Early maternal availability and prefrontal correlates of reward-related memory

Neurobiology of Learning and Memory

Volumn 80, Issue 2, 2003, Pages 97-104

  Lyons, David M ^a   Schatzberg, Alan F ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cognitive development; Emotional reactivity; Magnetic resonance imaging; Nonhuman primates; Postnatal stress; Prefrontal morphology

Indexed keywords

ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SIZE; CONTROLLED STUDY; CORRELATION ANALYSIS; EMOTION; FEMALE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEFT HEMISPHERE; MALE; MATERNAL DEPRIVATION; MEMORY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREFRONTAL CORTEX; REWARD; RIGHT HEMISPHERE; SQUIRREL MONKEY; STRESS; TASK PERFORMANCE;

EID: 0042661166     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7427(03)00044-3     Document Type: Article

References (74)

1. Aguilar R., Escorihuela R.M., Gil L., Tobena A., Fernandez-Teruel A. Differences between two psychogenetically selected lines of rats in a swimming pool matching-to-place task: long-term effects of infantile stimulation. Behavior Genetics. 32:2002;127-134.
2. Ahern G.L., Herring A.M., 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.
3. Andrews M.W., Rosenblum L.A. The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Development. 65:1994;1398-1404.
4. Balleine B.W., Dickinson A. Goal-directed instrumental action: Contingency and incentive learning and their cortical substrates. Neuropharmacology. 37:1998;407-419.
5. Beauchamp A.J., Gluck J.P., Fouty H.E., Lewis M.H. Associative processes in differentially reared rhesus monkeys (Macaca mulatta): Blocking. Developmental Psychobiology. 24:1991;175-189.
6. Brady A.G. Research techniques for the squirrel monkey (Saimiri). ILAR Journal. 41:2000;10-18.
7. Cabeza R., Nyberg L. Neural bases of learning and memory: Functional neuroimaging evidence. Current Opinion in Neurology. 13:2000;415-421.
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. Capitanio J.P., Mason W.A. Cognitive style: Problem solving by rhesus macaques (Macaca mulatta) reared with living or inanimate substitute mothers. Journal of Comparative Psychology. 114:2000;115-125.
10. Champoux M., Zanker D., Levine S. Food search demand effort effects on behavior and cortisol in adult female squirrel monkeys. Physiology and Behavior. 54:1993;1091-1097.
11. 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.
12. 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.
13. Cohen J., Cohen P. Applied multiple regression/correlation analysis for the behavioral sciences. 1983;Lawrence Erlbaum, Hillsdale, NJ.
14. Coplan J.D., Andrews M.W., Rosenblum L.A., Owens M.J., Friedman S., Gorman J.M., Nemeroff C.B. Persistent elevations of cerebrospinal fluid 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, USA. 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. Cerebrospinal fluid 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. Damasio A.R. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences. 351:1996;1413-1420.
17. 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.
18. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience. 1:2000;41-50.
19. Fernandez-Teruel A., Escorihuela R.M., Nunez J.F., Zapata A., Boix F., Salazar W., Tobena A. The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behavior: psychopharmacological validation. Brain Research Bulletin. 26:1991;173-176.
20. Fernandez-Teruel A., Gimenez-Llort L., Escorihuela R.M., Gil L., Aguilar R., Steimer T., Tobena A. Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms. Pharmacology, Biochemistry and Behavior. 73:2002;233-245.
21. 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.
22. Fuster J.M. Synopsis of function and dysfunction of the frontal lobe. Acta Psychiatrica Scandinavica Supplement. 395:1999;51-57.
23. 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.
24. Goldman-Rakic P.S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences. 351:1996;1445-1453.
25. Grafman J., Holyoak K.J., Boller F. Structure and functions of the human prefrontal cortex. Annals of the New York Academy of Sciences. 769:1995;1-411.
26. Griffin G.A., Harlow H.F. Effects of three months of total social deprivation on social adjustment and learning in the rhesus monkey. Child Development. 37:1966;533-547.
27. Hennessy M.B. Multiple, brief maternal separations in the squirrel monkey: Changes in hormonal and behavioral responsiveness. Physiology & Behavior. 36:1986;245-250.
28. Herman J.P., Cullinan W.E. Neurocircuitry of stress: Central control of the hypothalamo-pituitary-adrenocortical axis. Trends in Neuroscience. 20:1997;78-84.
29. 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.
30. Hikosaka K., Watanabe M. Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. Cerebral Cortex. 10:2000;263-271.
31. Hofer M.A. Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology. 21:1996;203-217.
32. Hopf S., Hartmann-Wiesner E., Kuhlmorgen B., Mayer S. The behavioral repertoire of the squirrel monkey (Saimiri). Folia Primatologica. 21:1974;225-249.
33. Huether G. Stress and the adaptive self-organization of neuronal connectivity during early childhood. International Journal of Developmental Neuroscience. 16:1998;297-306.
34. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocrine Review. 12:1991;118-134.
35. 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.
36. Keppel G. Design and Analysis, A Researcher's Handbook. 1982;Prentice-Hall, Englewood Cliffs, NJ.
37. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science. 156:1967;258-260.
38. Levine S., Champoux M., Wiener S.G. Social modulation of the stress response. Genazzani A.R., Nappi G., Petraglia F., Martignoni E. Stress and related disorders from adaptation to dysfunction. 1991;121-128 Parthenon Publishing, NJ.
39. Lewis D.A. Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neuropsychopharmacology. 16:1997;385-398.
40. Lewis M. Self-conscious emotions. American Scientist. 83:1995;68-78.
41. 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.
42. 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.
43. Lyons D.M., Afarian H., Schatzberg A.F., Sawyer-Glover A., Moseley M.E. Experience-dependent asymmetric variation in primate prefrontal morphology. Behavioural Brain Research. 136:2002;51-59.
44. Lyons D.M., Banks E.M. Ultrasounds in neonatal rats: Novel, predator and conspecific odor cues. Developmental Psychobiology. 15:1982;455-460.
45. 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.
46. 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.
47. 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.
48. 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. 58:2001;1145-1151.
49. Martin R.E., Sackett G.P., Gunderson V.M., Goodlin-Jones B.L. Auditory evoked heart rate responses in pigtailed macaques (Macaca nemestrina) raised in isolation. Developmental Psychobiology. 21:1988;251-260.
50. Mason W. Ontogeny of social behavior. Marler P., Vandenbergh J.G. Handbook of behavioral neurobiology. Social behavior and communication. Vol. 3:1979;1-28 Plenum Press, New York.
51. 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.
52. McIntosh J., Anisman H., Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: Gender-dependent effects. Brain Research. Developmental Brain Research. 113:1999;97-106.
53. Meaney M.J., Aitken D.H., Bhatnagar S., Sapolsky R.M. Postnatal handling attenuates certain neuroendocrine, anatomical, and cognitive dysfunctions associated with aging in female rats. Neurobiology of Aging. 12:1991;31-38.
54. 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.
55. Nunez J.F., Ferre P., Escorihuela R.M., Tobena A., Fernandez-Teruel A. Effects of postnatal handling of rats on emotional, HPA-axis, and prolactin reactivity to novelty and conflict. Physiology & Behavior. 60:1996;1355-1359.
56. Nunez J.F., Ferre P., Garcia E., Escorihuela R.M., Fernandez-Teruel A., Tobena A. Postnatal handling reduces emotionality ratings and accelerates two-way active avoidance in female rats. Physiology & Behavior. 57:1995;831-835.
57. 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.
58. Pham T.M., Soderstrom S., Henriksson B.G., Mohammed A.H. Effects of neonatal stimulation on later cognitive function and hippocampal nerve growth factor. Behavioural Brain Research. 86:1997;113-120.
59. Posner M.I., Rothbart M.K. Attention, self-regulation and consciousness. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences. 353:1998;1915-1927.
60. Rakic P. The development of the frontal lobe. A view from the rear of the brain. Advances in Neurology. 66:1995;1-6.
61. Roberts A.C., Wallis J.D. Inhibitory control and affective processing in the prefrontal cortex: Neuropsychological studies in the common marmoset. Cerebral Cortex. 10:2000;252-262.
62. Rolls E.T. The orbitofrontal cortex and reward. Annual Review of Psychology. 51:2000;599-630.
63. Rosabal F. Cytoarchitecture of the frontal lobe of the squirrel monkey. Journal of Comparative Neurology. 130:1967;87-108.
64. Rosenblum L.A., Andrews M.W. Influences of environmental demand on maternal behavior and infant development. Acta Paediatrica Supplement. 397:1994;57-63.
65. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: Effects of training and experience on brain and behavior. Behavioural Brain Research. 78:1996;57-65.
66. 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.
67. 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.
68. Schultz W., Tremblay L., Hollerman J.R. Reward processing in primate orbitofrontal cortex and basal ganglia. Cerebral Cortex. 10:2000;272-284.
69. Smith E.E., Jonides J. Storage and executive processes in the frontal lobes. Science. 283:1999;1657-1661.
70. Squire L.R., Zola S.M. Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences, USA. 93:1996;13515-13522.
71. Stanton M.E., Levine S. Brief separation elevates cortisol in mother and infant squirrel monkeys. Physiology & Behavior. 34:1985;1007-1008.
72. Steimer T., Escorihuela R.M., Fernandez-Teruel A., Driscoll P. Long-term behavioural and neuroendocrine changes in Roman high- (RHA/Verh) and low-(RLA-Verh) avoidance rats following neonatal handling. International Journal of Developmental Neuroscience. 16:1998;165-174.
73. Vallee M., MacCari S., Dellu F., Simon H., Le Moal M., Mayo W. Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: A longitudinal study in the rat. European Journal of Neuroscience. 11:1999;2906-2916.
74. 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.