Chapter 5 – Epigenetic Trauma Inheritance

This is a portion of Chapter 5 from the book RootEd: How Trauma Impacts Learning and Society

 

Chapter 5

The Epigenetic Factor’s Role in Education

Implications in Education

Epigenetic inheritance is the term defined by Lawrence V. Harper, professor of human development at University of California, Davis, as “the transmission to offspring of parental phenotypic responses to environmental challenges—even when the young do not experience the challenges themselves. Genetic inheritance is not altered, gene expression is” (Harper, 2005, p. 340). Epigenetics, therefore, operates like a light switch. Since all cells in the human body contain identical genetic potential, the differentiating factor is which segments of the genetic code are expressed in each tissue. Certain genes within each cell are turned on or off which can then be passed to further generations without changes in the DNA sequence. Harper also suggests that the light switch in DNA expression may be triggered by environmental stimuli which will affect the genetic expression physically or for behaviors in this lifetime and those of future generations (Harper, 2005). Evolution, therefore, plays a large role in the understanding of epigenetics. In theory, a phenotypic alteration in gene expression, which is an adaptation to environmental demands, would increase the chances of survival. This survival expression would naturally be passed down to future generations to ensure the continuation of the species.

The recent discovery of epigenetics has scientists reeling at the possible implications. Epigenetics suggests that traumatic events that have occurred to our ancestors are currently impacting our lives today (Alder, Fink, Bitzer, Hosli, & Holzgreve, 2007; Bird, 2007; Campbell, Marriott, Nahmias, & MacQueen, 2004; Cerqueira, Pego, Taipa, Bessa, Almeida, & Sousa, 2005; Cole, Hawkley, Arevalo, Sung, Rose, & Cacioppo, 2007; Dalton, Nacewicz, Alexander, & Davidson, 2007; Dalton, Nacewicz, Johnstone, Schaefer, Gernsbacher, Goldsmith, Davidson, 2005; DiPietro, 2009; Fales, Barch, Rundle, Mintun, Snyder, Cohen, Sheline, 2008; Ganzel, Kim, Glover, & Temple, 2008; Ganzel, Morris, Wethington, 2010; Gianaros, Jennings, Sheu, Greer, Kuller, & Matthews, 2007; Groome, Swiber, Bentz, Holland, & Atterbury, 1995; Harper, 2005; Jablonka & Lamb, 1995; Jablonka & Raz, 2009; Kaati, Bygren, & Edvinsson, 2002; Kessler, R., Sonnega, Bromet, Hughes, & Nelson, 1995; Masterpasqua, 2009; McGowan, Sasaki, D’Alessio, Dymov, Labonte, Szyf, J., et al., 2009; Meaney, 2001; Meaney, 2004; Meaney, Szyf, & Seckl, 2007; Mennes, Van den Bergh, Lagae, & Stiers, 2009; Mill & Petronis, 2008; Moffitt, Caspi & Rutter, 2006; Oberlander, Weinberg, Papsdorf, Grunau, Misri, & Devlin, 2008; Pray, 2006; Richards, 2006; Susser, Hoek, & Brown, 1998; Szyf, McGowan, & Meaney, 2008; Van den Bergh, 2010; Weaver, Cervoni, Champagne, D’Alessio, Sharma, Seckl, Meaney, 2004; Yehuda, Bierer, Schmeidler, Aferiat, Breslau, & Dolan, 2000; ). The research is currently focusing on diseases, and implications in psychological development is now being considered. I would like to consider the implications of this in education.

Students who statistically succeed utilizing standardized examinations have historically been of Asian or Caucasian descent (National Assessment of Educational Progress data, 2007, http://nces.ed.gov/programs/digest/d08/tables/dt08_116.asp?referrer=list ). Those who have statistically fared less successful are often African and First Nations students (among other recent historically tribal cultures). I would like to offer a theory which may influence our current approach to school reform. I begin with understanding the suggestion of epigenetics playing a role in their learning styles.

Epigenetics suggest that traumatic events turn the genetic switch so that future generations are able to handle similar circumstances more effectively than their ancestors. Traumatic events can include anything from famine to war. Isolating two specific cultures, the African and First Nations peoples have similar traumatic experience here in the United States. One group was forced to leave their homeland and forced into slavery, the other was encroached upon and many of their people were annihilated. Both groups were forced to attend boarding schools in America. Both were expected to forget their roots and adapt to the new European settler’s way of life. The children were removed from their homes and tribes and were forced into boarding schools that stripped them of their culture, their language, and their way of life. I believe that this common traumatic experience may epigenetically affect their learning today.

It could be suggested that these two cultures have an epigenetically instinctual resistance to the culture who subjected their ancestors to such trauma. Another factor to consider is that their indigenous pre-colonized way of life is still epigenetically ingrained in who they are. Their pre-colonized existence was often not ecologically or environmentally destructive (Lewis, 1995). The industrialized compulsory education machine that took over their lives in the mid-1800’s is very contradictory to their deeply rooted philosophies on co-existence with nature. The goal of the original compulsory schools was to create factory workers for the industrial revolution. This industrial revolution contributed greatly to many incredible inventions. It also contributed greatly to massive destruction and pollution of our earth. I believe the African and First Nations peoples’ deeply ingrained epigenetic instinct, from thousands of years of tribal life that respected the earth, could definitely play a role in their instinctive resistance to our factory model education system. The way that they educated their young pre-colonization is also another epigenetic factor to consider.

My assertion is that the field of epigenetics, discovering that what our ancestors did and the way that they did it, has implications for students in the classroom. What our ancestors experienced, for example, in terms of famines or other life-threatening scenarios, is passed on to their descendants through their genes. This discovery lends itself to investigate the possibility of epigenetics influencing why some learners of non-Western European descent could possibly be having trouble in a Western-style classroom: it’s not the way their ancestors learned. In fact, from a non-Western point of view, it would be easy to see the current Western-style educational system as oppressive. I define oppressive education as the debilitation of the students’ ability to acquire the skills necessary for them to develop their highest self expression and become a contributing member of society.

Epigenetics: Adaptation to Western Educational Methods

The study of epigenetics is actually not new, it was first suggested a millennia ago. The earliest extant discussion was by ancient Greek philosophers. The idea gained popularity again with Alfred Russell Wallace when he and Darwin discussed the concept of evolution by natural selection in 1859. Before Darwin, Lamarck addressed the idea in earnest only to be challenged by Weismann in 1880. Prior to the 1990’s, the scientific community consistently rejected the theory as its ability to analyze the genome and gene expression did not arrive until later (Wallace, 1893; Joffe 1969; Jablonka & Raz, 2009; Rakyan & Beck, 2006). In terms of a definition, epigenetics, as defined by Bird, is “the structural adaptation of chromosomal regions so as to register, signal or perpetuate altered activity states” (Bird, 2007, p. 398). This includes environmental impacts on genetic expression. It is important to understand that the DNA structure itself is not altered, it is the expression of the gene that changes and sometimes to varying degrees (Harper, 2005; Pray, 2006). In some cases, the expression is even silenced, also known as methylation (Harper, 2005; Pray, 2006; Ganzel, Morris, & Wethington, 2010).

As stated previously, epigenetics operates like a light switch. Since all cells in the human body contain identical genetic potential, the differentiating factor is which segments of the genetic code are expressed in each tissue. Certain genes within each cell are turned on or off which can then be passed to further generations without changes in the DNA sequence. Harper also suggests, as mentioned previously, that the light switch in DNA expression may be triggered by environmental stimuli which will affect the genetic expression physically or for behaviors in this lifetime and those of future generations (Harper, 2005).

Evolution, therefore, plays a large role in the understanding of epigenetics. In theory, a phenotypic alteration in gene expression, which is an adaptation to environmental demands, would increase the chances of survival. This survival expression would naturally be passed down to future generations to ensure the continuation of the species. Jablonca and Lamb (1995) have reviewed a large body of evidence showing that, from protozoa to mammals, selection has indeed favored the intergenerational transmission of modifications in gene expression. The genome itself is not altered; the degree of expression of inherited potentials for tracking an environment is influenced by events impinging on the parent. The evidence indicates that when certain aspects of an individual’s inherited range of reaction are expressed in response to events in the environment, the resulting epigenetic states may be transmitted, not just to daughter cells in that individual, but across generations (see also Rossiter, 1996) (Harper, 2005).

Until the discovery of epigenetics, research on evolutionary genetics focused on random DNA mutations. In the light of epigenetics, however, this theory no longer has any basis for merit. The concept of epigenetics influencing human evolution provides a clearer understanding of observed changes in DNA expression. Lamarck suggested that the human body would adapt to the conditions it was living in. This trait could then be passed down inter-generationally, providing a supporting idea for the evolutionary theory of Darwin. The theory goes that if an organ or appendage is used more or less, that strengthening or weakening of the organ or appendage would be passed down to future generations. As an example from our own personal experience, modern humans have body parts (appendix, wisdom teeth, etc.) that are no longer serving a function, yet we still have them in our bodies.

There is now substantial research demonstrating that alterations in the epigenetic patterns surrounding DNA plays an essential role in the normal development of human beings, as well as in the etiology of a number of diseases. These patterns are dynamic within the life span of the individual, may be influenced by experience, and, in some instances, may be transferred to subsequent generations. While epigenetic inheritance across more than one generation has been observed in mice exposed to prenatal chemical and nutritional changes, the evidence for trans-generational effects in humans, although suggestive, has yet to be corroborated by controlled studies. Nevertheless, these results suggest that the consequences of an individual’s lifestyle may extend beyond their own mortality to include their descendants (Masterpasqua, F., 2009). In our current psychological view, behavioral development of individuals is perceived as the direct result of genetics, culture, and parental practices (nature and nurture). We now have epigenetic inheritance as an additional contributor.

While the Human Genome Project provided a complete map of the DNA sequence, it was not designed to take into account gene expression. One of these researchers, Masterpasqua, expressed “epigenetics is defined as mechanisms of gene expression that can be maintained across cell divisions, and thus the life of the organism, without changing the DNA sequence” (Masterpasqua, 2009, p. 194). This research has provided us with the understanding of how epigenetics influences the physical and psychological development of multiple generations of descendants. The implications of this, how environmental and psychosocial factors are changing the epigenome, provide us with suggestions of monumental significance. (Masterpasqua, 2009). These implications not only create new perspectives on the treatment of physical and behavioral disorders, but suggest new areas of exploration as we realize that the results of our current choices as well as our responses to environmental impacts that are carried into the future by our very genes, outliving one body and carrying on in the next.

Epigenetics: Survival

The research on epigenetic inheritance is beginning to demonstrate that changes in gene expression are especially evident during repetitively traumatic environmental experiences, like cycles of famine. These occurrences do not necessarily have to happen in one singular lifetime, but if they occur repeatedly in future generations, are unpredictable, and uncontrollable by the affected persons, then they tend to be highly likely to be epigenetically passed down. Situations involving famine or forcible subjugation are prominent areas where changes in gene expression are created. Such circumstances can create intergenerational epigenetically inherited changes in phenotypic response. The traumatic circumstances do not have to be present in those future generations for this genetic expression to continue to occur. The number of generations affected can be numerous before the phenotypic gene expression reverts to its original state prior to the traumatic experience (Jablonca & Lamb, 1995; e.g., Zamenhof, vanMarthens & Grael, 1971; e.g., Lumey & Stein, 1997; Szyf et al., 2008).

Key factors that contribute to generational changes in phenotypic response include the severity of the environmental threat, how unpredictable it is and the variability of the threat. The individual needs to be able to develop a reliable response to a detectable cue which reduces the opportunity for injury and therefore increases chances for survival. This form of defense becomes an anticipated response prior to the imminent reality of the threat. This ultimately mitigates a more damaging experience than if it were inspired during or after a materialized trauma (Harvell and Tollrain, 1999).

Epigenetics: Pain Memory

Newer scientific studies are focusing on how the emotional state of a pregnant woman could impact the genomic expression of her child. Most of the research focuses on behavioral disorders thought to be generated by the mother’s negative emotional states. It is now fair to suggest that the emotional fight or flight experience of the mother can influence genetic expression in the child’s developing brain. This does not necessarily have to suggest a behavior disorder, but more importantly an instinctive response to certain circumstances (e.g., DiPietro, 2009; Groome, Swiber, Bentz, Holland, & Atterbury, 1995; Sjöström, Valentin, Thelin, & Marsal, 2002; Van den Bergh, 1990, 1992; Van den Bergh, Mulder, Visser, Poelmann-Weesjes, Bekedam et al., 1989; for reviews, see Alder, Fink, Bitzer, Hosli, & Holzgreve 2007; Mennes, Van den Bergh, Lagae, & Stiers, 2009; Talge, Neal, & Glover, 2007; Van den Bergh, Mulder, Mennes, & Glover, 2005; Van den Bergh, Van Calster, Smits, Van Huffel, & Lagae, 2008; Weinstock, 2008; Meaney, Szyf, & Seckl, 2007).

Just as convincing is the research on the parenting style of a parent who was traumatized as a child. The abuse experienced by the parent also impacts the emotional development of their child, who does not experience the trauma the parent did. Studies have shown that adult children of Holocaust survivors have greater instances of Post Traumatic Stress Syndrome than their parents. In fact, these studies have demonstrated that the children of these Holocaust survivors have a higher incidence of PTSD and other mood and anxiety disorders than other demographically similar persons (Yehuda, Bierer, Schmeidler, Aferiat, Breslau, & Dolan, 2000).

As mentioned, one potential mechanism for the increased prevalence of mood and anxiety disorders is altered HPA axis physiology. Children of Holocaust survivors have significantly lower 24-h urinary cortisol secretion when compared with control participants, and off- spring of holocaust-surviving parents with PTSD had lower cortisol levels than offspring of Holocaust survivors that did not manifest PTSD (Yehuda et al., 2000). In addition, adult children of Holocaust survivors who manifested PTSD exhibit enhanced cortisol negative feedback inhibition in response to a dexamethasone suppression test (DST; Yehuda, Blair, Labinsky, & Bierer, 2007). Collectively, these data demonstrate that abuse can alter HPA axis activity and risk of psychiatric disorder at least one generation removed from the trauma exposure (Neigh, Gillespie, & Nemeroff, 2009).

Michael Meaney and his colleagues have done extensive research using animal models of parenting. The parenting itself impacts both the neural development and gene expression of the young with that parental model being passed down through generations of youth by epigenetic inheritance (Meaney, 2001). Another recent study provided potential evidence of a specific type of gene expression in the brains of people who committed suicide. The difference was found systematically to be dependent upon the abuse experienced in the subjects’ childhoods (McGowan et al., 2009).

In the physical context, experiences such as famine can affect the physical health of future generations. A study was done in 1997 that focused on the famine which occurred during World War II in the Netherlands. Thanks to detailed records that were collected during this period of time, researchers were able to trace the long-term and intergenerational transmission of the effects of the trauma of famine experienced perinatally. The traits that were passed down to the grandchildren included “low birth weight, infant mortality, obesity, diabetes, coronary heart disease, cancer, and increased rates of schizophrenia and diagnoses of schizoid personality disorder in the exposed group” (Lumey & Stein, 1997).

Other studies were completed in 2002 and 2006 which focused on harvest and food price records to see if food availability in 1890, 1905 and 1920, in a small Swedish town, had any influence on future mortality rates. What they discovered was that the effects continued through two generations. Sex-specific reactions were also identified. What the paternal grandfathers experienced affected only the grandsons and the same gender specific result was found in the women. These researchers’ findings add a new, multigenerational dimension to the interplay between inheritance and environment in health and development; they provide proof of principle that sex-specific, male-line trans-generational effects exist in humans (Pembrey et al., 2006).

While epigenetic research is still ongoing, it is becoming more and more crucial in various universities and medical research facilities. There is sure to be much more discussion in the future regarding the impact that epigenetics plays on our daily living experiences, life expectancies, parenting practices, and how such knowledge can very easily be transferred into areas of focus such as education. Clearly this is a complex area of research that involves much more than mere genetic science. As we have seen, the experience of our parents as well as of the lives before us impacts both our physical and mental health today, while our experiences will impact the lives of generations to come. This brings me to the question I propose to address: How can epigenetic theories support a call for education reforms based on traditional Indigenous approaches to teaching and learning, especially for students with relatively recent tribal ancestry?

Current educational reform focuses on standardized examinations, rote memorization, fact regurgitation and does not promote self-discovery, connection to the earth and all living beings or intrinsic motivation. This focus perpetuates the cycle of consumerism in our world and destroys the cultural understandings and ways of living for indigenous peoples. There is an imbalance occurring that is literally consuming our planet. Adding the concept of epigenetic influence on educational outcomes adds to the concern. The epigenetic phenomenon may be causing two problems:

  • Those whose tribal ancestry is still serving in their gene expression will continue to “fail” according to maladaptive systems and suffer accordingly.
  • Those who are adapting will likely pass on genes that continue to promote the maladaptations that are causing our world to be out of balance.

For those who are experiencing stronger epigenetic influence counter to Western educational theories, success will remain fleeting. Classroom behavior may represent instinctual resistance to authoritarian structure based upon epigenetic pain memory or due to the inherent knowledge that the disconnect from the earth and their authentic self may very well lead to the destruction of the planet or themselves. True understanding of their culture, their ways of learning and teaching, and respecting their belief systems are necessary in order for true educational reform to find success. Not only is understanding necessary, action involving their historic learning and knowing methodologies are crucial. For those who are adapting to the Westernized education system, they will lose their instinctual indigenous knowledge which in turn will perpetuate the imbalance occurring on our planet today. Our world will also lose the knowledge that only they possess. Current educational reform represents a psychological holocaust for these cultures.

 

References:

Alder, J., Fink, N., Bitzer, J., Hosli, I., & Holzgreve, W. (2007). Depression and anxiety during pregnancy: A risk factor for obstetric, fetal and neonatal outcome? A critical review of the literature. Journal of Maternal– Fetal and Neonatal Medicine, 20, 189–209.

Bird, A. (2007). Perceptions of epigenetics. Nature, 447, 396–398.

Campbell, S., Marriott, M., Nahmias, C., & MacQueen, G. M. (2004). Lower hippocampal volume in patients suffering from depression: A meta-analysis. American Journal of Psychiatry, 161, 598–607.

Cerqueira, J. J., Pego, J. M., Taipa, R., Bessa, J. M., Almeida, O. F. X., & Sousa, N. (2005). Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. Journal of Neuroscience, 25, 7792–7800.

Cole, S. W., Hawkley, L. C., Arevalo, J. M., Sung, C. Y., Rose, R. M., & Cacioppo, J. T. (2007). Social regulation of gene expression in human leukocytes. Genome Biology, 8, R189.1–R189.13.

Dalton, K. M., Nacewicz, B. M., Alexander, A. L., & Davidson, R. J. (2007). Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry, 61, 512–520.

Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., Davidson, R. J. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8, 519–526.

DiPietro, J. A. (2009). Psychological and psychophysiological considerations on the maternal–fetal relationship. Infant & Child Development, DOI: 10.1002/icd.651.

Fales, C. L., Barch, D. M., Rundle, M. M., Mintun, M. A., Snyder, A. Z., Cohen, J. D., Sheline, Y. I. (2008). Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biological Psychiatry, 63, 377–384.

Ganzel, B., Kim, P., Glover, G., & Temple, E. (2008). Resilience after 9/11: Multimodal neuroimaging evidence for stress-related change in the healthy adult brain. NeuroImage, 40, 788–795.

Ganzel, B. L., Morris, P. A., & Wethington, E. (2010). Allostasis and the human brain: Integrating models of stress from the social and life sciences. Psychological Review, 117(1), 134–174. http://doi.org/10.1037/a0017773

Gianaros, P. J., Jennings, J. R., Sheu, L. K., Greer, P. J., Kuller, L. H., & Matthews, K. A. (2007). Prospective reports of chronic life stress predict decreased grey matter volume in the hippocampus. NeuroImage, 35, 795– 803.

Groome, L. J., Swiber, M. J., Bentz, L. S., Holland, S. B., & Atterbury, J. L. (1995). Maternal anxiety during pregnancy: Effect on fetal behavior at 38 and 40 weeks of gestation. Journal of Developmental and Behavioral Pediatrics, 16, 391–396.

Harper, L.V. (2005). Epigenetic inheritance and the intergenerational transfer of experience. University of California, Davis: Psychological Bulletin vol. 131, no. 3, 340-360. American Psychological Association.

Jablonka, E., & Lamb, M. J. (1995). Epigenetic inheritance and evolution. Oxford, England: Oxford University Press.

Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology, 84, 131–176.

Joffe, J. M. (1969). Prenatal determinants of behaviour. In H. J. Eysenck (General ed.) International series of monographs in experimental psychology (Vol. 7). Oxford: Pergamon.

Kaati, G., Bygren, L. O., & Edvinsson, S. (2002). Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. European Journal of Human Genetics, 10, 682– 688.

Kessler, R., Sonnega, A., Bromet, E., Hughes, M., & Nelson, C. (1995). Post-traumatic stress disorder in the National Comorbidity Study. Archives of General Psychiatry, 52, 1048–1059.

Lewis, D.R. (1995). Native Americans and the environment: A survey of twentieth century issues. American Indian Quarterly, vol. 19: p. 423-450. University of Nebraska Press.

Lumey, L. H., & Stein, A. D. (1997). Offspring birth weights after maternal intrauterine undernutrition: A comparison within sibships. American Journal of Epidemiology, 146, 810–819.

Masterpasqua, F. (2009). Psychology and epigenetics. Review of General Psychology, vol. 13, No. 3, 194-201, American Psychological Association.

McGowan, P. O., Sasaki, A., D’Alessio, A. C., Dymov, S., Labonte, B., Szyf, J., et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuro- science, 12, 342–348.

Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience, 24, 1161–1192.

Meaney, M. (2004). The nature of nurture: Maternal effects and chromatin remodeling. In J. T. Cacioppo & G. G. Berntson (Eds.), Essays in social neuroscience (pp. 1–14). Cambridge, MA: MIT Press.

Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine, 13, 269-277.

Mennes, M., Van den Bergh, B. R. H., Lagae, L., & Stiers, P. (2009). Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety. Clinical Neurophysiology, 120(6), 1116–1122.

Mill, P., & Petronis, A. (2008). Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): The potential role of epigenetic processes in mediating susceptibility. Journal of Child Psychology and Psychiatry, 49, 1020–1030.

National Assessment of Educational Progress data, (2007). Retrieved December 10, 2009, from http://nces.ed.gov/nationsreportcard/ ; http://nces.ed.gov/programs/digest/d08/tables/dt08_118.asp?referrer=list ; http://nces.ed.gov/programs/digest/d08/tables/dt08_116.asp?referrer=list

Neigh, G.N., Gillespie, C. F., & Nemeroff, C. B. (2009). The neurobiological toll of child abuse and neglect. Trauma, Violence, and Abuse 10(4), pp. 389-410.

Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant corti- sol stress responses. Epigenetics, 3, 97-106.

Pembrey, M. E., Bygren, L. O., Kaati, G., Edvinsson, S., Northstone, K., Sjöström, M., et al. (2006). Sex-specific, male-line transgenerational responses in humans. European Journal of Human Genetics, 14, 159– 166.

Pray, L. A. (2006). Epigenetics: Genome, meet your environment. Scientist, 18(13), 14–20.

Rakyan, V. K., & Beck, S. (2006). Epigenetic variation and inheritance in mammals. Current Opinion in Genetics and Development, 16, 573–577.

Richards, E. J. (2006). Inherited epigenetic variation: Revisiting soft inheritance. Nature Reviews Genetics, 7, 395–401.

Rossiter, M.C. (1996). Incidence and consequences of inherited environmental effects. Annual Review of Ecology and Systematics, 27:1, 451-476.

Sjöström, K., Valentin, L., Thelin, T., & Marsal, K. (2002). Maternal anxiety in late pregnancy: Effect on fetal movements and fetal heart rate. Early Human Development, 67, 87–100.

Susser, E., Hoek, H. W., & Brown, A. (1998). Neurodevelopmental disorders after prenatal famine: The story of the Dutch famine study. American Journal of Epidemiology, 147, 213–216.

Szyf, M., McGowan, P., & Meaney, M. J. (2008). The social environment and the epigenome. Environmental and Molecular Mutagenesis, 49, 46–60.

Talge, N. M., Neal, C., Glover, V., and the early stress translational research and prevention science network (2007). Fetal and neonatal experience on child and adolescent mental health. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? Journal of Child Psychology and Psychiatry, 48, 245–261.

Tollrain, R. & Harvell, C. D. (ed.) (1999). The ecology and evolution of inducible defenses. Princeton University Press.

Van den Bergh, B. R. H. (1990). The influence of maternal emotions during pregnancy on fetal and neonatal behavior. Pre- and Perinatal Psychology Journal, 5, 119–130

Van den Bergh, B. R. H. (1992). Maternal emotions during pregnancy and fetal and neonatal behaviour. In J. G. Nijhuis (Ed.), Fetal behaviour: Developmental and perinatal aspects (pp. 157–178). Oxford: Oxford University Press.

Van den Bergh, B. R. H. (2010). Some societal and historical scientific considerations regarding the mother-fetus relationship and parenthood, Infant and Child Development,InterScience, http://www.interscience.wiley.com, Department of Psychology, Tilburg University, The Netherlands Department of Welfare, Public Health and Family, Flemish Government, Belgium, pp. 39-44.

Van den Bergh, B. R. H., Mulder, E. J. H., Visser, G. H. A., Poelmann-Weesjes, G., Bekedam, D. J., & Prechtl, H. F. R. (1989). The effect of (induced) maternal emotions on fetal behaviour: A controlled study. Early Human Development, 19, 9–19.

Van den Bergh, B. R. H., Mulder, E. J. H., Mennes, M., & Glover, V. (2005). Antenatal maternal anxiety and stress and the neurobehavioral development of the fetus and child: Links and possible mechanisms. A review. Neuroscience & Biobehavioral Reviews, 29, 237–258.

Van den Bergh, B. R. H., Van Calster, B., Smits, T., Van Huffel, S., & Lagae, L. (2008). Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology, 33, 536–545.

Wallace, A. R. (1893c). Prenatal influences on character. Nature, 389–390 (http://www.wku/edu/~smithch/wallace/S476.htm).

Weaver, I. C. G., Cervoni, N., Champagne, F. A., D’Alessio, A. C., Sharma, S., Seckl, J. R., Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.

Weinstock, M. (2008). The long-term behavioural consequences of prenatal stress. Neuroscience & Biobehavioral Reviews, 32, 1073–1086.

Yehuda, R., Bierer, L. M., Schmeidler, J., Aferiat, D. H., Breslau, I., & Dolan, S. (2000). Low cortisol and risk for PTSD in adult offspring of holocaust survivors. The American Journal of Psychiatry, 157, 1252-1259.

Yehuda, R., Blair, W., Labinsky, E., & Bierer, L. M. (2007). Effects of parental PTSD on the cortisol response to dexamethasone administration in their adult offspring. The American Journal of Psychiatry, 164, 163-166.

Zamenhof, S., van Marthens, E., & Grauel, L. (1971). DNA (cell number) in neonatal brain: Second generation (F2) alteration by maternal (F0) dietary protein restriction. Science, 172, 850–851.