The Development of Brain and Behavior
Thomas R. Insel
Laboratory of Neurophysiology
National Institute of Mental Health
National Institutes of Health
Poolesville, Maryland 20837
current address:
Yerkes Regional Primate Research Center and Department of Psychiatry
Emory University
Atlanta, Georgia 30322.
REFERENCES
1. Jacobson M. Developmental Neurobiology. New York: Plenum Press, 1991.
2. Purves D, Lichtman JW. Principles of Neural Development. Sunderland: Sinauer Associates, 1985.
3. Parnavelas JG, Papadopoulos GC, Cavanagh ME. Changes in neurotransmitters during development. In: Peters A, Jones EG, eds. Cerebral Cortex, New York: Plenum Press, 1988;177205.
4. Zagon IS, McLaughlin PJ. Receptors in the Developing Nervous System. Growth Factors and Hormones, New York: Chapman & Hall, 1993.
5. Shair HN, Barr GA, Hofer MA. Developmental Psychobiology: New Concepts and Changing Methods, New York: Oxford University Press, 1991.
6. Jacobson M, Rutishauser U. Induction of neural cell adhesion molecule (NCAM) in Xenopus embryos. Dev Biol 1986;116:524531.
7. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. II. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in infant rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 1966;128:431474.
8. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977; 197:10921094.
9. Rakic P. Neuronal-glial interaction during brain development. Trends Neurosci 1981;4:184187.
10. McConnell SK, Ghosh A, Shatz CJ. Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 1989;245:978982.
11. Shatz CJ, Chun JJM, Luskin MB. The role of the subplate in the development of the mammalian telencephalon. In: Jones EG, ed. The Cerebral Cortex, New York: Plenum Press, 1988;3558.
12. Theodosis DT, Rougon G, Poulain DA. Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamoneurohypophysial system. Proc Natl Acad Sci USA 1991;88:54945498.
13. Nowakowski RS. Genetic disturbances of neuronal migration: some examples from the limbic system of mutant mice. In: Mednick SA, Cannon TD, Barr CE, Lyon M, eds. Fetal Neural Development and Adult Schizophrenia, New York: Cambridge University Press, 1991;6996.
14. Stanfield BB, Caviness VS Jr., Cowan WM. The organization of certain afferents to the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 1979;185:461484.
15. Floeter MK, Jones EG. Transplantation of fetal postmitotic neurons to rat cortex: survival, early pathway choices and long-term projections of outgrowing axons. Dev Brain Res 1985;22:1938.
16. Killackey HP, Chalupa LM. Ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. J Comp Neurol 1986;244:331348.
17. Innocenti GM, Clarke S. Bilateral transitory projections to visual areas from auditory cortex in kittens. Dev Brain Res 1984;14:143148.
18. Stanfield BB, O'Leary DD, Fricks C. Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurons. Nature 1982;298:371373.
19. Burkhalter A, Bernardo KL. Organization of corticocortical connections in human visual cortex. Proc Natl Acad Sci USA 1989; 86:10711075.
20. Godement P, Vanselow J, Thanos S, Bonhoeffer F. A study in developing visual system with a new method of staining neurones and their processes in fixed tissue. Development 1987;101:697713.
21. Korsching S. The neurotrophic factor concept: a reexamination. J Neurosci 1993;13:27392748.
22. Lin L-FH, Doherty DH, Lile JD, Bektesh S, Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993;260:11301132.
23. Cowan WM, Fawcett JW, O'Leary DDM, Stanfield BB. Regressive events in neurogenesis. Science 1984;225:12581265.
24. Sulston JE. Postembryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 1976;56:110156.
25. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239257.
26. Huttenlocher PR. Synaptic density in human frontal cortexdevelopmental changes and effects of aging. Brain Res 1979;163:195205.
27. Lichtman JW, Purves D. The elimination of redundant preganglionic innervation to hamster sympathetic ganglion cells in early post-natal life. J Physiol 1980;301:213228.
28. Purves D, Lichtman JW. Elimination of synapes in the developing nervous system. Science 1980;210:153157.
29. Jerison H. Brain size. In: Adelman G, ed. Encyclopedia of Neuroscience, Boston: Birkhauser, 1985;168170.
30. Yakovlev PI, Lecours A-R. The myelogenetic cycles of regional maturation of the brain. In: Minkowski A, ed. Regional Development of the Brain in Early Life, Oxford: Blackwell, 1967.
31. Black IB. Stages of neurotransmitter development in autonomic neurons. Science 1982;215:11981204.
32. Lauder JM, Krebs H. Do neurotransmitters, neurohumors, and hormones specify critical periods? In: Greenough WT, Juraska JM, eds. Developmental Neuropsychobiology, New York: Academic Press, 1986;119174.
33. Jones EG. The development of the primate neocortexan overview. In: Mednick SA, Cannon TD, Barr CE, Lyon M, eds. Fetal Neural Development and Adult Schizophrenia, New York: Cambridge University Press, 1991;4065.
34. Levitt P, Moore RY. Development of the noradrenergic innervation of neocortex. Brain Res 1979;162:243259.
35. Hohman CF, Hamon R, Batshaw ML, Coyle JT. Transient postnatal elevation of seotonin levels in mouse neocortex. Dev Br Res 1988;43:163166.
36. D'Amato RJ, Blue ME, Largent BL. Ontogeny of the serotonergic projection to rat neocortex: Transient expression of a dense innervation to primary sensory areas. Proc Natl Acad Sci USA 1987; 84:43224326.
37. Kvale I, Fosse VM, Fonnum F. Development of neurotransmitter parameters in lateral geniculate body, superior colliculus and visual cortex of the albino rat. Dev Brain Res 1983;7:137145.
38. Coyle JT, Yamamura HI. Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res 1976;118:429440.
39. Dori I, Parnavelas JG, Eckenstein F. The postnatal developmental of the cholinergic system in the rat visual cortex. Neurosci Lett [Suppl] 1985;22:S354.
40. Bear MF, Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 1986;320:172176.
41. Huntley GW, Hendry SHC, Killackey HP, Chalupa LM, Jones EG. Temporal sequence of neurotransmitter expression by developing neurons of fetal monkey visual cortex. Dev Brain Res 1988;43:6996.
42. Goldfarb J, Cantin C, Cohen MW. Intracellular and surface acetylcholine receptors during normal development of a frog skeletal muscle. J Neurosci 1990;10:500507.
43. Roth BL, Hamblin MW, Ciaranello RD. Developmental regulation of 5-HT2 and 5-HT1C mRNA and receptor levels. Dev Brain Res 1991;58:5158.
44. Insel TR. Long-term neural consequences of stress during development: Is early experience a form of chemical imprinting? In: Carroll BJ, Barrett JE, eds. Psychopathology and the Brain, New York: Raven Press, 1991;133152.
45. Milligan G, Streaty R, Gierschik P, Spiegel AM, Klee WE. Development of opiate receptors and GTP-binding regulatory proteins in neonatal rat brains. J Biol Chem 1987;262:86268630.
46. Enjalbert A, Bourgoin S, Hamon M, Adrien J, Bockaert J. Postsynaptic serotonin-sensitive adenylate cyclase in the central nervous system. Mol Pharmacol 1978;14:210.
47. Nicoletti F, Iadorola MJ, Wroblewski JT, Costa E. Excitatory amino acid recognition sites couples with inositol phospholipid metabolism: developmental changes and interaction with alpha-1 adrenoreceptors. Proc Natl Acad Sci USA 1986;83:19311935.
48. Insel TR, Battablia G, Fairbanks DW, De Souza EB. The ontogeny of brain receptors for corticotropin-releasing factor and the development of their functional association with adenylate cyclase. J Neurosci 1988;8:41514158.
49. Hamburger V, Wenger E, Oppenheim R. Motility in the chick embryo in the absence of sensory input. J Exp Zool 1966;162:133160.
50. Smotherman WP, Robinson SR. Accessibility of the rat fetus for investigation. In: Shair HN, Barr GA, Hofer MA, eds. Developmental Psychobiology: New Concepts and Changing Methods, New York: Oxford University Press, 1991;148163.
51. Kagan J, Snidman N. Temperamental factors in human development. Am Psychol 1991;46:856862.
52. Hofer MA. Relationships as regulators: a psychobiologic perspective on bereavement. Psychosom Med 1984;46:183197.
53. Kuhn CM, Pauk J, Schanberg SM. Endocrine responses to mother-infant separation in developing rats. Dev Psychobiol 1990;23:395410.
54. Stanton ME, Levine S. Inhibition of infant glucocorticoid stress response: specific role of maternal cues. Dev Psychobiol 1990; 23:411426.
55. Singer W. Neuronal activity as a shaping factor in postnatal development of visual cortex. In: Greenough WT, Juraska JM, eds. Developmental Neuropsychobiology Orlando: Academic Press, 1986; 271293.
56. Kaas J, Merzenich MM, Killackey HP. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing animals. Ann Rev Neurosci 1983;6:325356.
57. Knudsen E. Experience alters the spatial tuning of auditory units in the optic tectum during a sensitive period. J Neurosci 1985;5:30943109.
58. Knudsen E, Knudsen P. The sensitive period for auditory localization in barn owls is limited by age, not experience. J Neurosci 1986;6:19181924.
59. Hubel DH, Wiesel TN, LeVay S. Plasticity of ocular dominance columns in monkey genesis. Phil Trans R Soc Lond 1977;278.
60. Spinelli DN, Hirsch HVB, Phelps RW, Metzler J. Visual experience as a determinant of the response characteristics of cortical receptive fields in cats. Exp Brain Res 1972;15:289304.
61. Blakemore C, Cooper GF. Development of the brain depends on the visual environment. Nature 1970;228:477478.
62. Greenough WT. What's special about development? Thoughts on the basis of experience-psychobiology. In: Greenough WT, Juraska JM, eds. Developmental Neuropsychobiology, Orlando: Academic Press, 1986;387407.
63. Hebb DO. The Organization of Behavior. New York: John Wiley & Sons, 1949.
64. Phoenix CH, Gor RW, Gerall AA, Young WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the guinea pig. Endo 1959;65:369382.
65. MacLusky NJ, Naftolin F. Sexual differentiation of the central nervous system. Science 1981;211:1294.
66. Goy RW, McEwen BS. Sexual Differentiation of the Brain. Cambridge: MIT Press, 1980.
67. MacLusky NJ, Chaptal C, McEwen BS. The development of estrogen receptor systems in the rat brain and pituitary: postnatal development. Brain Res 1979;178:143160.
68. Ward IL. Prenatal stress feminizes and demasculinizes the behavior of males. Science 1972;175:8284.
69. Ward IL, Weisz J. Maternal stress alters plasma testosterone in fetal males. Science 1980;207:328329.
70. Toran-Allerand CD, Gerlach JL, McEwen BS. Autoradiographic localization of [3H] estradiol related to steroid responsiveness in cultures of the newborn mouse hypothalamus and preoptic area. Brain Res 1980;184:517522.
71. Wright LL, Smolen AJ. The role of neuron death in the development of the gender difference in the number of neurons in the rat superior cervical ganglion. Int J Dev Neurosci 1987;5:305311.
72. Diamond MC. Sex differences in the rat forebrain. Brain Res 1987;12:235240.
73. Allen LS, Hines M, Shryne JE, Gorski RA. Two sexually dimorphic cell groups in the human brain. J Neurosci 1989;9:497506.
74. Swaab DF, Fliers EA. A sexually dimorphic nucleus in the human brain. Science 1985;228:11121115.
75. Arnold AP, Breedlove SM. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 1985;19:469498.
76. Rosengarten H, Friedhoff AJ. Enduring changes in dopamine receptor cells of pups from drug administration to pregnant and nursing rats. Science 1979;203:11331135.
77. Handelmann GE. A developmental role of neuropeptides. J Physiol 1985;80:268274.
78. Boer GJ, Swaab DF. Neuropeptide effects on brain development to be expected from behavioral teratology. Peptides 1985;6:2128.
79. Meriney SD, Gray DB, Pilar G. Morphine-induced delay of normal cell death in the avian ciliary ganglion. Science 1985;228:14511453.
80. Bardo MT, Schmidt RH, Bhatnagar RK. Effects of morphine on sprouting of locus coeruleus fibers in the neonatal rat. Dev Brain Res 1985;22:161168.
81. Hauser KF, McLaughlin PJ, Zagon IS. Endogenous opioids regulate dendritic growth and spine formation in developing rat brain. Brain Res 1987;416:157161.
82. Kennard M. Reorganization of motor function in the cerebral cortex of monkeys deprived of motor and premotor areas in infancy. J Neurophysiol 1938;1:477496.
83. Keilhoff G, Wolf G, Stastny F, Schmidt W. Quinolinate neurotoxicity and glutamatergic structures. Neuroscience 1990;34:235242.
84. Weihmuller FB, Bruno JP. Age-dependent plasticity in the dopaminergic control of sensorimotor development. Behav Br Res 1989;35:95109.
85. Winslow JT, Insel TR. Serotonergic modulation of rat pup ultrasonic vocal development: Studies with 3,4-methylenedioxymethamphetamine. J Pharmacol Exp Ther 1990;254:212220.
86. Almli CR, Finger S. Early Brain Damage, Orlando: Academic Press, 1984.
87. Reinstein DK, Isaacson RL. Clonidine sensitivity in the developing rat. Brain Res 1977;135:378382.
88. Hartley EJ, Seeman P. Development of receptors for dopamine and noradrenaline in rat brain. Eur J Pharmacol 1983;91:391397.
89. Smythe JW, Pappas BA. Neonatal 6-hydroxydopamine potentiates clonidine's locomotor effects throughout maturation in the rat. Pharmacol Biochem Behav 1985;22:10751078.
90. Sargent Jones L, Gauger LL, Davis JN, Slotkin TA, Bartolome JV. Postnatal development on brain alpha1-adrenergic receptors: in vitro autoradiography with [125I]heat in normal rats and rats treated with alpha-difluoromethylornithine, a specific, irreversible inhibitor of ornithine decarboxylase. Neurosci 1985;15:11951202.
91. Saunders NR, Mollgard K. Development of the blood-brain barrier. J Dev Physiol 1984;6:4557.
published 2000