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Anita. Behav.

, 1966, 14, 273-281

BEHAVIOURAL EFFECTS OF DIFFERENTIAL EARLY EXPERIENCE


IN THE DOG

BY M. W. FOX & D. STELZNER


Thudichum Psychiatric Research Laboratory, Galesburg State Research Hospital, Galesburg, lllino&

The effects of various experimental procedures tions have been made by Fox (1965a) on the
on behavioural development notably electro- development of socialization, effects of domestic-
shock, 'handling' or 'gentling' and cold exposure, ation and dog-human relationships in the dog.
instigated either prenatally (Thompson & Sontag, Considerable work in the past has been con-
1956) or at specific times postnatally have been ducted on the effects of early experience on per-
reviewed by Thompson & Schaeffer (1961), ception and sensory feedback, and it is now well
Denenberg (1962b) and Levine (1962b). A great recognized that subnormal stimulation may dis-
variety of stimuli have been employed, differing rupt discriminative and manipulative abilities
in modality and intensity thus differing in the (Nissen, Chow & Semmes, 1951; Held & Hein,
degree of stress exerted upon the organism and 1963) as well as deterioration of receptor organs
their effects on subsequent development. Post- (Riesen, 1961). Early handling also has a differ-
natal handling by giving a variety of stimuli ential effect on animals of different genetic
such as cold exposure or electro-shock for ex- background (King & Eleftheriou, 1959). Also
ample, during the neonatal period results in the age at which handling is undertaken can
animals that are more docile to handle, are less result in widely differing effects, suggesting that
emotional (Levine, 1957a) have superior learn- there are certain critical periods when treatment
ing abilities (Denenberg & Bell, 1960; Bernstein, has a maximal effect (Denenberg, 1962a), also
1957) and also have heavier adrenal glands, modified by the intensity of stimulation (Denen-
elevated corticosteroid levels (Levine, 1962a) berg & Kline, 1964).
and greater survival rates in stressful situations Paulson (1965) in a study of the development
(Bovard, 1954; Levine, 1957b). Handling (also of evoked responses to photic stimulation re-
termed 'gentling') early in life or prenatally ported that ducklings exposed to photic stimu-
(Denenberg, 1963) therefore may be regarded as lation prior to hatching showed more mature
a stress phenomenon that produces psycho- evoked potentials with shorter latencies than
physiologically superior animals which are non-exposed controls.
better able to resist physical stress and are less Meier (1961) reported that early handling of
susceptible to emotional disturbances and can Siamese kittens resulted in faster development
adapt better to novel situations. of mature EEG patterns and that the handled
Brain weights, cholinesterase levels, cortical cats were more docile and easier to handle than
thickness and learning abilities are significantly controls. White & Castle (1964) have shown that
greater in rats reared in an enriched environ- postnatal handling of human infants results in
ment (Levine & Alpert, 1959; Rosenzweig et al., superior exploratory behaviour over their con-
1962a, b; Bennet et al., 1964; Krech et al., 1962; trols who were institution reared subjects.
Tapp & Markowitz, 1963). In contrast to rearing Early social deprivation or isolation in phylo-
animals in social isolation, the development of genetically diverse species such as fish (Shaw,
social attachment (imprinting, Hess, 1959) 1962), rats (Griffiths, !961), chickens (Padilla,
may be modified by socializing the animal with 1935) and in the monkey can result in the emerg-
another species, usually to man or to related ence of a wide variety of behavioural deficits
species (Thorpe, 1958). Such selective social or abnormalities. In monkeys, stereotyped (e.g.
deprivation studies have shown how early ex- rocking) and autistic behaviour, inferior learn-
perience during the critical period can greatly ing abilities, fear of novel objects and unpre-
alter the establishment of primary social re- dictable emotional reactions to slight environ-
lationships among different animals such as the ment changes have been observed (Seay, Hansen
squirrel and lamb (Denniston, 1959; Scott, & Harlow, 1962; Berkson & Mason, 1964;
1958). Such altered socialization has been found Harlow & Harlow, 1962; Harlow et al., 1963,
to effect learning, fear responses, sexual be- 1964; Jensen & Tolman, 1962; Mason & Green,
haviour and social preference. Similar observa- 1962; Menzel, 1963; Sackett, Porter & Holmes,

273
274 ANIMAL BEHAVIOUR, 14, 2-3

1965). Dourth & Brown (1961), Casler (1961) total of 280 hr of handling). The handling pro-
and Bowlby (1951) have reviewed these problems cedures briefly consisted of 1 hr of stimulation
in relation to child development. daily, comprising 10 rain photic stimulation in a
Thompson & Heron (1954a, b) reared pups light and sound proof box, with a flashing light
in a restricted environment (partial social iso- stimulus at 0.16 intensity and approximately
lation) from 4 weeks to 7-10 months of age. 1 sec frequency; 10 min labyrinthine stimulation
These dogs were hyperactive (highly exploratory) consisting of 5 rain antero-posterior and 5 min
in novels situations and were less competent to bitemporal tilting at an approximate frequency
solve a simple maze problem. They also showed of 1.5 sec through an excursion of 45 ~ from the
diffuse reactions to novel stimuli which were horizontal; 10 min auditory stimulation, 2 rain
either avoided if menacing, or approached if each at 1, 10, 102 and 103 cycles/see at an in-
apparently inocuous, by control subjects. These tensity of 1.0 V and duration of 1.0 msec.
inappropriate responses to possibly noxious This was followed by 1 rain exposure in a cold
stimuli were thought to represent abnormal room at 37~ 5 min in a centrifugal rotator at
development of normal fear reactions and approximately 45 rev/min and 10 min handling
Melzack & Scott (1957) found that restricted during which time a series of reflexes were
dogs were unable to perceive and respond appro- evoked, including the Magnus, rooting, right-
priately (i.e. avoid) painful stimuli. Angermeir ing, geotaxic, pain and paniculus reflexes (Fox,
& James (1961) and Melzack (1962) have also 1964). By eliciting these reflexes, the rate of
reported the effects of early sensory deprivation reflex development could be assessed. The sub-
on later perception in the dog and Krushinski jects were then placed in a water bath at 80~
(1962) and Fuller (1964) in long-term studies on and given 15 sec total immersion during which
the effects of isolation on canine behaviour found time they would swim; this was done during the
that there were genetic differences in suscep- first 3 weeks of age. Subjects were then rubbed
tibility to the effects of isolation in the different dry on a hand towel and groomed with a soft
breeds studied. These studies in the effects of brush for 10 min and received 2 rain general
domestication on the development of social- cutaneous stimulation with an air jet (60~
ization in the dog have recently been discussed From 3 weeks of age onwards the handling
(Fox, 1965a). period was increased to include 10 rain play
Dogs reared under partial social isolation with the operator. After this handling period
between the ages of 4 and i6 weeks developed an they were returned to the mother. Control
'isolation syndrome', characterized by extreme subjects were kept under typical rearing con-
activity-reduction in the intensity of social con- ditions with the mother, having frequent
tacts and decreased manipulative behaviom" scheduled human contact at twice daily feeding
(Fuller, 1964). These results are of psychiatric and cleaning routines. All subjects were weighed
interest because the isolation syndrome dogs and heart rates recorded at weekly intervals
showed some symptoms similar to those of so- while the pup was lying quietly in the hands of
called autistic children. Fuller's data indicate the investigator. The pups were weaned at 4
that the events surrounding the emergence from weeks of age, received ?,-globulin and piperazine
social isolation are critical to the origin and anthelminthic, and were reared singly in meta-
persistence of the syndrome as a mass-fear bolism cages in the animal house environment.
response. The slow recovery from the syndrome At this time subjects for rearing in social iso-
does not indicate the time lag in the learning of lation were selected; these subjects had been
new responses, but rather the gradual removal of previously raised in the same manner as the
a rigid activity pattern of intense avoidance be- control animals. Social isolation subjects were
haviour. placed in a quiet darkened room, housed in
single cages and were fed and cleaned twice daily
Materials and Methods with minimal contact with the handler (approx-
This investigation was designed to determine imately 1.5 min daily). It was decided to rear
the effects of differential rearing on several these pups for only 1 week in social isolation
aspects of behaviour and development of the dog. (from 4 to 5 weeks of age) to compare with
A total of eight control, eight handled, and six observations of other workers who socially
partially socially isolated pups were used. isolated their subjects for much longer periods
Handling was carried out from the first day after weaning. It must be emphasized that social
after birth until 5 weeks of age (representing a isolation was only partial, for auditory and
FOX & STELZNER: EARLY EXPERIENCE IN THE DOG 275

olfactory stimuli from the subject and other response while the observer walked a r o u n d the
dogs in the isolation room were not eliminated, arena. The ability of the pup to negotiate a
as was the case in most earlier social isolation or simple wire mesh barrier placed between him
deprivation studies with dogs. Control and and the observer was next used to assess detour
handled subjects were reared in single cages in behaviour. Four trials were allowed and if the
the animal house environment and control animal was able to come around the barrier
subjects had approximately the same amount of to the observer, one end was blocked and if
human contact daily as the isolation group. At there was an end preference, the preferred side
5 weeks of age the subjects were tested singly in a was first blocked. The time taken to pass around
behaviour arena equipped with one-way win- the barrier and number of trials required were
dows to enable the experimenter to observe the recorded. Finally, the social interactions of these
animals without being seen. The arena con- differentially reared subjects was observed when
tained cloth bedding from the mother of the they were placed together in the arena which
pups and in another corner a brightly coloured still contained the cloth and toy. After 5 min
child's toy. The reactions of the subjects were observations the experimenter entered the arena
observed when first placed in the arena for 5 rain and observed the effects of the presence of a
and observations continued for a further 5 min human on the group behaviour of the pups.
after these objects had been removed. The After these behaviour observations EEG record-
objects were then replaced and a further 5 min ings were taken using scalp electrodes (modified
of observations were conducted. Two observers Mitchell wound clips), bifrontal and bioccipital
with stop watches independently recorded the on a Grass 6 channel recorder: E K G recordings
duration of certain activities of each pup were also taken. Recordings were taken while
throughout each of the three 5 min observation the animals were lying quietly awake and also
periods, and time scores were then averaged for asleep in a darkened room and were restrained
each group. The activities observed and time- in a copper-gauze box lined with foam rubber.
scored were as follows. Animals were then euthanatized and several
1. Specific interaction with stimulus. Duration organs dissected and weighed in the cold room
of interaction with either cloth or toy including at 37~ Brain and spinal cord were dissected
approach, play, chewing, licking, carrying and for amino acid, esterase and lipid analysis of
lying beside or running around the object was various parts and for histological examination,
recorded. and the adrenal glands were dissected out and
2. Non-specific exploratory. The time spent prepared for epinephrine and norepinephrine
exploring arena was recorded, including sniffing analysis, and specimens of kidney, liver, sciatic
and licking walls and floor and jmnping up at nerve and lumbar muscle removed for L D H
walls, looking up at walls (visual) and attention (lactic dehydrogenase) and protein analysis.
to extraneous noises (air-conditioner turned on Results
as sound blanket). During this activity period,
pup never approached cloth or toy. No significant differences in b o d y weight
3. Random activity. The time spent sitting or gain was observed in the different groups nor
pacing arena without any overt reaction to were significant differences in total brain weight
cloth or toy or attention toward walls, floor or observed.* When tested at 3 and 4 weeks of age
extraneous noises was recorded. for a variety of reflex tests employed to deter-
4. Distress vocalization. As a level of emo- mine the degree of neuro-ontogenetic matura-
tional arousal, the number of distressful yelps tion (Fox, 1964), no significant differences were
and duration of distress vocalization was re- observed. Some handled pups, however, showed
corded by one observer only while the other *Analysis of brain parts so far completed indicates
observer noted what else the pup was doing considerable differences between control and handled
(random or non-specific exploratory activities). pups as compared with the isolates. The latter group
were found to have significantly more GABA (glutamic
There was a high correlation between distress aminobutyric acid) and less glutamine, threonine and
vocalization and r a n d o m activity, and distress alanine, and marked differences in esterases. The average
vocalization and non-specific exploratory (jump- percentage of epinephrine per gland was found to be
ing up at walls). 63 • 9 per cent in the handled and 56 • 7 per cent
After this 15 rain testing period, the animal's in the controls, there being no change in the total amine
content of the adrenals due to handling but a significant
approach to a passive observer in the arena was increase in epinephrine. These findings will be reported
determined and then approach and following in greater detail at a later date.
276 ANIMAL BEHAVIOUR, 14, 2-3

slightly superior coordination while standing interference but showed great emotional arousal
and walking at 4 weeks. Histologic examination when first put into the arena. The social isola-
of motor, occipital and frontal cortex and tion subjects showed little emotional arousal
vestibular neurons revealed no marked differ- in all of the test situations. Control subjects
ences in cell density or neuron size. Heart rates reacted more to the cloth stimulus than to the
were recorded in the control and handled groups toy while handled and social isolation pups
only because resting heart rates were not possible were somewhat similar in their reactions to both
to take at 5 weeks of age in the social isolation cloth and toy. The time spent with these specific
reared pups as they were hyperactive and had object stimuli was contrasted by the random and
tachycardia. The marked differences between the nonspecific exploratory activity of the various
handled and control groups were apparent from subjects; random activity was characterized by
the second week of age onward (Fig. 1). N o r m - the pup running around the arena in an aimless
ally there is a decrease in heart rate from 2 weeks undirected fashion while nonspecific exploratory
of age onwards due in part to an increase in activity was seen when the subject would in-
vagal tone which was seen in the control sub- tently explore the floor, walls and door of the
jects but in the handled group, cardio-acceler- arena. Random activity was greatest in the
ation from 2 weeks of age onwards was seen and isolation groups while the control group showed
at 5 weeks the heart rate in all handled subjects a high level random activity when the stimulus
were greater by 60 beats/rain, indicative of specific objects were present in the arena. In
greater sympathetic tone. contrast the handled group showed increased
random activity when these specific stinmli were
removed. This increase in random activity in the
handled group when the arena is empty is cor-
related with the greater distress vocalization at

t~
~I
35
*'/
..... A.
""A
this time. Nonspecific exploratory activity was
greatest in the handled group when the cloth
and toy were in the arena but was greatest in the

f
30 control group when the arena was empty. This
increase in nonspecific activity in the control
group is associated with their high interaction
ua 25
:r. with the cloth when it is present in the arena;
control subjects were therefore stimulus bound
~_. I I
throughout and when the stimulus was removed
20
I 3 4 they showed an increase in nonspecific explor-
AGE IN WEEK5
atory behaviour (in contrast with the diffuse
Fig. 1. Heart rates of control and handled dogs. Contrast reactions of the isolates). The level of non-
normal decrease in heart rate in eight controls (0) specific exploratory activity in the social isolation
at 2 weeks (due to sudden increase in vagotonia) and group was similar in the three test situations and
increase in eight handled (Ak) subjects, indicative of when assessed with the total random activity
greater sympathetic tone. show the relative hyperactivity of this group.
Behavioural Observations In the barrier test situation the handled pups
Extreme differences were not found among performed best in that they required the least
individuals in the same group and this surprising number of trials to negotiate the detour while the
uniformity facilitated comparisons among the control pups reacted more slowly and showed
three differentially reared groups. Generally, distress vocalization in this situation (Table I).
the handled pups were hyperactive, highly ex- In the cofitrol group, therefore, emotional
ploratory, very sociable towards humans and arousal in this situation prejudiced problem
dominant in social situations (e.g. play) with solving ability. The isolation group in four out of
their peers. They also performed best in the six cases were unable to negotiate the barrier
problem solving tasks of the barrier tests (Table while two were able to solve the detour problem
I and Fig. 2). The handled subjects showed the but unlike other subjects did not come directly
greatest distress vocalization immediately after around to the observer but wandered off to-
the handler had entered the testing arena and ward the toy or cloth. They behaved similarly
removed the cloth and toy. In contrast the to the control pups in that they became hyper-
control subjects were little distressed by this active and would run along the barrier 'pushing'
FOX & STELZNER: EARLY EXPERIENCE IN THE DOG 277

Table I. Open-field Behaviour Tests in Differentially Reared Dogs


(Detour scores expressed as percentage of correct scores per side)
Isolation from 4 to 5 weeks, handling from birth to 5 weeks

Specific stimulus Exploratory Distress Detour success rates


Activities Random (non- (vocaliz-
Cloth Toy specific) ation) Side pref. R. closed L. closed
78 '0 37 "2 32 '5 152.3 27 "2
Rl'8
Control 68'0 232.0 2'3 41 '5 41 '5
8 L 2"3
76"0 7'4 34'0 182'6 10'0
52"5 38 "25 22'0 187.25 17-2
Rl'6
Handled 183,0 117.0 75"5 93.0 96.5
8 L 2"2
49"75 47'0 13,0 190'25 8"5
47"0 32"6 51.25 169"15 1"4
RI.I
Isolated 136.5 163.75 3"5 23.0 28.0
8 L 2"1
24"7 42"5 96.0 136.8 0.1

Underlined figures = observations when cloth and toy are removed from arena. All figures represent average time in
seconds during three 5 min test periods, in which arena is full, then specific stimuli removed and replaced after 5 rain.

400

350

300 I

2'50

~ 2o0

150
,,r

50

110 MIN I

Fig. 2. Total time activity scores of differentially reared pups. For de-
tails see text. Note extreme differences in activity and distress reactions
in handled and socially isolated subjects. Open columns = controls;
shaded columns = handled pups; solid columns = isolated pups.
with the nose, but in contrast, they were non- arena. The control subjects were the most sub-
vocal. In the social situation (group behaviour ordinate but would interact constantly with the
test) in all cases t h e h a n d l e d p u p s w e r e d o m i n a n t g r o u p a n d n o t leave t h e g r o u p in c o n t r a s t to the
d u r i n g p l a y a n d w e r e the first to leave t h e g r o u p isolation reared pups who would frequently
to a p p r o a c h t h e o b s e r v e r w h e n he e n t e r e d t h e leave the p l a y f u l g r o u p a n d either i n d u l g e in 'self
278 ANIMAL BEHAVIOUR, 14, 2-3

L.F . - - - ~ ~
R.O.--~

-44444444 4444
5 0 JJVTI 4
5EC

Fig. 3. Sleeping EEG of handled (left) and control (right) 5-week-old pups.
Greater amplitude in handled subjects indicative of greater maturation over
controls. Note bradycardia and arriaythmia in control EKG, characteristic of
normal pups of this age.

L. F. - - ~

50 ~ v ~
I SEE

Fig. 4. Awake EEG of handled (left), control (centre) and isolated (right) 5-week-old-pups. Note 'spindling'
activity associated with extreme arousal (alerting) in socially isolated pups.

play' (e.g. tail chasing) or approach the cloth or avoid the observer. In contrast the isolation
toy. During aggressive play-fighting the controls reared pups often showed passive avoidance
were most subordinant and the isolation pups behaviour (fearful crouching) while those that
were intermediate in that they would fight with did follow only did so for a short distance
the handled pups to a greater extent. In those and were easily diverted and would approach
litters where two handled pups were present in the cloth or toy as they came into the vicinity
the group it was observed that these subjects of these objects. Throughout the test procedures,
would frequently leave the group together and vocalization in the isolated group was at a very
explore the test arena and indulge in aggressive low level: socialization processes may therefore
play away from the control and isolated pups. be important in developing and reinforcing vocal
Approach behaviour towards the observer behaviour and distress vocalization.
standing in the arena (cloth and toys still present) EEG recordings were extremely difficult to
and following response as the observer walked take in the isolation pups. The recordings were
around the arena was greatest in handled pups. originally to be taken when the animals were in a
Control pups were slower to approach and similar behavioural state. To achieve this it was
follow but in no instances did any pup actively decided to record when the pups were lightly
FOX & STELZNER: EARLY EXPERIENCE IN THE DOG 279

asleep in the arms of the observer and could be pups showed the greatest attraction to man. The
aroused by a loud noise. SUccessful recordings isolation-reared pups in spite of being isolated
were obtained in all control and handled pups for such a short period of time at the early part
while in the isolation subjects, it was found of the critical period of socialization (which ex-
almost impossible to get good recordings. These tends from 3-~-to 12 weeks of age, Scott & Mar-
animals would not rest for one moment and were ston, 1950; Scott, 1962) behaved similarly to
constantly alert. Successful recordings were pups reared for much longer periods in social
obtained in two of these subjects while they were deprivation. They were hyperactive and showed
lying quietly awake. In general the EEG activity diffuse reactions to novel objects and paid more
of handled pups showed a great amplitude during attention to their physical environment than to
light sleep as compared with the control sub- their litter mates when tested in the group situ-
jects (Fig. 2). As amplitude increases with age it ation. They had the lowest emotional attach-
may be presumed to be an indication of greater ment or attraction for man and showed the most
maturity in the handled subjects. The EEG inferior problem solving abilities. The E E G of
recordings from the isolation pups showed that these isolation subjects resembled the recordings
there was great alerting activity with sym- obtained by Scherrer & Fourment (1964) in the
metrical spread throughout the frontal and rabbit, in that there was constant alerting char-
occipital regions of the brain characterized by a acteristic of the high level of behavioural
fast frequency activity not normally seen in the arousal. Similar to the observations of Fisher
alert EEG of the normally reared pup at this (1955) pups reared in social deprivation isolated
age. * themselves from the group and would play in a
solitary fashion (self play). It is interesting that
Discussion such profound changes in behaviour following
The observations obtained from the handled this short period of isolation results in similar
group of pups indicates that in this experiment symptoms to those described in pups reared for
handling caused increased adrenal activity (re- much longer periods in isolation. In contrast,
flected in the ontogeny of the heart rate and abnormal fear reactions and adaptive approach
adrenal percentage of norepinephrine at 5 and avoidance response were not observed in
weeks), confirming the observations by other these isolation subjects, whereas Fuller (1964)
workers on the effects of the early handling reported such abnormalities in pups isolated for
stimulation in the rat and mouse reviewed up to 16 weeks of age. This is to be expected
earlier in this paper. The only significant neuro- because by 5 weeks of age the approach be-
logic finding was slightly superior locomotor haviour is normally at maximum intensity and
ability and equilibratory coordination in the avoidance behaviour is poorly developed (Freed-
handled pups. We may surmise that reflex man, King & Elliot, 1961). Long term isolation
development in the dog normally proceeds at a (partial social deprivation) results in inappro-
maximal rate postnatally and was little affected priate avoidance or approach responses to novel
by the manipulations in this experiment. stimuli. On emergence from long term isolation,
However, the general behaviour and electro- exploratory behaviour is overshadowed by mass
cortical activity of the handling group compared avoidance behaviour and fear of novel stimuli.
with the control group showed marked differ- Long term isolation rearing therefore causes
ences in that the EEG was more mature and deficit in the establishment of fear responses and
handled animals showed similar changes in by 16 weeks of age the capacity for long lasting
their behaviour patterns as reported in handling fear responses is developed. There is also a lack
studies in other species. They performed of response to social stimuli (autistic) and in-
superiorly in the problem solving situation (the hibition of aggressive behaviour. In the present
barrier test) and showed less emotional arousal study it is conceivable that the effects of isola-
in this situation. In group behaviour the handled tion if extended over a longer period may be
pups were the dominant individuals and these made more permanent but as social isolation
9This spindling activity has been further confirmed in five was discontinued earlier on the critical period of
pups isolated from 4-5 weeks. Chronic electrodes were socialization, the effects are transient. Thus, early
implanted and gave superior recordings. The spindling plasticity affords greater adaptability.
phenomenon disappears 4-7 days after emergence from
isolation. Evoked responses to photic and auditory Summary
stimuli are also of shorter latency in isolates, indicating
intense arousal (data to be published). The effects of handling from birth to 5 weeks
280 ANIMAL BEHAVIOUR, 14, 2-3

a n d isolation from 4 to 5 weeks were studied Denenberg, V. H. & Bell, R. W. (1960). Criticial periods
in twenty-two dogs a n d contrasted with the for the effects of infantile experience on adult
learning. Science, N. Y., 131, 227-228.
b e h a v i o u r of control subjects raised u n d e r Denenberg, V. H. & Kline, J. N. (1964). Stimulus in-
nor~rlal rearing conditions. Differences in be- tensity versus critical periods: A test of two
haviour, heart rate a n d E E G activity were hypotheses concerning infantile stimulation. Can.
evident in the three differentially reared groups or. PsychoL, 18, 1-5.
of dogs and were attributed to the effects of Denniston, R. H. (1959). Escape and avoidance learning
h a n d l i n g a n d isolation in the experimental as a function of emotionality level in the Wyoming
Squirrel. Anim. Behav., 7, 241-247.
groups as compared to the control group. Dourth, L. & Brown, K. B. (1961). Inadequate mothering
Preliminary biochemical data (adrenal a n d C N S and disturbance in the neonatal period. ChiM
analysis) are included a n d some correlation in Dev., 32, 287-295.
the differentially reared groups is shown. These Fisher, A. E. (1955). The effects of differential early
data in part support similar findings in other treatment on the social and exploratory behavior
of puppies. Unpublished doctoral thesis. Penn-
species reviewed in this paper. sylvania State University.
Acknowledgments Fox, M. W. (1964). The ontogeny of behaviour and
neurologic responses in the dog. Anim. Behav.,
The authors wish to acknowledge the assist- 12, 301-310.
ance of M r J. Briggs a n d the facilities provided by Fox, M. W. (1965a). Canine Behavior. Springfield, Ill.:
the Galesburg State Research Hospital, and are C. C. Thomas.
Fox, M. W. (1965b). Psychosocial and clinical application
most grateful to D r WiUiamina A. Himwich for of the critical period hypothesis in the dog. J. Am.
advice a n d encouragement t h r o u g h o u t this study. vet. reed. Ass., 146, 1117-1119.
We are also indebted to Drs H. C. Agrawal a n d Freedman, D. G., King, J. A. & Elliot, O. (1961).
G. R. Pscheidt of this laboratory, and Professor Critical period in the social development of dogs.
Science, N.Y., 133, 1016-1017.
Jon K a b a r a of the University of Detroit for Fuller, J. L. (1964). Effects of experimental deprivation
preliminary biochemical data. Some of this data upon behavior in aninaals. Proc. Third World
together with a clinical o r i e n t a t i o n to the prob- Cong. Psychiatry, III, pp. 223-227. University of
lem of early experience were recently presented Toronto Press.
Griffiths, W. J., Jr. (1961). Effect of isolation on tredmilI
by the senior a u t h o r at the 20th A n n u a l Meeting, running in the albino rat. PsychoL Rep., 8, 243-
Society of Biological Psychiatry, New York, 250.
1965. Harlow, H. F. & Harlow, M. (1962). Social deprivation
in monkeys. Scient. Am., 207, 137-146.
REFERENCES Harlow, H. F., Harlow, M. K. & Hansen, E. W. (1963).
Angameier, E. & James, W. T. (1961). The influence of The maternal affectional system of rhesus monkeys.
early sensory-social deprivation on the social Maternal Behavior in Mammals (Ed. by H. O.
operant in dogs. aT.genet. PsychoL, 99, 153-158. Rheingold), chapter 8. New York: Wiley.
Bennett, E. L., Diamond, M. C., Rosenzweig, M. R. & Harlow, H. F. et al. (1964). The effect of total social de-
Krech, D. (1964). Chemical and anatomical privation on the development of monkey be-
plasticity of brain. Science, N. Y., 146, 610-619. havior. Psychiat. Res. Rep. Am. Psychiat. Ass,.
Berkson, G. & Mason, W. A. (1964). Stereotyped be- 19, 116-135.
haviors of chimpanzees: Relation to general Held, R. & Hein, A. (1963). Movement produced stimu-
arousal and alternative activities. Percept. Mot. lation in the development of visually guided
Skills, 19, 635-652. behavior. J. comp. physioL Psyehol., 56, 872-876.
Bernstein, L. (1957). The effects of variations in handling Hess, E. H. (1959). Imprinting. Science, N.Y., 130,
upon learning and retention. J. comp. physiol. 133-141.
Psychol., 50, 162-167. Jensen, G. D. & Tolman, C. W. (1962). Mother-infant
Bovard, E. W. (1954). A theory to account for the effects relationship in the monkey, Maeaca nemestrina:
of early handling on viability of the albino rat. The effect of brief separation and mother-infant
Science, N.Y., 120, 187. specificity. J. comp. physiol. Psychol., 55, 131-136.
Bowlby, J. L. (1951). Maternal care of mental health. King, J. A. & Eleftheriou, B. (1959). Effects of early
W.H.O. Monogr. No. 2. handling upon adult behavior in two sub-species
Casler, L. (1961). Maternal deprivation; a critical review of deermice, Peromyscus maniculatas. J. comp.
of the literature. Monogr. Soc. Res. Child Dev., physioL PsychoL, 52, 82-88.
26, 1-64. Krech, O., Rosenzweig, M. R. & Bennett, E. L. (1962).
Denenberg, V. H. (1962a). Critical periods in the rat. Relation between brain chemistry and problem
J. comp. physioL PsychoL, 55, 813. solving among rats raised in enriched and im-
Denenberg, V. H. (1962b). The effects of early experience. poverished environments. J. eomp. physiol.
The Behaviour of Domestic Animals (Ed. by E. S. E. PsychoL, 55, 801-807.
Hafez), pp. 109-138. London: Bailliere, Tindall & Krushinski, I. V. (1962). Animal Behavior. New York:
Cox. Consultant Bureau.
Denenberg, V. H. (1963). Behavior of adult rats is modi- Levine, S. (1957a). Infantile experience and consum-
fied by the experiences their mothers had as in- matory behavior in adulthood. J. comp. physioL
fants. Science, N.Y., 142, 1192-1193. PsychoL, 50, 609-612.
FOX & STELZNER: EARLY EXPERIENCE IN THE DOG 281

Levine, S. & Alpert, M. (1959). Differential maturation Levine, S. (1957b). Infantile experience and resistance to
of the CNS as a function of early experience. physiological stress. Science, N.Y., 126, 405.
Archs gen. Psychiat., 1, 403-405. Scherrer, J. & Fourment, A. (1964). Electrocortical
Mason, W. A. & Green, P. C. (1962). The effects of social effects of sensory deprivation during development.
restriction on the behavior of rhesus monkeys: Developing Brcdn, Vol. 9 of Progress in Brain
IV. Responses to a novel environment and to an Research (Ed. by W. A. Himwich and H. E.
alien species. J. comp. physiol. Psychol., 55, 363- Himwich), pp. 103-112. New York & Amsterdam:
368. Elsevier.
Meier, G. W. (1961). Infantile handling and development Scott, J. P. (1962). Critical periods in behavioral develop-
in Siamese kittens. J. comp. physioL PsychoL, 54, ment. Science, N.Y., 138, 3-12.
284-286. Scott, J. P. (1958). Animal Behavior. University of
Melzack, R. (1962). Effects of early perceptual restriction Chicago Press.
on simple visual discrimination. Science, N.Y., Scott, J. P. & Marston, M. V. (1950). Critical periods
137, 978-979. affecting normal and maladjustive social behavior
Melzack, R. & Scott, T. H. (1957). The effect of early in puppies. J. genet. Psychol., 77, 25-60.
experience on the response to pain. J. comp. Seay, B., Hansen, E. W. & Harlow, H. F. (1962). Mother-
physiol. PsychoL, 50, 155-161. infant separation in monkeys. Y. Child PsychoL
Menzel, E. W., Jr. (1963). The effects of cumulative Psychiat., 3, 123-132.
experience on responses to novel objects in young Shaw, E. (1962). Environmental conditions and the
isolation-reared chimpanzees. Behaviour, 21, 1-12. appearance of sexual behavior in the platyfish.
Nissen, H. W., Chow, K. L. & Semmes, J. (1951). Roots of Behavior (Ed. by E. L. Bliss). New York:
Effects of restricted opportunity for taetual kines- Harper.
thetic and manipulative experience on the be- Tapp, J. T. & Markowitz, H. (1963). Infant handling:
havior of chimpanzees. Am. J. PsychoL, 64, 485. Effects on avoidance learning, brain weight and
Padilla, S. G. (1935). Further studies on the delayed cholinesterase activity. Science, N.Y., 140, 486-
pecking of chicks. J. comp. PsychoL, 20, 413-443. 487.
Paulson, G. W. (1965). Maturation of evoked responses Thompson, W. D., Jr. & Sontag, L. W. (1956). Be-
in the duckling. Exp. NeuroL, 11, 324-333. havioral effects in the offspring of rats subjected
Riesen, A. H. (1961). Stimulation as a requirement for to audiogenic seizures during the gestation period.
growth and function in behavioural development. J. comp. physiol. Psychol., 49, 454-456.
Functions of Varied Experience (Ed. by D. W. Thompson, W. R. & Heron, W. (1954a). The effects of
Fiske and S. R. Maddi). Homewood, Ill. : Dorsey early learning on activity in dogs. J. comp. physiol.
Press. PsychoL, 47, 77-82.
Rosenzweig, M. R., Krech, D., Bennett, E. L. & Dia- Thompson, W. R. & Heron, W. (1954b). The effects of
mond, M. C. (1962a). Effects of environmental restricting early experience on the problem solving
complexity and training on brain chemistry and capacity of dogs. Can. J. PsychoL, 8, 17-31.
anatomy: a replication and extension. J. comp. Thompson, W. R. & Schaefer, T. (1961). Early envir-
physiol. Psyehol., 55, 429-437. onmental stimulation. Functions of Varied Ex-
Rosenzweig, M. R., Krech, D., Bennett, E. L. & Zolman, perience (Ed. by D. W. Fiske and S. R. Maddi).
J. F. (1962b). Variation in environmental com- Homewood, IlL : Dorsey Press.
plexity and brain measures. J. comp. physiol. Thorpe, W. H. (1958). The learning of song patterns by
PsychoL, 55, 1092-t095. birds with special reference to the song of the
Sackett, G. P., Porter, M. & Holmes, H. (1965). Choice chaffinch, Fringilta coelebs. Ibis, 100, 535-570.
behavior in Rhesus monkeys: Effect of stimulation White, B. H. & Castle, P. W. (1964). Visual exploratory
during the first month of life. Science, N.Y., 147, behavior following postnatal handling of human
304-306. infants. Percept. Mot. Skills, 18, 497-502.
Levine, S. (1962a). Plasma-free corticosteroid response Wiesel, T. N. & Hubel, D. H. (1963). Single-cell responses
to electric shock in rats stimulated in infancy. in striate cortex of kittens deprived of vision in
Science, N.Y., 135, 795. one eye. J. Neurophysiol., 26, 1002-1017.
Levine, S. (1962b). The psychophysiological effects of
early stimulation. Roots of Behavior (Ed. by E. (Received 21 June 1965, revised 21 January 1966;
Bliss), pp. 246-253. New York: Harper. Ms. number: A352)

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