Abstract
How do we become who we are? Are we tabula rasa, blank slates randomly scrambling for imprintation of information, or are we merely the constructions of our selfish genetic blueprints? Current scientific philosophy tells us we are neither preprogrammed nor do we possess unadulterated free will. While mammalian neurobehavioral development is biologically constrained, it is also sensitive to experience. Neurophysiological patterning guides motivation and emotion that we use to navigate our environments. Our environments, however, often present unexpected challenges. We develop our strategies for responding to stress throughout prenatal and postnatal development. How does this neurobehavioral development unfold? It proceeds according to exceedingly elegant and precisely timed interactions between the genome and the environment. These interactions begin at conception and may last a lifetime but may be particularly potent at critical periods in development. During these critical periods of embryonic and early postnatal development, even the slightest variability in the coordination between the genome and the environment results in some of the breathtaking neurobehavioral variability in stress adaptation we observe in infant mammals. This chapter will examine some examples of genome– environment coordination that impacts prenatal and early postnatal neurobehavioral development in nonhuman primates. I will discuss how certain regions of the genome may put individuals at risk for disadvantageous neurobehavioral development following early stress and possible mechanisms for how this risk may occur. Next I will introduce the reader to the diverse role of epigenetics in the effects of early environment. Finally, I will consider the potential consequences of gene–environment coordination across generations. The goal of this chapter is to provide examples of the complexity of the inheritance and development of stress response strategies and to highlight new avenues for understanding why some nonhuman primates wither when challenged, while others thrive.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Andrews MW, Rosenblum LA (1994) The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Dev 65:1398–1404
Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA (2009) Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample. Am J Med Genet B Neuropsychiatr Genet 153B:710–713
Bohnen N, Nicolson N, Sulon J, Jolles J (1991) Coping style, trait anxiety and cortisol reactivity during mental stress. J Psychosom Res 35:141–147
Bowlby J (1951) Maternal care and mental health. Bull World Health Organ 3:355–533
Chen GL, Novak MA, Meyer JS, Kelly BJ, Vallender EJ, Miller GM (2010) TPH2 5’- and 3’-regulatory polymorphisms are differentially associated with HPA axis function and self-injurious behavior in rhesus monkeys. Genes Brain Behav 9(3):335–347
Falconer DS, MacKay TFC (1996) Quantitative genetics. Pearson, Harlow
Fite JE, French JA (2000) Pre- and postpartum sex steroids in female marmosets (Callithrix kuhlii): is there a link with infant survivorship and maternal behavior? Horm Behav 38(1):1–12
Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158
Franklin TB, Russig H, Weiss IC, Gräff J, Linder N, Michalon A et al (2010) Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68:408–415
Friedman M, Rosenman RH (1971) Type A behavior pattern: its association with coronary heart disease. Ann Clin Res 3:300–312
Higley JD, Linnoila M (1997) Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior. A nonhuman primate model investigating genetic and environmental influences on neurotransmission. Ann NY Acad Sci 836:39–56
Higley JD, Thompson WW, Champoux M, Goldman D, Hasert MF, Kraemer GW, Scanlan JM, Suomi SJ, Linnoila M (1993) Paternal and maternal genetic and environmental contributions to cerebrospinal fluid monoamine metabolites in rhesus monkeys (Macaca mulatta). Arch Gen Psychiatry 50:615–623
Jedema HP, Gianaros PJ, Greer PJ, Kerr DD, Liu S, Higley JD, Suomi SJ, Olsen AS, Porter JN, Lopresti BJ, Hariri AR, Bradberry CW (2010) Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Mol Psychiatry 15(5):512–522
Kagan J, Reznick JS, Snidman N (1987) The physiology and psychology of behavioral inhibition in children. Child Dev 58:1459–1473
Kalin NH, Shelton SE, Takahashi LK (1991) Defensive behaviors in infant rhesus monkeys: ontogeny and context-dependent selective expression. Child Dev 62:1175–1183
Karere GM, Kinnally EL, Sanchez JN, Famula T, Lyons LA, Capitanio JP (2009) What is early adversity? Monoamine oxidase A promoter polymorphism variation influences infant response to a human intruder in rhesus macaques. Biol Psychiatry 65:770–777
Kinnally EL, Karere GM, Mendoza SP, Lyons LA, Mason WA, Capitanio JP (2010) Serotonin pathway gene-gene and gene-environment interactions influence behavioral response to stress in infant rhesus macaques. Dev Psychopathol 22:35–44
Kinnally EL, Feinberg C, Kim D, Ferguson K, Leibel R, Coplan JD, Mann JJ (2011) DNA methylation as a risk factor in the effects of early life stress. Brain Behav Immun 25:1548–1553
Levine S (2001) Primary social relationships influence the development of the hypothalamic–pituitary–adrenal axis in the rat. Physiol Behav 73:255–260
Lindell SG, Schwandt ML, Sun H, Sparenborg JD, Björk K, Kasckow JW, Sommer WH, Goldman D, Higley JD, Suomi SJ, Heilig M, Barr CS (2010) Functional NPY variation as a factor in stress resilience and alcohol consumption in rhesus macaques. Arch Gen Psychiatry 67(4):423–431
Mathew SJ, Coplan JD, Smith EL, Scharf BA, Owens MJ, Nemeroff CB, Mann JJ, Gorman JM, Rosenblum LA (2002) Cerebrospinal fluid concentrations of biogenic amines and corticotropin-releasing factor in adolescent non-human primates as a function of the timing of adverse early rearing. Stress 5(3):185–193
McCormack K, Sanchez MM, Bardi M, Maestripieri D (2006) Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev Psychobiol 48(7):537–550
McCormack K, Newman T, Higley J, Maestripieri D, Sanchez M (2009) Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm Behav 55:538–547
Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192
Mendoza SP, Smotherman WP, Miner MT, Kaplan J, Levine S (1978) Pituitary-adrenal response to separation in mother and infant squirrel monkeys. Dev Psychobiol 11(2):169–175
Newman T, Syagailo YV, Barr CS, Wendland JR, Champoux M, Graessle M et al (2005) Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol Psychiatry 57:167–172
Parker KJ, Buckmaster CL, Sundlass K, Schatzberg AF, Lyons DM (2006) Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci USA 103(8):3000–3005
Rosenblum L, Paully G (1984) The effects of varying environmental demands on maternal and infant behavior. Child Dev 55:305–314
Rosenblum L, Forger C, Noland S, Trost R, Coplan J (2001) Response of adolescent bonnet macaques to an acute fear stimulus as a function of early rearing conditions. Dev Psychobiol 39:40–45
Roth T, Lubin F, Funk A, Sweatt J (2009) Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65:760–769
Sabol S, Hu S, Hamer D (1998) A functional polymorphism in themonoamine oxidase A gene promoter. Hum Genet 103:273–279
Schwandt ML, Lindell SG, Sjöberg RL, Chisholm KL, Higley JD, Suomi SJ, Heilig M, Barr CS (2010) Gene-environment interactions and response to social intrusion in male and female rhesus macaques. Biol Psychiatry 67(4):323–330
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Kinnally, E.L. (2013). Genome–Environment Coordination in Neurobehavioral Development. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_7
Download citation
DOI: https://doi.org/10.1007/978-1-4614-4060-4_7
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-4059-8
Online ISBN: 978-1-4614-4060-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)