COMPONENTS OF EARLY MATERNAL ENVIRONMENT AFFECT GENETIC DETERMINED BEHAVIORAL CHARACTERISTICS.
Olga I. Petrenko
Institute Cytology & Genetics, Laboratory of Evolutionary
genetics, Novosibirsk, Russia
human behaviour genetics where there exists a strong tendency
to ascribe the parent-offspring similarity to the role of
common environment and the mode of rearing, the animal behaviour
genetics is much more tolerant to purely genetic interpretations
of such similarity. Yet there are some data that indicate
that here, too, the nature-nurture problem is not so simple.
There have been studies on the role of changes of maternal
environment during prenatal and early postnatal development
in animals, especially rodents.
These and some other data suggest
that changes of maternal environment, such as cross-fostering,
can specifically influence some genetically determined behavioural
characteristics and even correct certain inherited abnormalities.
Besides, the long-lasting effects of changes of maternal environment
make revise the traditional opinion about the predominance
of genetic factors and justify the question "Is it all in
the genes or not?". Recent investigations in physiology, behaviour,
and social status of cross-fostered rhesus monkeys have given
rise to ideas of a possible role of maternal environment in
the development of social behaviour (Suomi, 1997). It is therefore
interesting to study the effects of the early maternal environment
on possibly most various genetically determined features and
on some related pleiotropic effects of the genes that control
In the present work we studied
the influence of changes in maternal environment (in-fostering
and cross-fostering) on the expression of genetically determined
predisposition to a behavioural abnormality in whose investigation
we are engaged - increased cataleptic reaction - in rats.
Our interest in this type of reaction is determined by the
fact that we consider it to be a possible animal model of
biological background on which schizophrenia develops in man
(Kolpakov et al., 1996). Besides, irrespective of whether
catalepsy has a construct validity as a model of schizophrenic
predisposition, it is a mode of adaptation widespread in the
animal world and most probably homologous to certain biological
features of human psychophysiology. We believed therefore
that such a study would be useful from the viewpoint of behaviour
Materials and methods
strains - the strain GC bred from a Wistar stock for the predisposition
to catalepsy, and the control Wistar stock - were used in
the experiments (Barykina et al., 1983). The animals were
divided into 6 groups: 1) control Wistar females that fostered
their natural offspring (n = 8), 2) control GC females who
fostered their natural offspring (n = 10), 3) Wistar females
who fostered adopted Wistar pups (in-fostering, n = 4), 4)
GC females who fostered adopted GC pups ( in-fostering, n
= 8), 5) GC females who fostered adopted Wistar pups (cross-fostering,
n = 6) , and 6) Wistar females who fostered adopted GC rats
(cross-fostering, n = 6).
The natural and foster-mothers`
nursing behaviour items to be studied were borrowed from Myers
et al. (1989) with slight modifications and were as follows:
1) mother in or out of nest (including cases when pups were
found sleeping without mother), 2) mother licking or grooming
any pup, 3) mother eating or drinking, 4) mother walking,
and 5) mother rearing. Two observation sessions, at 9.00 a.m.
and 3.00 p.m., were carried out daily for 20 days, 10 observations
being made at each session.
At the age of 2 weeks, the pinch-induced
catalepsy was tested according to Ornstein, Amir (1981), by
means of lifting the animal by the skin of the scruff and
recording the total time of cataleptic immobility between
motor paroxysms during a 2-minute test.
In order to elucidate the influence
of the factors studied (genotype and/or type of fostering)
or of their interaction, the data were analyzed by means of
two-way ANOVA with genotype and type of fostering as individual
variables. Besides ANOVA, the significance of differences
between specific groups was estimated by Student t-test. The
coefficient of linear correlation between the frequency of
finding mother staying in nest and the duration of pinch-induced
catalepsy was calculated.
- Characteristics of maternal
As shown by ANOVA, the frequency
of blanket nursing was influenced by genotype, being higher
in Wistar than in GC females (F [1, 36]= 4.3, p < 0.04).
So was the passive nursing (F [1,36]= 18.18, p < 0.0001)
which was influenced also by the type of fostering (F [2,36]=4.17,
p < 0.015) with interaction between these factors (F[2,
36] = 4.19, p < 0.02), i.e. apart from the interstrain difference
in this parameter, there was a difference in reaction of
females of the two strains to cross-fostering: this factor
decreased the frequency of passive nursing in GC, but increased
it in Wistar females. There were no differences in arched
nursing or any statistically significant effect of the type
of fostering on this parameter. Mother eating and drinking
frequency depended on the genotype, being higher among GC
(F [1,36] = 9.76, p<0.0035) and on the type of fostering,
being higher among foster-mothers than among natural mothers
irrespective of the genotype (p< 0.05 for Wistar and p <
0.008 for GC females). Mothers` eating frequency was higher
in GC females fostering alien adopted pups than in GC dams
fostering their own offspring (p < 0.02).
The total number of cases when
mother was in nest throughout the 20-day observation period
was significantly larger for Wistar foster-mothers than
for natural GC mothers (F [1, 36] = 9.76, p < 0.005. Therein,
which is important, the frequency of mother staying in nest
was significantly (p < 0.05) higher in Wistar females fostering
adopted GC pups than in GC females fostering their own pups.
- Duration of pinch-catalepsy:
As demonstrated by ANOVA, there
is a significant effect of genotype (F[1,395]=5.42, p< 0.02)
and of the type of fostering (F[2,395]=6.34, p<0.0019).
Although ANOVA did not show a significant interaction between
the genotype and the type of fostering ( p <0.075 ), post
hoc comparisons confirmed that in Wistar-fostered GC rats
the duration of catalepsy was significantly shorter than
in GC rats fostered by their natural mothers (p < 0.01).
Wistar rats did not react significantly to either in-or
cross-fostering. It is noteworthy that cross-fostering resulted
in a diminution of interstrain differences.
a significant negative correlation (r = - 0.32, p< 0.00001)
was found between the frequency of mother staying in nest
and the duration of pinch-induced catalepsy.
can see, the expression of catalepsy seems to depend not only
on genetic predisposition as it was found by us before (Kolpakov
et al., 1999), but also on the maternal environment and can
be corrected to some extent by means of changing the latter.
Therein, since in-fostering did not influence the expression
of catalepsy, and since cross-fostering had a tendency to
produce on Wistar rats an effect opposite to that produced
on GC rats, one may conclude that the cause of cross-fostering-induced
change was not the very fact of replacement of the natural
mother by a foster-mother, but a specific influence of genotype
(and therefore phenotype) of the foster-mother, although the
mechanisms of this specificity are still obscure. It is noteworthy
that all the significant changes are observed almost only
in GC but not in Wistar rats. It appears therefore that the
animals of the GC rat strain are more sensitive to the changes
of the maternal environment than animals of the Wistar strain.
It has been demonstrated earlier
that in rats mother can affect the behavioural and physiological
development of pups through various clues including pheromones
(Leon, Moltz, 1971; Leon, 1974), milk yield (McCarty, Tong,
1995) and maternal behaviour (see Meaney, 2001). The maternal
behaviour is an essential part of ontogenetic niche in rats
till weaning and may be considered as an envelope of deploying
of their intrinsic genetic program throughout the first 20-30
days of life.
Since we were interested in the
possible effect of maternal behaviour on the expression of
catalepsy in cross-fostering, we tried to compare the elements
of behaviour of Wistar foster-mothers to those of natural
GC mothers. If one considers the overall experimental data,
one can see that cases of mother staying in nest with her
pups were significantly more frequent among Wistar females
nursing their own or adopted GC pups than among any group
of GC females. At the same time, behavioural characteristics
reflecting mothers` proneness to leave the nest and the pups
(eating, locomotion, lying or sitting without pups etc.) were
observed more often among GC mothers.
This makes one think that the
attenuation of cataleptic predisposition found in GC rats
nursed by Wistar foster-mothers may have been caused by the
fact that Wistar foster-mothers nursed their adopted GC pups
better than their natural mothers did, and it cannot be ruled
out that the predisposition to catalepsy includes elements
of anaclitic depression. The positive correlation between
the duration of cataleptic reaction and the litter size (r
= 0.63, p<0.0008 in Wistar and r = 0.31, p < 0.04 in GC) suggests
that one of the factors on which the duration of catalepsy
depends is the share of maternal care obtained by each pup:
the larger the litter, the less care each pup obtains, and
the longer the duration of catalepsy is. This hypothesis is
corroborated by the fact that Wistar foster-mothers spent
more time with adopted GC pups than natural GC mothers did,
and especially by the negative correlation between the frequency
of mothers found in nest and the duration of pinch-induced
The results of the given work
are published in the following papers:
Amstislavsky S.Ya., Alekhina T.A.,
Barykina N.N., Chuguy V.F., Petrenko O.I., Kolpakov V.G.,
2001. Effects of change of maternal environment during early
postnatal development on behaviour in cataleptic rats. Behav.
Processes, 56: 41-47.
Kolpakov VG, Alekhina TA, Barykina
NN, Chugui VF, Petrenko OI, Amstislavskii. 2002, Effect of
changes in the early maternal environment on predisposition
to catalepsy in rats of different agesū (in Russian). Zh Vyssh
Nerv Deiat Im I P Pavlova, Mar-Apr;52(2):255-60.
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Alekhina T.A., Kolpakov V.G., 1983. Breeding of Wistar rats
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forms of catalepsy in rats: an attempt of genetic analysis.
Russian J. of Genetics, 35: 6, 807-810.
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