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New evidence for neurotransmitter influences on brain development
Abstract
The early appearance of monoamine systems in the developing mammalian CNS suggests that they play a role in neural development. We review data from two model systems that provide compelling new evidence of this role. In one model system-in utero exposure to cocaine-specific and robust alterations are seen in dopamine-rich areas of the cerebral cortex, such as the anterior cingulate cortex: D1 receptor-G protein coupling is greatly reduced, the GABAergic system is altered and pyramidal dendrites undergo excessive growth. In a second model system-a transgenic mouse line in which the gene that encodes monoamine oxidase A (MAOA) is disrupted, resulting in excessively high 5-HT levels-barrels fail to form in the developing somatosensory cortex. Both models reveal the effects of very early manipulation of monoamines on forebrain development, and the long-term anomalies that persist into adulthood.
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“Specific genes (e.g., 5-HTTLPR; (112, 113)) influencing neuromaturation have known associations with self-injurious behaviors (114, 115).”
From Neural correlates associated with suicide and nonsuicidal self-injury in youth (2021) · cites this paper as [113]
Citations
Cites
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0626 · Cited by 4,726
Psychopharmacology: The third generation of progress
O’Connell, R. A. (1988) · Comprehensive Psychiatry · doi:10.1016/0010-440x(88)90057-0 · Cited by 3,020
Drugs of abuse: anatomy, pharmacology and function of reward pathways
Koob, G. F. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90060-j · Cited by 2,070
Psychopharmacology: The Third Generation of Progress.
(1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-108-3-509_2 · Cited by 2,021
Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse
ANGEVINE, J. B., & SIDMAN, R. L. (1961) · Nature · doi:10.1038/192766b0 · Cited by 1,530
Neuronal migration, with special reference to developing human brain: a review
Sidman, R. L., & RAKIC, P. T. (1973) · Brain Research · doi:10.1016/0006-8993(73)90617-3 · Cited by 1,260
Aggressive Behavior and Altered Amounts of Brain Serotonin and Norepinephrine in Mice Lacking MAOA
Cases, O., Seif, I., Grimsby, J. S., Gaspar, P., Chen, K., Vandormael‐Pournin, S., Müller, U., Aguet, M., Babinet, C., Shih, J. C., et al. (1995) · Science · doi:10.1126/science.7792602 · Cited by 1,225
Rakic, P. (1974) · Science · doi:10.1126/science.183.4123.425 · Cited by 1,161
Lipsitt, L. P., & Rovee‐Collier, C. (1981) · Ablex Publishing Corp. eBooks · Cited by 1,146
Moore, R. Y., & Bloom, F. E. (1979) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.02.030179.000553 · Cited by 1,118
The dopamine hypothesis of the reinforcing properties of cocaine
Kuhar, M. J., Ritz, M. C., & Boja, J. W. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90141-g · Cited by 1,005
Central Catecholamine Neuron Systems: Anatomy and Physiology of the Dopamine Systems
Moore, R. Y., & Bloom, F. E. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001021 · Cited by 931
Modulation of visual cortical plasticity by acetylcholine and noradrenaline
Bear, M. F., & Singer, W. (1986) · Nature · doi:10.1038/320172a0 · Cited by 858
Neurotransmitters as growth regulatory signals: role of receptors and second messengers
Lauder, J. M. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90162-f · Cited by 806
Neurobiology of Cingulate Cortex and Limbic Thalamus
Vogt, B. A., & Gabriel, M. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6704-6 · Cited by 777
Embryonic vertebrate central nervous system: Revised terminology
Angevine, J. B., Bodian, D., Coulombre, A. J., Edds, M. V., Hamburger, V., Jacobson, M., Lyser, K. M., Prestige, M. C., Sidman, R. L., Varon, S. S., et al. (1970) · The Anatomical Record · doi:10.1002/ar.1091660214 · Cited by 727
Lauder, J. M., & Bloom, F. E. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901550407 · Cited by 658
The Biology of the Laboratory Rabbit
(1974) · Elsevier eBooks · doi:10.1016/c2013-0-11681-9 · Cited by 619
From neuropathology to neurodevelopment
Weinberger, D. R. (1995) · The Lancet · doi:10.1016/s0140-6736(95)91386-6 · Cited by 558
Development of the dopaminergic innervation in the prefrontal cortex of the rat
Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., & Uylings, H. B. M. (1988) · Journal of Comparative Neurology · doi:10.1002/cne.902690105 · Cited by 545
Neurotransmitters in the regulation of neuronal cytoarchitecture
Mattson, M. P. (1988) · Brain Research Reviews · doi:10.1016/0165-0173(88)90020-3 · Cited by 518
Cases, O., Vitalis, T., Seif, I., Maeyer, E. D., Sotelo, C., & Gaspar, P. (1996) · Neuron · doi:10.1016/s0896-6273(00)80048-3 · Cited by 514
Olson, L., & Seiger, �. (1972) · Anatomy and Embryology · doi:10.1007/bf00519099 · Cited by 501
Morris, R. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)60029-0 · Cited by 479
Kasamatsu, T., & Pettigrew, J. D. (1976) · Science · doi:10.1126/science.959850 · Cited by 436
The serotonin innervation of the cerebral cortex in the rat—an immunohistochemical analysis
Lidov, H. G. W., Grzanna, R., & Molliver, M. E. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90099-8 · Cited by 417
Neurobiology of cingulate cortex and limbic thalamus : a comprehensive handbook
Vogt, B. A., & Gabriel, M. (1993) · Medical Entomology and Zoology · Cited by 378
Immunohistochemical study of the development of serotonergic neurons in the rat CNS
Lidov, H. G. W., & Molliver, M. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90164-2 · Cited by 376
Carlos, J. D., & O'Leary, D. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-04-01194.1992 · Cited by 339
Xu, M., Hu, X., Cooper, D., Moratalla, R., Graybiel, A. M., White, F. J., & Tonegawa, S. (1994) · Cell · doi:10.1016/0092-8674(94)90026-4 · Cited by 333
Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages
Woolsey, T. A., & Wann, J. R. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901700105 · Cited by 330
Lewis, D., Campbell, M., Foote, S., Goldstein, M., & Morrison, J. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-01-00279.1987 · Cited by 325
Lankford, K. L., DeMello, F. G., & Klein, W. L. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.8.2839 · Cited by 307
Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys
Goldman, P. S., & Brown, R. M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90146-8 · Cited by 285
Neurotransmitters as developmental signals
Meier, E., Hertz, L., & Schousboe, A. (1991) · Neurochemistry International · doi:10.1016/0197-0186(91)90113-r · Cited by 278
Noradrenaline neuron innervation of the neocortex in the rat
Levitt, P., & Moore, R. Y. (1978) · Brain Research · doi:10.1016/0006-8993(78)90925-3 · Cited by 270
A role for subplate neurons in the patterning of connections from thalamus to neocortex
Ghosh, A., & Shatz, C. J. (1993) · Development · doi:10.1242/dev.117.3.1031 · Cited by 263
Dopamine D1 receptors facilitate transmitter release
Cameron, D. L., & Williams, J. T. (1993) · Nature · doi:10.1038/366344a0 · Cited by 263
Neurotransmitters as morphogens
Lauder, J. M. (1988) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60516-6 · Cited by 257
Olson, L., Bor�us, L. O., & Seiger, �. (1973) · Anatomy and Embryology · doi:10.1007/bf00519968 · Cited by 255
Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat.
Catalano, S. M., Robertson, R. T., & Killackey, H. P. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.8.2999 · Cited by 231
Development of the noradrenergic innervation of neocortex
Levitt, P., & Moore, R. Y. (1979) · Brain Research · doi:10.1016/0006-8993(79)90287-7 · Cited by 214
Schambra, U. B., Duncan, G. E., Breese, G. R., Fornaretto, M. G., Caron, M. G., & Fremeau, R. T. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90315-8 · Cited by 209
Levitt, P. R., RAKIC, P. T., & Goldman, P. S. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902270105 · Cited by 190
Todd, R. D. (1992) · Biological Psychiatry · doi:10.1016/0006-3223(92)90311-m · Cited by 187
SPEAR, L. P., Kirstein, C. L., & Frambes, N. A. (1989) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1989.tb21027.x · Cited by 184
Zecevic, N., & Verney, C. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903510404 · Cited by 149
Structural and functional effects of prenatal cocaine exposure in adult rat brain
Dow-Edwards, D. L., Freed, L. A., & Fico, T. A. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90052-z · Cited by 149
Levitt, P. R., & RAKIC, P. T. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90095-5 · Cited by 145
Prenatal cocaine exposure disrupts the development of the serotonergic system
Akbari, H. M., Kramer, H. K., Whitaker‐Azmitia, P. M., SPEAR, L. P., & Azmitia, E. C. (1992) · Brain Research · doi:10.1016/0006-8993(92)90450-n · Cited by 140
Innervation of embryonic rat cerebral cortex by catecholamine‐containing fibers
Schlumpf, M., Shoemaker, W. J., & Bloom, F. E. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901920210 · Cited by 132
Cocaine-induced disturbances of corticogenesis in the developing murine brain
Gressèns, P., Kosofsky, B. E., & Evrard, P. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90694-3 · Cited by 125
Growth and Development of the Rabbit Brain
Harel, S., Watanabe, K. S., Linke, I., & Schain, R. J. (2009) · Biology of the Neonate · doi:10.1159/000240527 · Cited by 121
Long‐Term Neurochemical and Neurobehavioral Consequences of Cocaine Use during Pregnancya
Dow-Edwards, D. L. (1989) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1989.tb21026.x · Cited by 110
Emergence of Connectivity in the Embryonic Rat Parietal Cortex
Erzurumlu, R. S., & Jhaveri, S. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.4.336 · Cited by 106
Wang, H. Y., Runyan, S., Yadin, E., & Friedman, E. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)09613-2 · Cited by 105
Schwartz, M. L., RAKIC, P. T., & RAKIC, P. T. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.4.1354 · Cited by 102
Jones, L. B., Fischer, I., & Levitt, P. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.431 · Cited by 99
Rodrigues, P. D. S., & Dowling, J. E. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.24.9693 · Cited by 99
The effect of neonatal 6‐hydroxydopamine treatment on synaptogenesis in the visual cortex of the rat
Blue, M. E., & Parnavelas, J. G. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902050211 · Cited by 93
Short, A. L. (1995) · Toxicology Letters · doi:10.1016/0378-4274(95)90249-x · Cited by 93
Lankford, K. L., Mello, F. G. D., & Klein, W. L. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90292-8 · Cited by 87
Friedman, E., Yadin, E., & Wang, H. Y. (1996) · Neuroscience · doi:10.1016/s0306-4522(96)83011-9 · Cited by 84
Lidov, H. G. W., Molliver, M. E., & Zečević, N. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901810311 · Cited by 77
Seidler, F. J., & Slotkin, T. A. (1992) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)10365-0 · Cited by 77
Freeman, J. H., Cuppernell, C., Flannery, K., & Gabriel, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-04-01538.1996 · Cited by 75
Tennyson, V. M., Mytilineou, C., & Barrett, R. E. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901490208 · Cited by 69
Akbari, H. M., & Azmitia, E. C. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90093-c · Cited by 64
D�rries, U., Taylor, J., Xiao, Z., Lochter, A., Montag, D., & Schachner, M. (1996) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19960215)43:4 · Cited by 62
Wang, X.-H., Levitt, P. R., Grayson, D. R., & Murphy, E. H. (1995) · Brain Research · doi:10.1016/0006-8993(95)00528-x · Cited by 61
Goldberg, J. I., Mills, L. R., & Kater, S. B. (1991) · Journal of Neurobiology · doi:10.1002/neu.480220208 · Cited by 60
Prenatal exposure to cocaine disrupts discrimination learning in adult rabbits
Romano, A. G., & Harvey, J. A. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02061-6 · Cited by 59
Reader, T. A., Masse, P., & de Champlain, J. (1979) · Brain Research · doi:10.1016/0006-8993(79)90467-0 · Cited by 56
Tilson, H. A., & Harry, G. J. (2002) · CRC Press eBooks · doi:10.1201/9780203219096-9 · Cited by 53
Lidow, M. S., & RAKIC, P. T. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-07-04064.1994 · Cited by 48
Simansky, K. J., & Kachelries, W. J. (1996) · Neuropharmacology · doi:10.1016/0028-3908(95)00151-4 · Cited by 47
Potential mechanisms of cocaine-induced developmental neurotoxicity: a minireview.
Olsen, G. D. (1995) · PubMed · Cited by 46
Prenatal cocaine administration stimulates fetal brain tyrosine hydroxylase activity
Meyer, J. S., & Dupont, S. A. (1993) · Brain Research · doi:10.1016/0006-8993(93)90783-j · Cited by 46
Wang, X., Jenkins, A., Choi, L., & Murphy, E. H. (1996) · Experimental Brain Research · doi:10.1007/bf00227942 · Cited by 44
The rabbit as a model for studies of cocaine exposure in utero.
Eh, M., Jg, H., Schumann, M. D., My, G., Xh, W., Jones, L., Ag, R., & Harvey, J. A. (1995) · PubMed · Cited by 35
Aceves, J., Florán, B., Martínez‐Fong, D., Benitez, J., Sierra, A., & Flores, G. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90198-g · Cited by 33
Wang, X., Levitt, P. R., Jenkins, A., & Murphy, E. H. (1996) · Brain Research · doi:10.1016/0006-8993(96)00012-1 · Cited by 27
Fantel, A. G., & Shepard, T. H. (1990) · Reproductive Toxicology · doi:10.1016/0890-6238(90)90001-c · Cited by 17
Prenatal cocaine treatment reduces haloperidol-induced catalepsy on postnatal day 10
Meyer, J. S., Robinson, P., & Todtenkopf, M. S. (1994) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(94)90117-1 · Cited by 16
Stadlin, A., Choi, H. L., Tsim, K. W. K., & Tsang, D. (1995) · Molecular Neurobiology · doi:10.1007/bf02740685 · Cited by 15
Goodwin, G. A., Rajachandran, L., Moody, C. A., Francis, R., Kuhn, C. M., & SPEAR, L. P. (1995) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(95)00010-o · Cited by 9
Research works printed but not linked: 13
- Olsen, 1995, Neurotoxicology, 16, 159
- Spear, 1995, Vol. 9, 55
- Seidler, 1992, J. Pharmacol. Exp. Ther., 263, 413
- Battaglia, 1995, NIDA Res. Monogr. Ser., 158, 115
- Lidow, 1994, Soc. Neurosci. Abstr., 20, 596
- Murphy, 1995, Lab. Anim. Sci., 45, 163
- Breslin, N.A. and Weinberger, D.R. (1991) in Fetal Neural Development and Adult Schizophrenia (Mednick, S.A. et al., eds), pp. pp. 199–215, Cambridge University Press
- Wang, 1997, Exp. Brain Res., 112, 359
- Murphy, E.H. et al. Exp. Brain Res. (in press)
- Wang, 1995, J. Pharmacol. Exp. Ther., 273, 492
- Grayson, 1941, Soc. Neurosci. Abstr., 22
- Wang, 1996, Brain Res., 715, 221, 10.1016/0006-8993(96)00012-1 · DOI
- Goldberg, 1989, Dev. Biol., 141, 438
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Behnke, M., Smith, V. C., Behnke, M., Smith, V. C., Levy, S., Ammerman, S. D., Gonzalez, P. K., Ryan, S. A., Smith, V. C., Wunsch, M. J., et al. (2013) · PEDIATRICS · doi:10.1542/peds.2012-3931 · Cited by 603
Metadata
- Authors
- Levitt, P., Harvey, J. A., Friedman, E., Simansky, K., & Murphy, E. H.
- Affiliations
- University of Pittsburgh (US)
- Venue
- Trends in Neurosciences
- Publisher
- Elsevier BV
- Published
- 1997-06
- Volume
- 20
- Issue
- 6
- Pages
- 269-274
- ISSN
- 0166-2236 (ISSN-L)
- OpenAlex
- W2167345246
- Cited by
- 362
- References
- 86
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 7 · 2023: 2 · 2022: 9 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 5 · 2016: 7 · 2015: 6 · 2014: 5 · 2013: 11 · 2012: 11
- FWCI
- 2.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Neurosciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p01da006871-04)
- National Institute on Drug Abuse (P01DA06871)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- monoaminergic systems, brain development, dopamine, dopamine D1 receptor, G protein coupling, GABAergic system, anterior cingulate cortex, monoamine oxidase A, serotonin, somatosensory cortex, transgenic mice, forebrain development, developmental neurotoxicity
- MeSH terms
- Animals, Brain, Cocaine, Female, Mice, Transgenic, Pregnancy, Prenatal Exposure Delayed Effects, Neurotransmitter Agents, Mice
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