a day.
In conclusion: "industrial" kennel conditions suffice
to cause anxiety and inhibition (undoubtedly favored in this case
by the breed and enclosure in a 9m² cage). Nevertheless a
mere daily contact, and handling every other week were enough
to lower the level of inhibition and anxiety in this group of
young adult dogs significantly.
Indeed, the process of organizing stimuli from the outside
world, classifying them as known or unknown, agreeable, disagreeable
or indifferent (their "significance", meaning, socialization)
is similar to the process of interspecific socialization.
Eventually, this is merely one element in the acquisition of self-regulation
as regards particular stimuli because they are interactive.
We thus have a phase of facilitated spontaneous learning that
begins with a dog's sensorial opening and investigation of stimuli
(3 ± ½ weeks) and ends when it develops fear
of the unknown (12 ± 2 weeks).
The characteristics of this learning phase are the same
as those of interspecific socialization (facilitated but requiring
reinforcement, low level of generalization, etc.).
The result is frames of reference acquired for each isolated
or grouped sense (multi-sensorial referential,
or tolerance level (according to Fox, 1975), or even "thymostat"),
since each referential is probably a "mental object"
identified by an activated assembly of neurons, according to Changeux,
This referential determines the stimulation level at which the
individual must begin to adjust by activating the appropriate
emotion (fear, wariness, etc.) and adopting the most appropriate
adaptive behavior (investigation, avoidance, flight, aggression,
The referentials that come into play are level of noise, visual
agitation, intensity of olfactory stimulation, number of vibrations,
occupation of three-dimensional space, flexibility or rigidity
of movements, etc. Here we can directly see the overall differences
between a city and rural environment of development.
The corollary to the development of a puppy's attachment to its
surroundings is its detachment from its parent(s).
A puppy's malleability enables it to rapidly adapt to almost all
human environments without undo stress.
Differences in the quality and amount of stimuli a puppy receives
in its environment of development as compared to its adult surroundings
determine the degree of risk it may not be able to adapt
its sensorial referential (thymostat) and thus achieve emotional
homeostasis (this includes development of phobias and anxieties).
Clinical observation has also confirmed that it is easier to transfer
from an environment with a high level of stimulation (city) to
an environment with a low level (rural) than the contrary. A puppy
raised in a deprived environment may be tempted to compensate
for this lack of sensorial stimulation by self-stimulation:
this is how certain stereotyped behavior develops, as well as
self-centered behavior (Fox, 1975), such as self-induced dermatoses.
Lastly, stimulus-poor puppies run the risk of developing hyper-attachments
to their biological or adoptive parents (transposition of hyper-attachment
to its new human masters), which is a source of intolerance to
isolation, attention-seeking behavior, reutilization of behavior
acquired during illnesses, etc.
The precocious learning-conditioning phase
This is another variant of the phase sensitive to emotional development
that occurs between 3 ± ½ and 12 ± 2 weeks. Three
behavioral situations are of particular interest in precocious
learning: elimination, eating, and vocalization.
Elimination is a reflex present at birth (it is provoked when
the mother licks the puppy's perineum) and becomes spontaneous
around 2-3 weeks. From 3 weeks on, the elimination reflex
disappears and the puppy tends to leave its bedding to eliminate.
At 8½ weeks it defecates in specific spots, usually
at a distance from its eating and sleeping area.
Elimination behavior (1) is preceded by sniffing around, probably
in search of typical odors (urine, feces, chlorine, ammonia, etc.)
that will spark the elimination reflex, (2) occurs almost every
waking hour, (3) is not activated for several hours during sleep.
It is thus the dog breeder who conditions the location and medium
favored for elimination. The acquirer (when he receives the 7-9
week old puppy) must then respect these socio-ecological conditions
- he must limit the space available when the puppy is not under
human control and provide the adequate elimination medium (why
not a large litter box in an apartment?) placed at the right location
(at least 2-3 meters from where the puppy eats and sleeps).
Clinical observation shows that when some puppies are limited
to one spot and medium until the age of 15 weeks (puppies kept
in the house and elimination on newspapers, for example) it becomes
almost impossible for them to learn to use other media and locations
(conditioning) and they retain themselves for hours when walking
outside until they can eliminate on their preferred medium and
This ease of conditioning can be put to an advantage in teaching
dogs to eliminate in gutters and other sewer outlets.
Food conditioning studies have been conducted on cats that became
vegetarian or imitated their mother who ate bananas. This type
of conditioning is also well-known in humans: preferences or aversions
for certain odors or tastes are already determined before birth
(preference-aversion experiments with a rubber teat dipped in
garlic sauce) (Cyrulnik, 1989). We can postulate an intra-uterine
and post-natal food acculturation. To my knowledge, no experiments
have been made to determine the duration of the food imprinting
phase. It is possible that this phase is similar to the self-regulation
phase, both in its duration and characteristics, since it engenders
a food or feeding preference that is persistent but changeable
Feeding a puppy solely on standardized food, invariable in taste
and appearance (dry or moist) can lead to long-term preferences
and rejection of other types of food (this has been clinically
proven in cats). This problem can be avoided by giving the puppy
a variety of food.
Barking from distress when left alone in an unknown place increases
from 3 to 6-8 weeks (maximum) then decreases until 12 weeks.
The rising curve reflects a progressive attachment to a familiar
place (attachment location) while the descending curve after
7-8 weeks is a sign of emotional maturing (more than habituation)
and motivation to explore the unknown.
When a puppy is acquired at 7 weeks and left alone at night it
will bark in distress. This barking disappears spontaneously after
a few days as it becomes familiar with its new home (with reassuring
significance), unless its behavior receives positive reinforcement
from its new masters (who come to pet, calm or scold the distressed
puppy, or take it into their room, all signs of attention - thus
The intensity and frequency of this vocalization normally diminish,
to be replaced by intraspecific communication such as postures
and rituals. Vocalization is used to ward off strangers ('territorial'
defense) from the age of 11-15 weeks (see below). Some breeds
have a greater tendency to bark than others (Hounds, Poodles,
Yorkshires, etc.). Barking is easy to condition.
Interspecific communication with humans, also a vocal and verbal
animal, reinforces the vocal element (learning by imitation),
which then becomes preponderant, even disruptive.
Play-fighting and learning to control biting
Play-fighting, which begins at 3 weeks, can sometimes be painful
when a puppy begins cutting teeth, especially when its ears are
bitten. A bitten puppy whimpers or squeals. In a one-on-one or
one-on-two fight the bitten puppy is able to turn the tide of
the 'battle' and bite its adversary(ies). And this is precisely
one of the "rules of the game": to change roles, with
the biter becoming the bitten and vice versa.
w The puppy learns to make an empathetic
link between the opponent's squeal and the pain invoked.
w Reciprocal biting negatively reinforces
w Biting is thus stopped,
inhibited and controlled.
These play-fights also lead to a certain hierarchization of relations
(less than 25% among litter-mates at 5 weeks of age)
The intensity of the bite is (congenitally) variable depending
on the individual, line and breed, and can be modified considerably
From 7 weeks on puppies of a litter occasionally form groups to
gang up on a lone puppy. In these cases biting is uncontrolled
and the attacked puppy can be wounded (sometimes fatally). This
phenomenon is more prominent in certain breeds or lines (Fox terriers,
according to Scott and Fuller, 1965; Schnauzers, Huskies, and
Malamutes among others, in my experience).
From 11 to 15 weeks play-fighting recedes; it becomes less
aggressive and more controlled. The fights become ritualized,
a sign that stable hierarchical relations are being established.
Agonistic co-operation is directed towards outsiders who are investigated
and attacked in a manner more "serious" than play-fighting.
Learning to control the intensity of its bite is actually part
of a puppy's growing general control of its movements,
enabling it to adopt postures and facial mimics which become the
prevalent form of communication in animals having highly developed
If the puppy's owners fail to reproduce play-fighting postures
and allow it to bite their hands, arms and legs, this can
1- the puppy's hierarchical dominance that can induce relational
problems later on (competitive aggressivity, sociopathy).
2- failure to control the intensity of biting and risk of serious
(wounding) biting in minor confrontations.
Human skin is more fragile than a dogs. Dogs that are family pets
must be given more thorough training in controlling the intensity
of their bite.
A dog encouraged to pull at objects it holds in its jaws
reinforces the biting reaction, which is undesirable in a family
pet (although it may be useful for police and guard dogs).
And lastly, failure to develop a dog's general motor control encourages
hyperkinetic forms of behavior.
Weaning-detachment and (food) hierarchization
A mother's care and attachment towards her puppies are strongest
during the first 3 weeks of life, and after that progressively
The first phase of weaning begins around 5 ± ½ weeks;
the mother growls and bares her teeth when puppies attempt to
nurse (painful when the puppies cut their teeth); the puppy yaps
and rolls over on its back and then learns to keep away from its
mother's teats (Scott and Fuller, 1965). An aggression-inhibition
relationship - a dominant-submissive hierarchization - is then
established between the mother and puppy for access to the mother's
This attitude is extended towards other mother-young conflicts
and adopted in the presence of other adults, as shown by the following
personal observation. In a husky breeding station the presence
of the mother beyond the 5th week led to her puppies' spontaneous
submission to the adults of the pack. In another station the mother
was taken from the breeding kennel when her puppies were 5 weeks
old; these puppies were not submissive to adults when they were
first placed with the rest of the group at 12 to 16 weeks. They
did not use the submissive posture (rolling over); the ritual
was not acquired.
The presence of the mother is thus favorable, even necessary,
for the development of appeasement-submission rituals and for
the puppy's hierarchization in the adult pack.
Lactation wanes around 7 to 10 weeks.
From the age of 5 weeks the puppies begin to growl to gain possession
of their food. At the mother's arrival the puppies assemble in
the attempt to nurse and wait for their mother to regurgitate
pre-digested food: they wag their tails, lick and bite at the
mother's chops and try to take regurgitated food directly from
The mother does not compete with her young (7 weeks of age) and
allows them full access to the food (even if it is a bone) (Scott
and Fuller, 1965). This free access ends as the puppy becomes
autonomous and takes its place in the adult hierarchy (Pageat).
At about 16 weeks the puppies must take their place in line for
food, i.e. after the dominant and sub-dominant members, almost
last. The puppies share and fight over what is left, and gobble
it up rapidly, to the complete indifference of the dominant members
who return to other activities. Puppies attempting to snitch food
while the dominant members are eating are snapped at, growled
at and threatened with being bitten. Some puppies nonetheless
manage through appeasement rituals to grab some food and escape
with it to a corner. Hierarchization for food privileges thus
occurs around 16 weeks.
When a pair of puppies not competing for maternal attention are
given a bone there is aggressive competition ending with
a winner and a looser. The fight is rarely traumatic since adult
fighting capacities are as yet undeveloped. Hierarchization
between litter-mates varies with age and breed (Scott and
- 25% at 5 weeks,
- 50% at 11 weeks,
- 75% at 15 weeks in terriers,
- 75% at 1 year in basenjis and shelties,
- 50% maximum in cockers and beagles.
Food hierarchization varies by race and age. According
to Scott and Fuller (1965), it is predominant in short-haired
fox terriers and basenjis (the male dominates the female); and
rare in shelties at 11 and even 15 weeks (less than 50% of couples
although this figure increases to 75% around 1 year). This breed
has been shown to "respect" (accept) the female's priority
to food. Food hierarchization is average in cockers and beagles
with no predominance of either sex. The sheltie, on the other
hand, develops a strong hierarchy in defending the nest (spatial-territorial)
and submissive members (females) are pushed inside the nest.
The more "aggressive" the litter (line, breed), the
greater the tendency for linear hierarchization.
All puppies that are correctly socialized will "leap"
towards humans who enter their area (bed, cage,...). The boldest
ones are generally the most dominant; they push back their submissive
pack-mates, barring access. Choosing a bold puppy (to avoid adopting
a seemingly unsociable one who stays at the back of the cage)
may thus mean selecting a dog that will be more aggressive to
In conclusion: this period leads to food hierarchization among
litter-mates from 5 to 15 weeks (occasionally later), between
puppies and adults from 4 ± ½ months, and reutilization
of submissive postures (dorsal-lateral decubitus) towards
adults (from 5 weeks) and appeasement postures (nibbling the
chop and extending the paw) from 8 weeks.
There can be several risks involved in acquiring a puppy as a
1- 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.
2- 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.
3- 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.
4- 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.
5- 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 sensitisation-rationalisation phase
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
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:
w quickly in the solitary species
(from 4 months in foxes),
w later in species of average sociability
(around 1 year for jackals and coyotes),
w 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
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.
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 hierarchization
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
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
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.
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
from -4 (before birth) to +7 weeks
from 3±½ to 12±5 weeks
Filial, fraternal and sexual imprinting
from 3±½ to 12±2 weeks
Socialization - Thymostasis - Conditioning, etc.
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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Attachment, cognitive, conditioning, detachment, development,
domestication, emotion, elimination, epigenesis, ethogenesis,
expectancy posture, feeding, hierarchy, homeostasis, identification,
imprinting, learning, ontogenesis, play-fighting, sensitive period,
socialization, thymostasis, vocalization.
©Dr Joël Dehasse