Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2004 Sep 29;359(1449):1349–1358. doi: 10.1098/rstb.2004.1517

Understanding well-being in the evolutionary context of brain development.

Eric B Keverne 1
PMCID: PMC1693423  PMID: 15347526

Abstract

Much of the work on well-being and positive emotions has tended to focus on the adult, partly because this is when problems are manifest and well-being often becomes an issue by its absence. However, it is pertinent to ask if early life events might engender certain predispositions that have consequences for adult well-being. The human brain undergoes much of its growth and development postnatally until the age of seven and continues to extend its synaptic connections well into the second decade. Indeed, the prefrontal association cortex, areas of the brain concerned with forward planning and regulatory control of emotional behaviour, continue to develop until the age of 20. In this article, I consider the significance of this extended postnatal developmental period for brain maturation and how brain evolution has encompassed certain biological changes and predispositions that, with our modern lifestyle, represent risk factors for well-being. An awareness of these sensitive phases in brain development is important in understanding how we might facilitate secure relationships and high self-esteem in our children. This will provide the firm foundations on which to develop meaningful lifestyles and relationships that are crucial to well-being.

Full Text

The Full Text of this article is available as a PDF (147.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Apter Dan. The role of leptin in female adolescence. Ann N Y Acad Sci. 2003 Nov;997:64–76. doi: 10.1196/annals.1290.008. [DOI] [PubMed] [Google Scholar]
  2. Bechara A., Damasio H., Damasio A. R., Lee G. P. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci. 1999 Jul 1;19(13):5473–5481. doi: 10.1523/JNEUROSCI.19-13-05473.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bechara A., Tranel D., Damasio H. Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain. 2000 Nov;123(Pt 11):2189–2202. doi: 10.1093/brain/123.11.2189. [DOI] [PubMed] [Google Scholar]
  4. Biro Frank M., Lucky Anne W., Simbartl Loretta A., Barton Bruce A., Daniels Stephen R., Striegel-Moore Ruth, Kronsberg Shari S., Morrison John A. Pubertal maturation in girls and the relationship to anthropometric changes: pathways through puberty. J Pediatr. 2003 Jun;142(6):643–646. doi: 10.1067/mpd.2003.244. [DOI] [PubMed] [Google Scholar]
  5. Botvinick M., Nystrom L. E., Fissell K., Carter C. S., Cohen J. D. Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature. 1999 Nov 11;402(6758):179–181. doi: 10.1038/46035. [DOI] [PubMed] [Google Scholar]
  6. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P. M., Meaney M. J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5335–5340. doi: 10.1073/pnas.95.9.5335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chacko R. C., Corbin M. A., Harper R. G. Acquired obsessive-compulsive disorder associated with basal ganglia lesions. J Neuropsychiatry Clin Neurosci. 2000 Spring;12(2):269–272. doi: 10.1176/jnp.12.2.269. [DOI] [PubMed] [Google Scholar]
  8. Damasio A. R. Emotion in the perspective of an integrated nervous system. Brain Res Brain Res Rev. 1998 May;26(2-3):83–86. doi: 10.1016/s0165-0173(97)00064-7. [DOI] [PubMed] [Google Scholar]
  9. Davison Kirsten Krahnstoever, Susman Elizabeth J., Birch Leann Lipps. Percent body fat at age 5 predicts earlier pubertal development among girls at age 9. Pediatrics. 2003 Apr;111(4 Pt 1):815–821. doi: 10.1542/peds.111.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. De Bellis M. D., Keshavan M. S., Beers S. R., Hall J., Frustaci K., Masalehdan A., Noll J., Boring A. M. Sex differences in brain maturation during childhood and adolescence. Cereb Cortex. 2001 Jun;11(6):552–557. doi: 10.1093/cercor/11.6.552. [DOI] [PubMed] [Google Scholar]
  11. Elliott Rebecca, Newman Jana L., Longe Olivia A., Deakin J. F. William. Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: a parametric functional magnetic resonance imaging study. J Neurosci. 2003 Jan 1;23(1):303–307. doi: 10.1523/JNEUROSCI.23-01-00303.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Everitt B. J., Dickinson A., Robbins T. W. The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev. 2001 Oct;36(2-3):129–138. doi: 10.1016/s0165-0173(01)00088-1. [DOI] [PubMed] [Google Scholar]
  13. Fombonne E. Increased rates of psychosocial disorders in youth. Eur Arch Psychiatry Clin Neurosci. 1998;248(1):14–21. doi: 10.1007/s004060050013. [DOI] [PubMed] [Google Scholar]
  14. Francis D., Diorio J., Liu D., Meaney M. J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science. 1999 Nov 5;286(5442):1155–1158. doi: 10.1126/science.286.5442.1155. [DOI] [PubMed] [Google Scholar]
  15. Giedd J. N., Blumenthal J., Jeffries N. O., Castellanos F. X., Liu H., Zijdenbos A., Paus T., Evans A. C., Rapoport J. L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci. 1999 Oct;2(10):861–863. doi: 10.1038/13158. [DOI] [PubMed] [Google Scholar]
  16. Grant K. E., Compas B. E. Stress and anxious-depressed symptoms among adolescents: searching for mechanisms of risk. J Consult Clin Psychol. 1995 Dec;63(6):1015–1021. doi: 10.1037//0022-006x.63.6.1015. [DOI] [PubMed] [Google Scholar]
  17. Greenberg J. L., Lewis S. E., Dodd D. K. Overlapping addictions and self-esteem among college men and women. Addict Behav. 1999 Jul-Aug;24(4):565–571. doi: 10.1016/s0306-4603(98)00080-x. [DOI] [PubMed] [Google Scholar]
  18. Hinde R. A., Leighton-Shapiro M. E., McGinnis L. Effects of various types of separation experience on rhesus monkeys 5 months later. J Child Psychol Psychiatry. 1978 Jul;19(3):199–211. doi: 10.1111/j.1469-7610.1978.tb00464.x. [DOI] [PubMed] [Google Scholar]
  19. Joyce P. R., Oakley-Browne M. A., Wells J. E., Bushnell J. A., Hornblow A. R. Birth cohort trends in major depression: increasing rates and earlier onset in New Zealand. J Affect Disord. 1990 Feb;18(2):83–89. doi: 10.1016/0165-0327(90)90063-e. [DOI] [PubMed] [Google Scholar]
  20. Kalin N. H., Shelton S. E., Lynn D. E. Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology. 1995;20(7):735–742. doi: 10.1016/0306-4530(95)00023-2. [DOI] [PubMed] [Google Scholar]
  21. Kerns John G., Cohen Jonathan D., MacDonald Angus W., 3rd, Cho Raymond Y., Stenger V. Andrew, Carter Cameron S. Anterior cingulate conflict monitoring and adjustments in control. Science. 2004 Feb 13;303(5660):1023–1026. doi: 10.1126/science.1089910. [DOI] [PubMed] [Google Scholar]
  22. Keverne E. B., Martel F. L., Nevison C. M. Primate brain evolution: genetic and functional considerations. Proc Biol Sci. 1996 Jun 22;263(1371):689–696. doi: 10.1098/rspb.1996.0103. [DOI] [PubMed] [Google Scholar]
  23. Keverne E. B., Nevison C. M., Martel F. L. Early learning and the social bond. Ann N Y Acad Sci. 1997 Jan 15;807:329–339. doi: 10.1111/j.1749-6632.1997.tb51930.x. [DOI] [PubMed] [Google Scholar]
  24. Klentrou P., Plyley M. Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls. Br J Sports Med. 2003 Dec;37(6):490–494. doi: 10.1136/bjsm.37.6.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Koob G. F., Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science. 1997 Oct 3;278(5335):52–58. doi: 10.1126/science.278.5335.52. [DOI] [PubMed] [Google Scholar]
  26. Kraemer G. W., Ebert M. H., Schmidt D. E., McKinney W. T. Strangers in a strange land: a psychobiological study of infant monkeys before and after separation from real or inanimate mothers. Child Dev. 1991 Jun;62(3):548–566. [PubMed] [Google Scholar]
  27. Ladd C. O., Owens M. J., Nemeroff C. B. Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology. 1996 Apr;137(4):1212–1218. doi: 10.1210/endo.137.4.8625891. [DOI] [PubMed] [Google Scholar]
  28. Leckman J. F., Goodman W. K., North W. G., Chappell P. B., Price L. H., Pauls D. L., Anderson G. M., Riddle M. A., McDougle C. J., Barr L. C. The role of central oxytocin in obsessive compulsive disorder and related normal behavior. Psychoneuroendocrinology. 1994;19(8):723–749. doi: 10.1016/0306-4530(94)90021-3. [DOI] [PubMed] [Google Scholar]
  29. Leckman J. F., Mayes L. C., Feldman R., Evans D. W., King R. A., Cohen D. J. Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder. Acta Psychiatr Scand Suppl. 1999;396:1–26. doi: 10.1111/j.1600-0447.1999.tb10951.x. [DOI] [PubMed] [Google Scholar]
  30. Leckman J. F., Mayes L. C. Preoccupations and behaviors associated with romantic and parental love. Perspectives on the origin of obsessive-compulsive disorder. Child Adolesc Psychiatr Clin N Am. 1999 Jul;8(3):635–665. [PubMed] [Google Scholar]
  31. Lorberbaum Jeffrey P., Newman John D., Horwitz Amy R., Dubno Judy R., Lydiard R. Bruce, Hamner Mark B., Bohning Daryl E., George Mark S. A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry. 2002 Mar 15;51(6):431–445. doi: 10.1016/s0006-3223(01)01284-7. [DOI] [PubMed] [Google Scholar]
  32. Martel F. L., Nevison C. M., Rayment F. D., Simpson M. J., Keverne E. B. Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology. 1993;18(4):307–321. doi: 10.1016/0306-4530(93)90027-i. [DOI] [PubMed] [Google Scholar]
  33. Martel F. L., Nevison C. M., Simpson M. J., Keverne E. B. Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups. Dev Psychobiol. 1995 Mar;28(2):71–84. doi: 10.1002/dev.420280202. [DOI] [PubMed] [Google Scholar]
  34. Mayberry Rachel I., Lock Elizabeth, Kazmi Hena. Linguistic ability and early language exposure. Nature. 2002 May 2;417(6884):38–38. doi: 10.1038/417038a. [DOI] [PubMed] [Google Scholar]
  35. Meaney M. J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001;24:1161–1192. doi: 10.1146/annurev.neuro.24.1.1161. [DOI] [PubMed] [Google Scholar]
  36. Modrcin-Talbott M. A., Pullen L., Zandstra K., Ehrenberger H., Muenchen B. A study of self-esteem among well adolescents: seeking a new direction. Issues Compr Pediatr Nurs. 1998 Oct-Dec;21(4):229–241. doi: 10.1080/014608698265438. [DOI] [PubMed] [Google Scholar]
  37. Monk Christopher S., McClure Erin B., Nelson Eric E., Zarahn Eric, Bilder Robert M., Leibenluft Ellen, Charney Dennis S., Ernst Monique, Pine Daniel S. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage. 2003 Sep;20(1):420–428. doi: 10.1016/s1053-8119(03)00355-0. [DOI] [PubMed] [Google Scholar]
  38. Panksepp J., Nelson E., Bekkedal M. Brain systems for the mediation of social separation-distress and social-reward. Evolutionary antecedents and neuropeptide intermediaries. Ann N Y Acad Sci. 1997 Jan 15;807:78–100. doi: 10.1111/j.1749-6632.1997.tb51914.x. [DOI] [PubMed] [Google Scholar]
  39. Ploj K., Roman E., Nylander I. Long-term effects of maternal separation on ethanol intake and brain opioid and dopamine receptors in male Wistar rats. Neuroscience. 2003;121(3):787–799. doi: 10.1016/s0306-4522(03)00499-8. [DOI] [PubMed] [Google Scholar]
  40. Rauch S. L. Neuroimaging research and the neurobiology of obsessive-compulsive disorder: where do we go from here? Biol Psychiatry. 2000 Feb 1;47(3):168–170. doi: 10.1016/s0006-3223(99)00297-8. [DOI] [PubMed] [Google Scholar]
  41. Richter S. S., Brown S. A., Mott M. A. The impact of social support and self-esteem on adolescent substance abuse treatment outcome. J Subst Abuse. 1991;3(4):371–385. doi: 10.1016/s0899-3289(10)80019-7. [DOI] [PubMed] [Google Scholar]
  42. Robbins T. W., Everitt B. J. Drug addiction: bad habits add up. Nature. 1999 Apr 15;398(6728):567–570. doi: 10.1038/19208. [DOI] [PubMed] [Google Scholar]
  43. Schultz W., Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci. 2000;23:473–500. doi: 10.1146/annurev.neuro.23.1.473. [DOI] [PubMed] [Google Scholar]
  44. Shalitin S., Phillip M. Role of obesity and leptin in the pubertal process and pubertal growth--a review. Int J Obes Relat Metab Disord. 2003 Aug;27(8):869–874. doi: 10.1038/sj.ijo.0802328. [DOI] [PubMed] [Google Scholar]
  45. Sowell E. R., Delis D., Stiles J., Jernigan T. L. Improved memory functioning and frontal lobe maturation between childhood and adolescence: a structural MRI study. J Int Neuropsychol Soc. 2001 Mar;7(3):312–322. doi: 10.1017/s135561770173305x. [DOI] [PubMed] [Google Scholar]
  46. Sowell E. R., Thompson P. M., Holmes C. J., Jernigan T. L., Toga A. W. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci. 1999 Oct;2(10):859–861. doi: 10.1038/13154. [DOI] [PubMed] [Google Scholar]
  47. Sowell E. R., Thompson P. M., Tessner K. D., Toga A. W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. J Neurosci. 2001 Nov 15;21(22):8819–8829. doi: 10.1523/JNEUROSCI.21-22-08819.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sroufe L. A., Carlson E. A., Levy A. K., Egeland B. Implications of attachment theory for developmental psychopathology. Dev Psychopathol. 1999 Winter;11(1):1–13. doi: 10.1017/s0954579499001923. [DOI] [PubMed] [Google Scholar]
  49. Sund Anne Mari, Larsson Bo, Wichstrøm Lars. Psychosocial correlates of depressive symptoms among 12-14-year-old Norwegian adolescents. J Child Psychol Psychiatry. 2003 May;44(4):588–597. doi: 10.1111/1469-7610.00147. [DOI] [PubMed] [Google Scholar]
  50. Tremblay L., Schultz W. Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. J Neurophysiol. 2000 Apr;83(4):1877–1885. doi: 10.1152/jn.2000.83.4.1877. [DOI] [PubMed] [Google Scholar]
  51. Vega W. A., Apospori E., Gil A. G., Zimmerman R. S., Warheit G. J. A replication and elaboration of the esteem-enhancement model. Psychiatry. 1996 Summer;59(2):128–144. doi: 10.1080/00332747.1996.11024755. [DOI] [PubMed] [Google Scholar]
  52. Weiss M., Baerg E., Wisebord S., Temple J. The influence of gonadal hormones on periodicity of obsessive-compulsive disorder. Can J Psychiatry. 1995 May;40(4):205–207. doi: 10.1177/070674379504000408. [DOI] [PubMed] [Google Scholar]
  53. Williams K. E., Koran L. M. Obsessive-compulsive disorder in pregnancy, the puerperium, and the premenstruum. J Clin Psychiatry. 1997 Jul;58(7):330–336. doi: 10.4088/jcp.v58n0709. [DOI] [PubMed] [Google Scholar]
  54. Zohar J., Hermesh H., Weizman A., Voet H., Gross-Isseroff R. Orbitofrontal cortex dysfunction in obsessive-compulsive disorder? I. Alternation learning in obsessive-compulsive disorder: male-female comparisons. Eur Neuropsychopharmacol. 1999 Sep;9(5):407–413. doi: 10.1016/s0924-977x(99)00019-x. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES