“Transgeneration Effects of Social Environment on Variations in Maternal Care and Behavioral Response to Novelty

Columbia University, Department of Psychology, New York, NY 10027, USA.
Behavioral Neuroscience (Impact Factor: 2.73). 04/2008; 121(6):1353-63. DOI: 10.1037/0735-7044.121.6.1353
Source: PubMed


Cross-fostering studies in the rat have illustrated the importance of the postnatal environment in mediating the transmission of maternal licking/grooming (LG) from mother to offspring. The authors addressed the question of how postweaning social conditions can alter the patterns of maternal behavior. Juvenile female offspring of high LG and low LG mothers were placed in either standard, enriched, or impoverished postweaning environments for 50 consecutive days and then mated and observed with their own litters. Analysis of LG behavior indicated that the effect of postweaning environment was dependent on the level of postnatal mother-infant interaction. Postweaning isolation reduced exploratory behavior, maternal LG, and oxytocin receptor binding in the offspring of high LG mothers, whereas social enrichment enhanced exploration, LG behavior, and oxytocin receptor binding of low LG offspring. These effects were also transmitted to the next generation of offspring. Thus, maternal LG and the neural mechanisms that regulate this behavior exhibited a high degree of plasticity in response to changes in environment both within and beyond the postnatal period, with implications for the transmission of behavioral response to novelty and maternal care across generations.

Full-text preview

Available from:
    • "This behaviour is stably transmitted between generations and cross-fostering studies show that the offspring inherit the behaviour from the nursing mother and not the biological mother (Champagne and Meaney, 2001). Such intergenerational transmission of maternal behaviour is seen in rodents (Francis et al., 1999a, Champagne and Meaney, 2007, Roth et al., 2009), primates (Fairbanks, 1989, Maestripieri, 2005) and humans, and may underlie adaptive changes in the HPA axis (Champagne and Meaney, 2001). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The prenatal and postnatal early-life periods are both dynamic and vulnerable windows for brain development. During these important neurodevelopmental phases, essential processes and structures are established. Exposure to adverse events that interfere with this critical sequence of events confers a high risk for the subsequent emergence of mental illness later in life. It is increasingly accepted that the gastrointestinal microbiota contributes substantially to shaping the development of the central nervous system. Conversely, several studies have shown that early-life events can also impact on this gut community. Due to the bidirectional communication between the gut and the brain, it is possible that aberrant situations affecting either organ in early life can impact on the other. Studies have now shown that deviations from the gold standard trajectory of gut microbiota establishment and development in early life can lead to not only disorders of the gastrointestinal tract but also complex metabolic and immune disorders. These are being extended to disorders of the central nervous system and understanding how the gut microbiome shapes brain and behavior during early life is an important new frontier in neuroscience.
    Neuroscience 10/2015; DOI:10.1016/j.neuroscience.2015.09.068 · 3.36 Impact Factor
    • "Although the machinery of empathy for recognizing distress may be genetically transmitted, the behavior of consoling others may possibly be culturally transmitted. For example, maternal behavior is often influenced by the early experience of being cared for by the mother and observing the maternal behaviors of others (Gonzalez et al. 2001; Champagne and Meaney 2007), although in mammals mothers may also take care of their offspring through instinct. In other words, consolation behavior may remain in the population even when consolation is costly because the behaviors of empathetic consolers are more likely to be transmitted culturally. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The replacement of Neanderthals by modern humans may possibly have been influenced by the different cultural transmission mechanisms of the two hominins. Since teaching is widespread in modern human societies, but extremely rare in animals, it may have played an important role in human cultural evolution. In modern humans, how and whom to teach may, in part, be transmitted culturally. Therefore, in this paper, I develop a cultural transmission model of teaching. I show that even when costly, teaching can evolve provided that teachers transmit their cultural traits more actively than non-teachers. Teaching is more likely to evolve when the cost of social learning is low relative to individual learning, social learning is accurate, the environment is stable, and the effect of teaching is extensive. Under certain conditions, two states, existence and non-existence of teaching in the population, are evolutionarily stable (bistable). When this happens, social learning is sometimes maintained by teaching under unstable environments where social learning cannot exist without teaching. Differences in subsistence strategy and group structure between Neanderthals and modern humans may have affected the evolution of the teaching behaviors of the two hominins.
    Learning Strategies and Cultural Evolution during the Palaeolithic, Edited by Alex Mesoudi, Kenichi Aoki, 05/2015: chapter 3: pages 23-33; Springer Japan., ISBN: 978-4-431-55362-5
  • Source
    • "Phenotypic modifications can be transmitted across generations through various mechanisms like parental behavior, transfer of physical substances, hormonal effects that influence gene expression, or epigenetic inheritance of environmental variation (West-Eberhard 2003; Jablonka and Lamb 2005; Badyaev 2005; Champagne and Meaney 2007). Parental behavior during the lactation period is rather unlikely to have caused the observed differences in phenotypes and reproductive strategy in this study because guinea pig young are born in a state of advanced maturation. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The prenatal social environment affects offspring development in most studied taxa with potentially lifelong consequences. To understand the adaptive significance of such maternal influences on offspring development, it is important to study their effects on fitness. In guinea pigs, social instability during pregnancy leads to delayed development of male offspring. This has been interpreted as an adaptation to high social densities, where young males need to queue for reproductive opportunities since they cannot out-compete older dominant males. The consequences for male reproductive success are, however, so far unknown. To study the effects of different prenatal social densities on offspring reproductive performance, we housed females individually or in small groups during late pregnancy. Offspring from both treatments were reared together in large groups until independence and thereafter housed in same-sex pairs of the same treatment. We then observed courtship, aggressive behavior, and reproductive success in a low-density context with one male from each treatment competing over access to two females. Sons born to individually housed females initiated more fights, had more social contacts, courted females more, and had a higher reproductive success than sons of group-housed females. Sons born to mothers experiencing low social densities before birth therefore perform better at low social group sizes, suggesting that male development may be adaptively adjusted to anticipated social densities, although performance under high densities still needs to be compared.
    Behavioral Ecology and Sociobiology 07/2014; 68(10). DOI:10.1007/s00265-014-1774-z · 2.35 Impact Factor
Show more