INTERNATIONALLY SUPPORTED PROJECTS ON HUMAN ETHOLOGY AND EVOLUTIONARY PSYCHOLOGY IN NOVOSIBIRSK
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Olga Petrenko
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    Olga Petrenko

COMPONENTS OF EARLY MATERNAL ENVIRONMENT AFFECT GENETIC DETERMINED BEHAVIORAL CHARACTERISTICS.

Olga I. Petrenko

Institute Cytology & Genetics, Laboratory of Evolutionary genetics, Novosibirsk, Russia

Introduction

    Unlike the 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 them.
        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 genetics.

Materials and methods

        Two rat 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.

Results

  1. Characteristics of maternal behavior:
            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.
  2. 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.

        Also 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.

Discussion

        As one 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 catalepsy.

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.

References

  1. Barykina N.N., Chepkasov I.L., Alekhina T.A., Kolpakov V.G., 1983. Breeding of Wistar rats for predisposition to catalepsy. Genetika, 19: 2014-2021 (in Russian).
  2. Kolpakov et al., 1996. Some Genetic Animal Models for Comparative Psychology and Biological Psychiatry. Inst. of Cytol. and Genetics., Novosibirsk, pp. 172.
  3. Kolpakov V.G., Barykina N.N., Chuguy V.F., Alekhina T.A., 1999. Relationship between some forms of catalepsy in rats: an attempt of genetic analysis. Russian J. of Genetics, 35: 6, 807-810.
  4. Leon M., 1974. Maternal pheromone. Physiol. Behav., 13: 441-453.
  5. Leon M., Moltz H., 1971. Maternal pheromone: discrimination by preweaning albino rat. Physiol. Behav., 7: 265-267.
  6. McCarty R., Tong H., 1995. Development of hypertension in spontaneously hypertensive rats: role of milk electrolytes. Clin. Exptl. Pharmacol. Physiol., Suppl.1: S215-S217.
  7. Meaney M.J., 2001. Maternal care, gene expression and the transmission of individual differences in stress reactivity across generations. Ann. Rev. Neurosci., 24: 1161-1192.
  8. Myers M.M., Brunelli S.A, Squire J.M., Shindeldecker R.D., Hofer M.A., 1989. Maternal behaviour of SHR rats and its relationship to Offspring blood pressure. Developmental Psychobiology, 22 (1): 29-53.
  9. Ornstein K., Amir Sh., 1981. Pinch-induced catalepsy in mice. J. Comp. Physiol. Psychol., 95: 827-835.
  10. Suomi S.J., 1997. Early determinants of behavior: evidence from primate studies. Br. Med. Bull. 53, 170 - 184.