Experience-dependent asymmetric variation in primate prefrontal morphology

Behavioural Brain Research

Volumn 136, Issue 1, 2002, Pages 51-59

  Lyons, David M ^a   Afarian, Hagop ^a   Schatzberg, Alan F ^a   Sawyer Glover, Anne ^b   Moseley, Michael E ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Early life stress; Emotional behavior; Hypothalamic pituitary adrenal hormones; Magnetic resonance imaging; Nonhuman primates; Postnatal development; Prefrontal cortex

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN SIZE; CONTROLLED STUDY; EMOTION; EXPERIENCE; FEMALE; FOLLOW UP; GRAY MATTER; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MONKEY; MORPHOLOGY; MOTHER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; SOCIAL ADAPTATION; STRESS; WHITE MATTER;

ANIMALS; BODY WEIGHT; FEMALE; FUNCTIONAL LATERALITY; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; MATERNAL DEPRIVATION; ORGAN SIZE; PREFRONTAL CORTEX; SAIMIRI; SEX CHARACTERISTICS; SOCIAL ENVIRONMENT;

EID: 0037126167     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(02)00100-6     Document Type: Article

References (81)

1. Ahern G.L., Herring A.K., Tackenberg J.N., Schwartz G.E., Seeger J.F., Labiner D.M., Weinand M.E., Oommen K.J. Affective self-report during the intracarotid sodium amobarbital test. Journal of Clinical and Experimental Neuropsychology. 16:1994;372-376.
2. Andrews M.W., Rosenblum L.A. The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Development. 65:1994;1398-1404.
3. Barbazanges A., Vallee M., Mayo W., Day J., Simon H., Le Moal M., Maccari S. Early and later adoptions have different long-term effects on male rat offspring. Journal of Neuroscience. 16:1996;7783-7790.
4. Bartley A.J., Jones D.W., Weinberger D.R. Genetic variability of human brain size and cortical gyral patterns. Brain. 120:1997;257-269.
5. Bartzokis G., Beckson M., Lu P.H., Nuechterlein K.H., Edwards N., Mintz J. Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. Archives of General Psychiatry. 58:2001;461-465.
6. Bourgeois J.P., Goldman-Rakic P.S., Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cerebral Cortex. 4:1994;78-96.
7. Brady A.G. Research techniques for the squirrel monkey (Saimiri). International Laboratory Animal Research Journal. 41:2000;10-18.
8. Canli T., Desmond J.E., Zhao Z., Glover G., Gabrieli J.D. Hemispheric asymmetry for emotional stimuli detected with fMRI. Neuroreport. 9:1998;3233-3239.
9. Chapmoux M., Coe C.L., Schanberg S., Kuhn C., Suomi S.J. Hormonal effects of early rearing conditions in the infant rhesus monkey. Americal Journal of Primatology. 19:1989;111-117.
10. Cheverud J.M., Falk D., Vannier M., Konigsberg L., Helmkamp R.C., Hildebolt C. Heritability of brain size and surface features in rhesus macaques (Macaca mulatta). Journal of Heredity. 81:1990;51-57.
11. Chrousos G.P., Gold P.W. A healthy body in a healthy mind - and vice versa - the damaging power of 'uncontrollable' stress. Journal of Clinical and Endocrinological Metabolism. 83:1998;1842-1845.
12. Clarke A.S., Kammerer C.M., George K.P., Kupfer D.J., McKinney W.T., Spence M.A., Kraemer G.W. Evidence for heritability of biogenic amine levels in the CSF of rhesus monkeys. Biological Psychiatry. 38:1995;572-577.
13. Coe C.L., Glass J.C., Wiener S.G., Levine S. Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology. 8:1983;401-409.
14. Coplan J.D., Andrews M.W., Rosenblum L.A., Owens M.J., Friedman S., Gorman J.M., Nemeroff C.B. Persistent elevations of CSF concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences of the United States of America. 93:1996;1619-1623.
15. Coplan J.D., Trost R.C., Owens M.J., Cooper T.B., Gorman J.M., Nemeroff C.B., Rosenblum L.A. CSF concentrations of somatostatin and biogenic amines in grown primates reared by mothers exposed to manipulated foraging conditions. Archives of General Psychiatry. 55:1998;473-477.
16. Denenberg V.H. Critical periods, stimulus input, and emotional reactivity: a theory of infantile stimulation. Psychological Review. 71:1964;335-351.
17. Diamond A. Developmental time course in human infants and infant monkeys, and the neural bases of, inhibitory control of reaching. Annals of the New York Academy of Sciences. 608:1990;637-676.
18. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. Journal of Neuroscience. 13:1993;3839-3847.
19. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature. 386:1997;824-827.
20. Fahlke C., Lorenz J.G., Long J., Champoux M., Suomi S.J., Higley J.D. Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcoholism: Clinical and Experimental Research. 24:2000;644-650.
21. Falconer D.S., Mackay T.F.C. Introduction to quantitative genetics. 4th ed. 1996;Longman Group, London.
22. Fonta C., Imbert M. Angiogenesis in the developing marmoset visual cortex. Society for Neuroscience Abstracts. 27:2001;475-522.
23. Fox N.A., Rubin K.H., Calkins S.D., Marshall T.R., Coplan R.J., Porges S.W., Long J.M., Stewart S. Frontal activation asymmetry and social competence at four years of age. Child Development. 66:1995;1770-1784.
24. 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. Nature Neuroscience. 2:1999;861-863.
25. Goldman-Rakic P.S. Development of cortical circuitry and cognitive function. Child Development. 58:1987;601-622.
26. Greenough W.T., Black J.E., Wallace C.S. Experience and brain development. Child Development. 58:1987;539-559.
27. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathologica and Microbiologica Scandinavica. 96:1988;379-394.
28. Heim C., Newport D.J., Heit S., Graham Y.P., Wilcox M., Bonsall R., Miller A.H., Nemeroff C.B. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association. 284:2000;592-597.
29. Hennessy M.B. Multiple, brief maternal separations in the squirrel monkey: changes in hormonal and behavioral responsiveness. Physiology and Behavior. 36:1986;245-250.
30. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neuroscience. 20:1997;78-84.
31. Higley J.D., Suomi S.J., Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biological Psychiatry. 32:1992;127-145.
32. Higley J.D., Thompson W.W., Champoux M., Goldman D., Hasert M.F., Kraemer G.W., Scanlan J.M., Suomi S.J., Linnoila M. Paternal and maternal genetic and environmental contributions to CSF monoamine metabolites in rhesus monkeys (Macaca mulatta). Archives of General Psychiatry. 50:1993;615-623.
33. Hopf S., Hartmann-Wiesner E., Kuhlmorgen B., Mayer S. The behavioral repertoire of the squirrel monkey (Saimiri). Folia Primatologica. 21:1974;225-249.
34. Huether G. Stress and the adaptive self-organization of neuronal connectivity during early childhood. International Journal of Developmental Neuroscience. 16:1998;297-306.
35. Huntley G.W., Benson D.L., Jones E.G., Isackson P.J. Developmental expression of brain derived neurotrophic factor mRNA by neurons of fetal and adult monkey prefrontal cortex. Brain Research Developmental Brain Research. 70:1992;53-63.
36. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocrine Review. 12:1991;118-134.
37. Kaemingk K., Reite M. Social environment and nocturnal sleep: studies in peer-reared monkeys. Sleep. 10:1987;542-550.
38. Kalin N.H., Larson C., Shelton S.E., Davidson R.J. Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behavioral Neuroscience. 112:1998;286-292.
39. Kim D.K., Kim B.L., Sohn S.E., Lim S.W., Na D.G., Paik C.H., Krishnan K.R., Carroll B.J. Candidate neuroanatomic substrates of psychosis in old-aged depression. Progress in Neuropsychopharmacology and Biological Psychiatry. 23:1999;793-807.
40. Kraemer G.W. Psychobiology of early social attachment in rhesus monkeys. Clinical implications. Annals of the New York Academy of Science. 807:1997;401-418.
41. Leventhal C., Rafii S., Rafii D., Shahar A., Goldman S.A. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Molecular and Cellular Neuroscience. 13:1999;450-464.
42. Levine S. Infantile experience and resistance to physiological stress. Science. 126:1957;405-406.
43. Lewis D.A. Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neuropsychopharmacology. 16:1997;385-398.
44. Lewis M. Self-conscious emotions. American Scientist. 83:1995;68-78.
45. Lewis M.H., Gluck J.P., Beauchamp A.J., Keresztury M.F., Mailman R.B. Long-term effects of early social isolation in Macaca mulatta: changes in dopamine receptor function following apomorphine challenge. Brain Research. 513:1990;67-73.
46. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience. 3:2000;799-806.
47. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science. 277:1997;1659-1662.
48. Lyons D.M., Kim S., Schatzberg A.F., Levine S. Postnatal foraging demands alter adrenocortical activity and psychosocial development. Developmental Psychobiology. 32:1998;285-291.
49. Lyons D.M., Martel F.L., Levine S., Risch N.J., Schatzberg A.F. Postnatal experiences and genetic effects on squirrel monkey social affinities and emotional distress. Hormones and Behavior. 36:1999;266-275.
50. Lyons D.M., Yang C., Mobley B.W., Nickerson J.T., Schatzberg A.F. Early environmental regulation of glucocorticoid feedback sensitivity in young adult monkeys. Journal of Neuroendocrinology. 12:2000;723-728.
51. Lyons D.M., Yang C., Sawyer-Glover A.M., Moseley M.E., Schatzberg A.F. Early life stress and inherited variation in monkey hippocampal volumes. Archives of General Psychiatry. 68:2001;1145-1151.
52. Mason W. Ontogeny of social behavior. Marler P., Vandenbergh J.G., Handbook of Behavioral Neurobiology. Social Behavior and Communication. 3:1979;1-28 Plenum Press, New York.
53. Mason W.A., Mendoza S.P., Moberg G.P. Persistent effects of early social experience on physiological responsiveness. Ehara A., Kimura R., Takenaka O., Iwamoto M., Primatology Today. 1991;469-471 Elsevier, New York.
54. McEwen B.S. Protective and damaging effects of stress mediators. New England Journal of Medicine. 338:1998;171-179.
55. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., Seckl J.R., Plotsky P.M. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Developmental Neuroscience. 18:1996;49-72.
56. O'Donnell D., Larocque S., Seckl J.R., Meaney M.J. Postnatal handling alters glucocorticoid, but not mineralocorticoid messenger RNA expression in the hippocampus of adult rats. Brain Research Molecular Brain Research. 26:1994;242-248.
57. Ongur D., Drevets W.C., Price J.L. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proceedings of the National Academy of Sciences of the United States of America. 95:1998;13290-13295.
58. Ongur D., Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex. 10:2000;206-219.
59. Patel P.D., Lopez J.F., Lyons D.M., Burke S., Wallace M., Schatzberg A.F. Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. Journal of Psychiatric Research. 34:2000;383-392.
60. Pennington B.F., Filipek P.A., Lefly D., Chhabildas N., Kennedy D.N., Simon J.H., Filley C.M., Galaburda A., DeFries J.C. A twin MRI study of size variations in human brain. Journal of Cognitive Neuroscience. 12:2000;223-232.
61. Pfefferbaum A., Sullivan E.V., Swan G.E., Carmelli D. Brain structure in men remains highly heritable in the seventh and eighth decades of life. Neurobiology of Aging. 21:2000;63-74.
62. Posner M.I., Rothbart M.K. Developing mechanisms of self-regulation. Developmental Psychopathology. 12:2000;427-441.
63. Preuss T.M. Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. Journal of Cognitive Neuroscience. 7:1995;1-24.
64. Rabinowicz T. The differentiated maturation of the cerebral cortex. Falkner F., Tanner J.M., Human Growth. 2:1986;385-410 Plenum Press, New York.
65. Rajkowska G., Miguel-Hidalgo J.J., Wei J., Dilley G., Pittman S.D., Meltzer H.Y., Overholser J.C., Roth B.L., Stockmeier C.A. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biological Psychiatry. 45:1999;1085-1098.
66. Rakic P. The development of the frontal lobe. A view from the rear of the brain. Advances in Neurology. 66:1995;1-6.
67. Raz N., Gunning F.M., Head D., Dupuis J.H., McQuain J., Briggs S.D., Loken W.J., Thornton A.E., Acker J.D. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cerebral Cortex. 7:1997;268-282.
68. Rosabal F. Cytoarchitecture of the frontal lobe of the squirrel monkey. Journal of Comparative Neurology. 130:1967;87-108.
69. Rosenblum L.A., Andrews M.W. Influences of environmental demand on maternal behavior and infant development. Acta Paediatrica Supplement. 397:1994;57-63.
70. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behavioral Brain Research. 78:1996;57-65.
71. Sanchez M.M., Young L.J., Plotsky P.M., Insel T.R. Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. Journal of Neuroscience. 20:2000;4657-4668.
72. Sanides F. The architecture of the cortical taste nerve areas in squirrel monkey (Saimiri sciureus) and their relationships to insular, sensorimotor and prefrontal regions. Brain Research. 8:1968;97-124.
73. Schatzberg A.F., Nemeroff C.B. Textbook of Psychopharmacology. 1998;American Psychiatric Press, Washington, DC.
74. Schleicher A., Amunts K., Geyer S., Kowalski T., Schormann T., Palomero-Gallagher N., Zilles K. A stereological approach to human cortical architecture: identification and delineation of cortical areas. Journal of Chemical Neuroanatomy. 20:2000;31-47.
75. Schore A.N. The experience-dependent maturation of a regulatory system in the orbital prefrontal cortex and the origin of developmental psychopathology. Developmental Psychopathology. 8:1996;59-87.
76. Sheline Y.I., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. Journal of Neuroscience. 19:1999;5034-5043.
77. 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. Nature Neuroscience. 2:1999;859-861.
78. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Review. 24:2000;417-463.
79. Stanton M.E., Levine S. Brief separation elevates cortisol in mother and infant squirrel monkeys. Physiology and Behavior. 34:1985;1007-1008.
80. Suomi S.J. Genetic and maternal contributions to individual differences in rhesus monkey biobehavioral development. Krasnegor N.A., Blass E.M., Hofer M.A., Smotherman W.P., Perinatal Development. A Psychobiological Perspective. 1987;Academic Press, New York.
81. Wittling W., Pfluger M. Neuroendocrine hemisphere asymmetries: salivary cortisol secretion during lateralized viewing of emotion-related and neutral films. Brain Cognition. 14:1990;243-265.