Variations in maternal care in the rat as a mediating influence for the effects of environment on development
Introduction
Despite the common assumption in both psychology and biology that parental behavior exerts a pervasive influence on phenotype, the ability to clearly establish such effects has been troublesome. The unambiguous demonstration of parental effects in mammals is thwarted by the absence of experimental models that can reliably distinguish parental effects that are nongenomic in nature from those associated with genetic transmission. The issues here concern the transmission of traits from parents to offspring. Ideally, we need to effectively describe the similarity between parent and offspring in the expression of a given trait, as well as the mechanism of transmission.
In mammalian species, experimental evidence for the role of maternal care is commonly derived from deprivation studies. Thus, in both primates and rodents, infants deprived of maternal care for extended periods of time exhibit dramatically increased fearfulness, inappropriate and often excessively aggressive patterns of social behavior, and impaired cognitive development (e.g., [1], [2], [3], [4]). The decreased mother–infant contact resulting from extended periods of maternal separation seems likely to be critical for the effects on development. But does this imply that under normal conditions maternal care actively contributes to the development of specific neural systems, or simply that the absence of the mother is so disruptive to pup physiology that it affects the development of these systems? If maternal care is indeed critical under normal conditions, then what are the relevant features of mother–pup interactions, and how do they influence neural development? Are variations in maternal behavior within a normal range a relevant source of individual differences in development? Could such variations serve as the basis for a nongenomic transmission of traits from parent to offspring?
One obvious approach to such questions is to simply examine the relationship between variations in maternal behavior under normal conditions and development of specific traits in the offspring. Indeed, within developmental psychology parental care has often been considered as a major influence over the development of the brain and behavior [4], [5]. In humans, however, evidence for the importance of parental care is often compromised by the inherently correlational nature of studies in child development. Similar issues prevail in the primate literature, where large-scale cross-fostering studies that could define the influence of infant-directed behaviors at a particular time in development are extremely difficult. The answer would seem to lie in the use of species with a shorter life span, where the potential consequences of variation in parent–offspring interactions could be examined within a far shorter time period. However, with the exception of the primate literature, maternal behavior in mammalian species has often been characterized as the stereotyped, invariant or “innate” behavior patterns in that emerge from the combination of endocrine signals associated with the later stages of pregnancy and the stimulus properties of the young. The assumption has been that animals are either maternal or not, and such conditions are defined by endocrine events and the presence of young. Indeed such endocrine signals are of unquestionable importance in triggering the onset of maternal behavior, and for many species they are obligatory events [6], [7], [8], [9], [10]. Likewise, stimuli derived from the neonates are a necessary feature of the conditions that support the expression of maternal care [7], [10]. But do these findings necessarily imply invariance?
Reports of individual differences in maternal behavior in several species would seem to contradict the idea that maternal behavior is necessarily the inevitable consequence of gestational hormones in combination with the presence of the young. In old world monkeys, for example, individual differences in maternal behavior are stable and are commonly transmitted from mother to daughter [11], [12]. However, while nonhuman primates offer a fascinating opportunity for the study of behavioral development, invasive studies that clearly establish causal relationships or the opportunity to study underlying mechanism are usually very difficult or virtually impossible. The question is whether we can readily identify reliable individual differences in a nonhuman species in which both experimental manipulations of rearing conditions and studies of mechanism are feasible.
In the studies reported here, we have expanded on the results of an earlier report of Myers et al. [13] describing naturally occurring variations in maternal behavior in the Long–Evans rats over the first week postpartum. The focus of both the previous and current report is on licking/grooming and arched-back nursing, two behaviors implicated in many aspects of developmental regulation in the rat (e.g., [13], [14]). As with the primates, such individual differences in maternal behavior are stable across litters and are reliably transmitted from mother to female offspring. We think that this model will prove useful in the study of the influence of maternal care on neural and behavioral development, in a species whose life span permits more definitive longitudinal analysis as well as greater potential for intervention. Finally, the development of such models also permits studies on the functional importance of parental effects on phenotype.
Section snippets
Subjects
Adult, Long–Evans rats derived from animals obtained from Charles River Canada (St. Constant, Quebec) were used in these studies. For most studies, the adult females used to characterize maternal behavior were born in our colony. However, in other cases, adult females were obtained directly from the breeder. These animals also served to replenish the colony. For all studies, females and their litters were the only animals housed in the colony room. Food and water was permitted ad libitum, and
Frequency distribution
Lactating female rats differ in their frequency of licking/grooming and arched-back nursing of pups over the first 6–8 days postpartum (Fig. 2a). We first examined the frequency distribution for these behaviors to determine whether mothers which exhibit high or low levels of these behaviors form distinct populations, or simply lie at opposite ends on a single, continuous population. To examine this question 115 females were mated, allowed to give birth and maternal behavior was observed over
Discussion
Blaffer-Hrdy [18] summarized evidence from several species for variation in maternal care. This work has clearly questioned the idea that maternal behavior emerges as an invariant property of the endocrine events accompanying pregnancy and parturition. In nonhuman primates, the amount of time mothers spend in physical contact with infants exhibits natural variation and this trait is transmitted to female offspring [12], [19]. Likewise, in macaques, there are stable individual differences in the
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