“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.

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    • "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. "
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    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.
    Full-text · Chapter · May 2015
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    • "Also after birth the newborn remains very sensitive to the (positive or negative) action of the environment. Given the primary source of environmental stimulation is represented by the mother, pup's post-natal development is mainly sculptured by maternal care (Francis and Meaney, 1999; Meaney, 2001; Macrì and Wurbel, 2006; Champagne and Meaney, 2007; Rosenfeld and Weller, 2012). Notably, maternal care may be in turn altered by the environmental factors experienced by the mothers. "
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    ABSTRACT: Environmental enrichment (EE) is a widely used paradigm for investigating the influence of complex stimulations on brain and behavior. Here we examined whether pre-reproductive exposure to EE of female rats may influence their maternal care and offspring cognitive performances. To this aim, from weaning to breeding age enriched females (EF) were reared in enriched environments. Females reared in standard conditions were used as controls. At 2.5 months of age all females were mated and reared in standard conditions with their offspring. Maternal care behaviors and nesting activity were assessed in lactating dams. Their male pups were also behaviorally evaluated at different post-natal days (pnd). Brain BDNF, reelin and adult hippocampal neurogenesis levels were measured as biochemical correlates of neuroplasticity. EF showed more complex maternal care than controls due to their higher levels of licking, crouching and nest building activities. Moreover, their offspring showed higher discriminative (maternal odor preference T-maze, pnd 10) and spatial (Morris Water Maze, pnd 45; Open Field with objects, pnd 55) performances, with no differences in social abilities (Sociability test, pnd 35), in comparison to controls. BDNF levels were increased in EF frontal cortex at pups’ weaning and in their offspring hippocampus at pnd 21 and 55. No differences in offspring reelin and adult hippocampal neurogenesis levels were found. In conclusion, our study indicates that pre-reproductive maternal enrichment positively influences female rats’ maternal care and cognitive development of their offspring, demonstrating thus a transgenerational transmission of EE benefits linked to enhanced BDNF-induced neuroplasticity.
    Full-text · Article · Mar 2015 · Frontiers in Behavioral Neuroscience
    • "PCS induces changes in postnatal maternal care, that effects behavioral and neuronal development in the offspring. Such a behavioral transmission has been shown in a number of studies focusing on variations in maternal care during early life periods (Weaver et al. 2004;Champagne 2008;Champagne and Curley 2009;Champagne and Meaney 2007). However, in our study a strict behavioral transmission appears unlikely, since in similar experiments we have recently shown that changes in the brain of PCS offspring are already evident at birth and similar to those in the adult offspring, suggesting that such changes are not due to altered maternal nurturing (Zaidan et al. 2013). "
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    ABSTRACT: Perinatal adverse experience programs social and emotional behavioral traits and is a major risk factor for the development of behavioral and psychiatric disorders. Little information is available on how adversity to the mother prior to her first pregnancy (preconception stress, PCS) may affect brain structural development, which may underlie behavioral dysfunction in the offspring. Moreover, little is known about possible sex-dependent consequences of PCS in the offspring. This study examined spine number/density and dendritic length/complexity of layer II/III pyramidal neurons in the anterior cingulate (ACd), prelimbic/infralimbic (PL/IL) and orbitofrontal cortex (OFC) of male and female rats born to mothers exposed to unpredictable variable stress at different time points prior to reproduction. Our main findings are that in line with our hypothesis adversity to the mother before her pregnancy results in highly complex changes in neuronal morphology in the medial prefrontal, but not in the orbitofrontal cortical regions of her future offspring that persist into adulthood. Moreover, our study revealed that (1) in the PCS2 group (offspring of dams mated two weeks after stress) spine numbers and dendritic length and complexity were increased in response to PCS in the ACd and PL/IL, (2) these regional effects depended on the temporal proximity of adversity and conception, (3) in the ACd of the PCS2 group only males and the left hemispheres were affected. We speculate that these transgenerational brain structural changes are mediated by stress-induced epigenetic (re)programming of future gene activity in the oocyte.
    No preview · Article · Nov 2014 · Brain Structure and Function
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