Convergence and Plasticity of Monoaminergic Systems in the Medial Prefrontal Cortex during the Postnatal Period: Implications for the Development of Psychopathology
Abstract
A variety of observations have suggested that the dopamine and serotonin systems may play a role in the pathophysiology and treatment of major mental disorders of childhood, adolescence and early adulthood. A recent triple immunofluorescence study has demonstrated a convergence of serotonin and dopamine fibers onto both pyramidal cells and GABAergic interneurons in the rat medial prefrontal cortex (mPFCx). These findings are consistent with the results of an electrophysiological study conducted in another laboratory that suggested such a relationship exists in the pyriform cortex of the rodent brain. During postnatal development, the dopamine system shows a progressive ingrowth of fibers into this region that continues until the early adult period. In contrast, GABAergic neurons appear to complete their postnatal maturation by the fourth postnatal week (the early post-weanling period). As dopamine fibers infiltrate the rat mPFCx, they progressively increase their interaction with neural elements within the neuropil and with the cell bodies of both pyramidal cells and GABAergic interneurons. This process appears to be influenced by the serotonin system, since lesioning of the nucleus raphe dorsalis during the neonatal period results in a significant increase of dopamine fibers. This finding suggests that lesions of the serotonin system induce plasticity of the cortical dopamine system; however, it is not known whether this inferred suppressive effect of serotonin fibers occurs at brainstem levels or within the mPFCx itself. Taken together, these various studies suggest that the convergence of dopamine and serotonin fiber systems on intrinsic cortical neurons shows considerable plasticity during postnatal life that could theoretically contribute to the development of 'miswired' circuits in individuals with neuropsychiatric disorders.
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The dopaminergic innervation of the mPFC in rodent surges during adolescence, hallmarked by massive changes in the organization, shape and density of the dopaminergic fibers.
“The dopaminergic innervation of the mPFC in rodent surges during adolescence hallmarked by massive changes in the organization, shape and density of the dopaminergic fibers [162–164].”
From Development of prefrontal cortex (2022) · cites this paper as [163]
Cites
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
Implications of Normal Brain Development for the Pathogenesis of Schizophrenia
Weinberger, D. R. (1987) · Archives of General Psychiatry · doi:10.1001/archpsyc.1987.01800190080012 · Cited by 3,724 · see citing works
Modulation of memory fields by dopamine Dl receptors in prefrontal cortex
Williams, G. V., & Goldman-Rakic, P. S. (1995) · Nature · doi:10.1038/376572a0 · Cited by 1,593 · see citing works
Cognitive Deficit Caused by Regional Depletion of Dopamine in Prefrontal Cortex of Rhesus Monkey
Brozoski, T. J., Brown, R. M., Rosvold, H. E., & Goldman, P. S. (1979) · Science · doi:10.1126/science.112679 · Cited by 1,500 · see citing works
Selective activation of the mesocortical DA system by stress
Thierry, A. M., Tassin, J., BLANC, G., & Glowinski, J. (1976) · Nature · doi:10.1038/263242a0 · Cited by 1,033 · see citing works
Schizophrenia: A neural diathesis-stress model.
Walker, E. F., & Diforio, D. (1997) · Psychological Review · doi:10.1037//0033-295x.104.4.667 · Cited by 930 · see citing works
The Dopamine Hypothesis of Schizophrenia: A Review*
Meltzer, H. Y., & Stahl, S. M. (1976) · Schizophrenia Bulletin · doi:10.1093/schbul/2.1.19 · Cited by 883 · see citing works
Prenatal developmental disturbances in the limbic allocortex in schizophrenics
Jakob, H., & Beckmann, H. (1986) · Journal of Neural Transmission · doi:10.1007/bf01249090 · Cited by 875 · see citing works
Benes, F. M. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950060041004 · Cited by 744 · see citing works
Self-citationNeurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain
Coyle, J. T., & Yamamura, H. I. (1976) · Brain Research · doi:10.1016/0006-8993(76)90310-3 · Cited by 732 · see citing works
Dopamine D4 receptors elevated in schizophrenia
Seeman, P. M., Guan, H., & Tol, H. H. M. V. (1993) · Nature · doi:10.1038/365441a0 · Cited by 627 · see citing works
Postnatal maturation of the GABAergic system in rat neocortex
Luhmann, H. J., & Prince, D. A. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.65.2.247 · Cited by 575 · see citing works
Noradrenergic mechanisms in stress and anxiety: I. preclinical studies
Bremner, J., Krystal, J., Southwick, S., & Charney, D. (1996) · Synapse · doi:10.1002/(sici)1098-2396(199605)23:1 · Cited by 571 · see citing works
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 · see citing works
Jakab, R. L., & Goldman-Rakic, P. S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.2.735 · Cited by 536 · see citing works
INCREASED DOPAMINE-RECEPTOR SENSITIVITY IN SCHIZOPHRENIA
Owen, F., Crow, T. J., Poulter, M., Cross, A. J., Longden, A., & Riley, G. J. (1978) · The Lancet · doi:10.1016/s0140-6736(78)91740-3 · Cited by 517 · see citing works
Bergson, C. M., Mrzljak, L., Smiley, J., Pappy, M., Levenson, R. G., & Goldman-Rakic, P. S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-12-07821.1995 · Cited by 488 · see citing works
Myelination of Cortical-hippocampal Relays During Late Adolescence
Benes, F. M. (1989) · Schizophrenia Bulletin · doi:10.1093/schbul/15.4.585 · Cited by 448 · see citing works
Self-citationDopamine synaptic complex with pyramidal neurons in primate cerebral cortex.
Goldman-Rakic, P. S., Leranth, C., Williams, S. M., Mons, N. E., & Geffard, M. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.22.9015 · Cited by 433 · see citing works
Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics
BEASLEY, C., & REYNOLDS, G. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(96)00122-3 · Cited by 426 · see citing works
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 · see citing works
Organization of catecholamine neurons projecting to the frontal cortex in the rat
Lindvall, O., Björklund, A., & Divac, I. (1978) · Brain Research · doi:10.1016/0006-8993(78)90173-7 · Cited by 412 · see citing works
A subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia
Woo, T.-U. W., Whitehead, R. E., Melchitzky, D. S., & Lewis, D. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5341 · Cited by 410 · see citing works
Increased Brain Dopamine and Dopamine Receptors in Schizophrenia
Mackay, A. V. P. (1982) · Archives of General Psychiatry · doi:10.1001/archpsyc.1982.04290090001001 · Cited by 399 · see citing works
Smiley, J. F., Levey, A. I., Ciliax, B. J., & Goldman‐Rakic, P. S. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.12.5720 · Cited by 383 · see citing works
Yang, C., & Seamans, J. K. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01922.1996 · Cited by 369 · see citing works
Neurochemical aspects of the ontogenesis of gabanergic neurons in the rat brain
Coyle, J. T., & Enna, S. J. (1976) · Brain Research · doi:10.1016/0006-8993(76)91053-2 · Cited by 352 · see citing works
Stress and the Mesocorticolimbic Dopamine Systemsa
ROTH, R. H., TAM, S., IDA, Y., YANG, J., & DEUTCH, A. Y. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb42102.x · Cited by 342 · see citing works
Anatomie des menschlichen Gehirns und Rückenmarks : auf myelogenetischer Grundlage
Flechsig, P. (1920) · Medical Entomology and Zoology · Cited by 341 · see citing works
Serotonin Uptake Sites and Serotonin Receptors Are Altered in the Limbic System of Schizophrenics
Joyce, J. N., Shane, A. L., Lexow, N., Winokur, A., Casanova, M. F., & Kleinman, J. E. (1993) · Neuropsychopharmacology · doi:10.1038/npp.1993.32 · Cited by 340 · see citing works
Gaspar, P., Bloch, B., & Le Moine, C. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01092.x · Cited by 323 · see citing works
Dopamine receptors and transporters in Parkinson's disease and schizophrenia
Seeman, P. M., & Niznik, H. B. (1990) · The FASEB Journal · doi:10.1096/fasebj.4.10.2197154 · Cited by 301 · see citing works
An overview of the mechanism of action of clozapine.
Meltzer, H. Y. (1994) · PubMed · Cited by 288 · see citing works
The origin and distribution of dopamine-containing afferents to the rat frontal cortex
Emson, P. C., & Koob, G. F. (1978) · Brain Research · doi:10.1016/0006-8993(78)90634-0 · Cited by 287 · see citing works
D'Amato, R. J., Blue, M. E., Largent, B. L., Lynch, D. R., Ledbetter, D. J., Molliver, M. E., & Snyder, S. H. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.12.4322 · Cited by 275 · see citing works
Benes, F. M., Vincent, S. L., Marie, A. S., & Khan, Y. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00328-4 · Cited by 274 · see citing works
Self-citationCorticosteroids regulate brain hippocampal 5-HT1A receptor mRNA expression
Chalmers, D. T., Kwak, S. K., Mansour, A., Akil, H., & Watson, S. J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00914.1993 · Cited by 265 · see citing works
Microdialysis and SPECT measurements of amphetamine-induced dopamine release in nonhuman primates
Laruelle, M. A., Iyer, R. N., Al‐Tikriti, M. S., Zea‐Ponce, Y., Malison, R. T., Zoghbi, S. S., Baldwin, R. M., Kung, H. F., Charney, D. S., Hoffer, P. B., et al. (1997) · Synapse · doi:10.1002/(sici)1098-2396(199701)25:1 · Cited by 264 · see citing works
Gudelsky, G. A., & Nash, J. F. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.66010243.x · Cited by 252 · see citing works
(3H]MK-801 binding sites in postmortem brain regions of schizophrenic patients
Kornhuber, J., Mack-Burkhardt, F., Riederer, P. F., Hebenstreit, G. F., Reynolds, G. P., Andrews, H., & Beckmann, H. (1989) · Journal of Neural Transmission · doi:10.1007/bf01248936 · Cited by 250 · see citing works
First demonstration of highly specific and sensitive antibodies against dopamine
Geffard, M., Buijs, R. M., Séguéla, P., Pool, C. W., & Moal, M. L. (1984) · Brain Research · doi:10.1016/0006-8993(84)91323-4 · Cited by 250 · see citing works
Neurotransmitter Receptors in Frontal Cortex of Schizophrenics
Bennett, J. P. (1979) · Archives of General Psychiatry · doi:10.1001/archpsyc.1979.01780090013001 · Cited by 250 · see citing works
Modulatory role for biogenic amines in the cerebral cortex. Microiontophoretic studies
Reader, T. A., Ferron, A., Descarries, L., & Jasper, H. H. (1979) · Brain Research · doi:10.1016/0006-8993(79)90420-7 · Cited by 236 · see citing works
Morilak, D. A., Garlow, S. J., & Ciaranello, R. D. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90241-7 · Cited by 231 · see citing works
Implications of Normal Brain Development for the Pathogenesis of Schizophrenia
Siris, S. G. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800350089019 · Cited by 224 · see citing works
Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex
Vincent, S. L., Khan, Y., & Benes, F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02551.1993 · Cited by 223 · see citing works
Self-citationDecreased serotonin S2 and increased dopamine D2 receptors in chronic schizophrenics
Mita, T., Hanada, S., Nishino, N., Kuno, T., Nakai, H., Yamadori, T., Mizoi, Y., & Tanaka, C. (1986) · Biological Psychiatry · doi:10.1016/0006-3223(86)90332-x · Cited by 222 · see citing works
Elevation of brain neuroleptic/dopamine receptors in schizophrenia
Lee, T., & Seeman, P. M. (1980) · American Journal of Psychiatry · doi:10.1176/ajp.137.2.191 · Cited by 219 · see citing works
D1Receptor in Interneurons of Macaque Prefrontal Cortex: Distribution and Subcellular Localization
Muly, E. C., Szigeti‐Buck, K., & Goldman‐Rakic, P. S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10553.1998 · Cited by 217 · see citing works
INCREASED DOPAMINE CONCENTRATION IN LIMBIC AREAS OF BRAIN FROM PATIENTS DYING WITH SCHIZOPHRENIA
Bird, E. D., SPOKES, E. G. S., & Iversen, L. L. (1979) · Brain · doi:10.1093/brain/102.2.347 · Cited by 211 · see citing works
Smiley, J. F., & Goldman-Rakic, P. S. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.3.223 · Cited by 211 · see citing works
Excitation of rat prefrontal cortical neurons by dopamine: An in vitro electrophysiological study
Penit-Soria, J., Audinat, É., & Crépel, F. (1987) · Brain Research · doi:10.1016/0006-8993(87)90509-9 · Cited by 205 · see citing works
Deficit and hemispheric asymmetry of GABA uptake sites in the hippocampus in schizophrenia
Reynolds, G. P., Czudek, C., & Andrews, H. B. (1990) · Biological Psychiatry · doi:10.1016/0006-3223(90)90039-5 · Cited by 201 · see citing works
Neuromodulatory actions of dopamine on synaptically-evoked neostriatal responses in slices
Levine, M. S., Li, Z., Cepeda, C., Cromwell, H. C., & Altemus, K. L. (1996) · Synapse · doi:10.1002/(sici)1098-2396(199609)24:1 · Cited by 200 · see citing works
Dopamine Decreases the Excitability of Layer V Pyramidal Cells in the Rat Prefrontal Cortex
Gulledge, A. T., & Jaffe, D. B. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-09139.1998 · Cited by 200 · see citing works
Reduced GABA uptake sites in the temporal lobe in schizophrenia
Simpson, M. D. C., Slater, P., Deakin, J. F. W., Royston, M. C., & Skan, W. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90819-7 · Cited by 192 · see citing works
Kornhuber, J., Riederer, P. F., Reynolds, G. P., Beckmann, H., Jellinger, K. A., & Gabriel, E. (1989) · Journal of Neural Transmission · doi:10.1007/bf01250639 · Cited by 189 · see citing works
Akbarian, S., Huntsman, M. M., Kim, J. J., Tafazzoli, A., Potkin, S. G., Bunney, W. E., & Jones, E. G. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.6.550 · Cited by 181 · see citing works
Kale'n, P., Rosegren, E., Lindvall, O., & Björklund, A. (1989) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1989.tb00786.x · Cited by 175 · see citing works
Joyce, J. N., Lexow, N., Bird, E., & Winokur, A. (1988) · Synapse · doi:10.1002/syn.890020511 · Cited by 167 · see citing works
Hashimoto, T., Nishino, N., Nakai, H., & Tanaka, C. (1991) · Life Sciences · doi:10.1016/0024-3205(91)90556-q · Cited by 166 · see citing works
Cross, A. J., Crow, T. J., & Owen, F. (1981) · Psychopharmacology · doi:10.1007/bf00432676 · Cited by 164 · see citing works
Sheldon, P. W., & Aghajanian, G. K. (1990) · Brain Research · doi:10.1016/0006-8993(90)91199-q · Cited by 164 · see citing works
Neurotrophic effects of GABA in cultures of embryonic chick brain and retina
Spoerri, P. E. (1988) · Synapse · doi:10.1002/syn.890020104 · Cited by 161 · see citing works
Gellman, R. L., & Aghajanian, G. K. (1993) · Brain Research · doi:10.1016/0006-8993(93)90402-9 · Cited by 160 · see citing works
Séguéla, P., Watkins, K. C., & Descarries, L. (1988) · Brain Research · doi:10.1016/0006-8993(88)91427-8 · Cited by 157 · see citing works
Verney, C., Berger, B., Adrien, J., Vigny, A., & Gay, M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90111-0 · Cited by 147 · see citing works
Mantz, J., Milla, C., Glowinski, J., & Thierry, A. M. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90285-0 · Cited by 147 · see citing works
Verney, C., Alvarez, C., Geffard, M., & Berger, B. (1990) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1990.tb00008.x · Cited by 147 · see citing works
Prenatal and postnatal development of GABA‐accumulating cells in the occipital neocortex of rat
Chronwall, B. M., & Wolff, J. R. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900113 · Cited by 146 · see citing works
Dopamine Receptor Transcript Expression in Striatum and Prefrontal and Occipital Cortex
Meador‐Woodruff, J. H. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830240045007 · Cited by 144 · see citing works
[3H]Muscimol binding sites increased in autopsied brains of chronic schizophrenics
Hanada, S., Mita, T., Nishino, N., & Tanaka, C. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90341-9 · Cited by 140 · see citing works
Cellular colocalization of dopamine D1 and D2 receptors in rat medial prefrontal cortex
Vincent, S. L., Khan, Y., & Benes, F. M. (1995) · Synapse · doi:10.1002/syn.890190207 · Cited by 139 · see citing works
Self-citationDopamine Modulation of Membrane and Synaptic Properties of Interneurons in Rat Cerebral Cortex
Zhou, F.-M., & Hablitz, J. J. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.3.967 · Cited by 136 · see citing works
Serotonin-mediated increase in prefrontal cortex dopamine release: pharmacological characterization.
Iyer, R. N., & Bradberry, C. W. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12836-x · Cited by 131 · see citing works
Sheldon, P. W., & Aghajanian, G. K. (1991) · Synapse · doi:10.1002/syn.890090307 · Cited by 131 · see citing works
Benes, F. M., Sorensen, I., Vincent, S. L., Bird, E. D., & Sathi, M. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.6.503 · Cited by 128 · see citing works
Self-citationBockstaele, E. J. V., Cestari, D. M., & Pickel, V. M. (1994) · Brain Research · doi:10.1016/0006-8993(94)91330-7 · Cited by 126 · see citing works
Tritiated LSD Binding in Frontal Cortex in Schizophrenia
Whitaker, P. M. (1981) · Archives of General Psychiatry · doi:10.1001/archpsyc.1981.01780280046004 · Cited by 126 · see citing works
Ontogeny of GABA and benzodiazepine receptors: Effects of Triton X-100, bromide and muscimol
PALACIOS, J. M., Niehoff, D. L., & Kuhar, M. J. (1979) · Brain Research · doi:10.1016/0006-8993(79)90456-6 · Cited by 124 · see citing works
Linking the Family of D2 Receptors to Neuronal Circuits in Human Brain: Insights into Schizophrenia
Joyce, J. N. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00276-x · Cited by 123 · see citing works
Moine, C. L., & Gaspar, P. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(98)00118-1 · Cited by 117 · see citing works
Acute stress enhances the activity of the GABA receptor-gated chloride ion channel in brain
Schwartz, R. D., Wess, M. J., Labarca, R., Skolnick, P., & Paul, S. M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90692-5 · Cited by 111 · see citing works
Rétaux, S., Besson, M., & Penit-Soria, J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90150-m · Cited by 102 · see citing works
The role of stress and dopamine-GABA interactions in the vulnerability for schizophrenia
Benes, F. M. (1997) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(96)00044-1 · Cited by 102 · see citing works
Self-citationHuntley, G. W., Morrison, J. H., Prikhozhan, A., & Sealfon, S. C. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90107-m · Cited by 100 · cited 4× · see citing works
“the somata of both pyramidal and nonpyramidal neurons probably also serve as non-random targets for these fibers in the rat mPFCx (Verney et al., 1990; Huntley et al., 1992; Benes et al., 1993; Vincent et al., 1993, 1995a; Taylor and Benes, 1996; Davidoff and Benes, 1998; Davidoff et al., 2000).”
BackgroundInfluentialBenes, F. M., Vincent, S. L., & Molloy, R. P. (1993) · Synapse · doi:10.1002/syn.890150405 · Cited by 98 · see citing works
Self-citationMarek, G. J., & Aghajanian, G. K. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00036-5 · Cited by 96 · see citing works
Bruinink, A., LICHTENSTEIGER, W., & Schlumpf, M. (1983) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1983.tb13561.x · Cited by 95 · see citing works
Cytoarchitecture of the entorhinal cortex in schizophrenia
Akil, M., & Lewis, D. A. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.7.1010 · Cited by 93 · see citing works
Krimer, L. S., Jakab, R. L., & Goldman‐Rakic, P. S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-19-07450.1997 · Cited by 85 · see citing works
Changes in Neurotransmitters during Development
Parnavelas, J. G., Papadopoulos, G. C., & Cavanagh, M. E. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_6 · Cited by 84 · see citing works
Benes, F. M., Wickramasinghe, R., Vincent, S. L., Khan, Y., & Todtenkopf, M. S. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00113-3 · Cited by 82 · see citing works
Self-citationThierry, A. M., Douarin, C. L., Penit-Soria, J., Perron, A., & Glowinski, J. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90027-4 · Cited by 79 · see citing works
Deskin, R., Seidler, F. J., Whitmore, W. L., et al. (1981) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1981.tb00419.x · Cited by 79 · see citing works
Reader, T. A. (1981) · Journal of Neural Transmission · doi:10.1007/bf01254910 · Cited by 75 · see citing works
Broderick, P. A., & Phelix, C. F. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00048-6 · Cited by 72 · see citing works
Development and Characterization of Monoclonal Antibodies Specific to the Serotonin 5-HT 2A Receptor
Wu, C., Yoder, E. J., Shih, J. C., Chen, K., Dias, P., Shi, L., Ji, X.-D., Wei, J., Conner, J. M., Kumar, S., et al. (1998) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215549804600704 · Cited by 69 · see citing works
Kalsbeek, A., Matthijssen, M. A. H., & Uylings, H. B. M. (1989) · Experimental Brain Research · doi:10.1007/bf00228899 · Cited by 66 · see citing works
3H-spiperone binding in normal and schizophrenic post-mortem human brain
Mackay, A. V. P., Doble, A., Bird, E. D., et al. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90166-2 · Cited by 63 · see citing works
Postnatal maturation of GABA‐immunoreactive neurons of rat medial prefron tal cortex
Vincent, S. L., Pabreza, L. A., & Benes, F. M. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903550110 · Cited by 62 · see citing works
Self-citationIs There a Neuroanatomic Basis for Schizophrenia? An Old Question Revisited
Benes, F. M. (1995) · The Neuroscientist · doi:10.1177/107385849500100207 · Cited by 58 · see citing works
Self-citationRétaux, S., Besson, M., & Penit-Soria, J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90296-z · Cited by 56 · see citing works
Regulation of Hippocampal 5-HT1A Receptor Gene Expression by Dexamethasone
Chalmers, D. T., López, J. F., Vázquez, D. M., Akil, H., & Watson, S. J. (1994) · Neuropsychopharmacology · doi:10.1038/npp.1994.24 · Cited by 56 · see citing works
Regional distribution of neurotrophin receptors in the developing auditory brainstem
Hafidi, A., Moore, T., & Sanes, D. H. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960408)367:3 · Cited by 51 · see citing works
Benes, F. M. (1988) · PubMed · Cited by 48 · see citing works
Self-citationPharmacological interactions between serotonin and dopamine on behavior in the squirrel monkey
Howell, L. L., Czoty, P. W., & Byrd, L. D. (1997) · Psychopharmacology · doi:10.1007/s002130050263 · Cited by 46 · see citing works
Biochemistry of Neurotransmitters in Cortical Development
Johnston, M. V. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_7 · Cited by 46 · see citing works
Tam, S. Y., & Roth, R. H. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20219-1 · Cited by 44 · see citing works
Kalsbeek, A., DEBRUIN, J., Matthijssen, M. A. H., & Uylings, H. B. M. (1989) · Behavioural Brain Research · doi:10.1016/s0166-4328(89)80079-8 · Cited by 39 · see citing works
Seeman, P. M., Ohara, K., Ulpian, C., et al. (1993) · Neuropsychopharmacology · doi:10.1038/npp.1993.15 · Cited by 39 · see citing works
Dopamine receptor changes in schizophrenia in relation to the disease process and movement disorder.
Cross, A. J., Crow, T. J., Ferrier, I. N., et al. (1983) · PubMed · Cited by 39 · see citing works
Stress and GABAergic transmission: biochemical and behavioural studies.
Mg, C., & Biggio, G. (1986) · PubMed · Cited by 36 · see citing works
Schizophrenia: Dopamine D1 Receptor Sequence Is Normal, But Has DNA Polymorphisms
Ohara, K., Ulpian, C., Seeman, P. M., et al. (1993) · Neuropsychopharmacology · doi:10.1038/npp.1993.14 · Cited by 31 · see citing works
Meshul, C. K., Buckman, J. F., Allen, C., Riggan, J. P., & Feller, D. J. (1996) · Synapse · doi:10.1002/(sici)1098-2396(199604)22:4 · Cited by 30 · see citing works
Ding, Y., Volkow, N. D., Logan, J., Garza, V., Pappas, N. R., King, P. T., & Fowler, J. S. (2000) · Synapse · doi:10.1002/(sici)1098-2396(20000301)35:3 · Cited by 25 · see citing works
Neonatal raphe lesions increase dopamine fibers in prefrontal cortex of adult rats
Taylor, J. B., Cunningham, M. C., & Benes, F. M. (1998) · Neuroreport · doi:10.1097/00001756-199806010-00026 · Cited by 22 · see citing works
Self-citationBenes, F. M., & Barrnett, R. J. (1978) · Brain Research · doi:10.1016/0006-8993(78)90280-9 · Cited by 20 · see citing works
Self-citationLidow (1998) · doi:10.1002/(sici)1098-2396(199801)28:1
Benes (1996) · doi:10.1002/(sici)1098-2396(199608)23:4
Xiao (1998) · doi:10.1002/(sici)1098-2396(199808)29:4
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GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082 · see citing works
Self-citationPubertal hormones organize the adolescent brain and behavior
Sisk, C. L., & Zehr, J. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.003 · Cited by 1,082 · see citing works
Beyond simple models of self-control to circuit-based accounts of adolescent behavior
Casey, B. J. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015156 · Cited by 742 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
Serotonin and brain development: role in human developmental diseases
Whitaker-Azmitia, P. M. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00615-3 · Cited by 506 · see citing works
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
Tremblay, L. K., Naranjo, C. A., Graham, S. J., Herrmann, N., Mayberg, H. S., Hevenor, S., & Busto, U. E. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.11.1228 · Cited by 340 · see citing works
Dopamine Modulation of Prefrontal Cortical Interneurons Changes during Adolescence
Tseng, K.-Y., & O'Donnell, P. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl034 · Cited by 339 · see citing works
Uchida, S., Hara, K., Kobayashi, A., Funato, H., Hobara, T., Otsuki, K., Yamagata, H., McEwen, B. S., & Watanabe, Y. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1436-10.2010 · Cited by 310 · see citing works
Spear, L. P. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.08.001 · Cited by 292 · see citing works
Adolescence: what do transmission, transition and translation have to do with it?
Casey, B. J., Duhoux, S., & Cohen, M. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.033 · Cited by 297 · see citing works
Steketee, J. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00233-3 · Cited by 293 · see citing works
Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats
Belluzzi, J., Lee, A., Oliff, H., & Leslie, F. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1758-6 · Cited by 280 · see citing works
Telzer, E. H. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.10.010 · Cited by 274 · see citing works
McCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
Pistis, M., Perra, S., Pillolla, G., Melis, M., Muntoni, A. L., & Gessa, G. L. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.05.006 · Cited by 194 · see citing works
Epigenetic mechanisms mediating vulnerability and resilience to psychiatric disorders
Dudley, K. J., Li, X., Kobor, M. S., Kippin, T. E., & Bredy, T. W. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.016 · Cited by 180 · see citing works
Tseng, K. Y., & O'Donnell, P. (2007) · Synapse · doi:10.1002/syn.20432 · Cited by 141 · see citing works
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Manitt, C., Mimee, A., Eng, C., Pokinko, M., Stroh, T., Cooper, H. M., Kolb, B., & Flores, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0606-11.2011 · Cited by 133 · see citing works
Yang, C.-J., Tan, H.-P., & Du, Y.-J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.02.021 · Cited by 132 · see citing works
Manitt, C., Eng, C., Pokinko, M., Ryan, R. T., Torres-Berrío, A., Lopez, J. P., Yogendran, S. V., Daubaras, M. J. J., Grant, A., Schmidt, E. R. E., et al. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.105 · Cited by 125 · see citing works
Doremus-Fitzwater, T. L., & Spear, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.015 · Cited by 125 · see citing works
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McQuown, S. C., Belluzzi, J. D., & Leslie, F. M. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.012 · Cited by 117 · see citing works
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Rodrigues, A.-J., Leão, P., Carvalho, M., Almeida, O. F. X., & Sousa, N. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2085-3 · Cited by 97 · see citing works
Leussis, M. P., Lawson, K., Stone, K., & Andersen, S. L. (2008) · Synapse · doi:10.1002/syn.20483 · Cited by 95 · see citing works
Schochet, T. L., Kelley, A. E., & Landry, C. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.057 · Cited by 93 · see citing works
Juárez, I., Gratton, A., & Flores, G. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21651 · Cited by 89 · see citing works
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Padmanabhan, A., & Luna, B. (2014) · Brain and Cognition · doi:10.1016/j.bandc.2013.09.011 · Cited by 87 · see citing works
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Reynolds, L. M., Yetnikoff, L., Pokinko, M., Wodzinski, M., Epelbaum, J. G., Lambert, L. C., Cossette, M.-P., Arvanitogiannis, A., & Flores, C. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy247 · Cited by 75 · see citing works
Adolescents exhibit behavioral differences from adults during instrumental learning and extinction
Sturman, D. A., Mandell, D. R., & Moghaddam, B. (2010) · Behavioral Neuroscience · doi:10.1037/a0018463 · Cited by 69 · see citing works
Tobacco use across the formative years: a road map to developmental vulnerabilities
Jamner, L., Whalen, C., Loughlin, S., Mermelstein, R., Audrain-McGovern, J., Krishnan-Sarin, S., Worden, J., & Leslie, F. (2003) · Nicotine & Tobacco Research · doi:10.1080/14622200310001625573 · Cited by 60 · see citing works
Bergstrom, H. C., McDonald, C. G., French, H. T., & Smith, R. F. (2008) · Synapse · doi:10.1002/syn.20467 · Cited by 60 · see citing works
Parr, A. C., Calabro, F., Larsen, B., Tervo-Clemmens, B., Elliot, S., Foran, W., Olafsson, V., & Luna, B. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.101997 · Cited by 60 · see citing works
Milstein, J. A., Elnabawi, A., Vinish, M., Swanson, T., Enos, J. K., Bailey, A. M., Kolb, B., & Frost, D. O. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057308 · Cited by 57 · see citing works
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Bernheim, A., Halfon, O., & Boutrel, B. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00118 · Cited by 49 · see citing works
McQuown, S. C., Dao, J. M., Belluzzi, J. D., & Leslie, F. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1642-0 · Cited by 39 · see citing works
Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat
Yetnikoff, L., Reichard, R. A., Schwartz, Z. M., Parsely, K. P., & Zahm, D. S. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23459 · Cited by 30 · see citing works
- Authors
- Benes, F. M.
- Affiliations
- Harvard University (US)
- Corresponding author
- Benes, F. M.
- ORCID
- Benes, F. M.
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2000-10-01
- Volume
- 10
- Issue
- 10
- Pages
- 1014-1027
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2137587432
- Cited by
- 268
- References
- 121
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 5 · 2023: 2 · 2022: 6 · 2021: 9 · 2020: 8 · 2019: 8 · 2018: 13 · 2017: 10 · 2016: 18 · 2015: 12 · 2014: 11 · 2013: 21 · 2012: 9
- FWCI
- 0.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH.NS 31862, MH-42261, MH00423)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- medial prefrontal cortex, dopamine, serotonin, postnatal development, GABAergic interneurons, pyramidal neurons, dorsal raphe nucleus, neuroplasticity, psychopathology, immunofluorescence
- MeSH terms
- Animals, Animals, Newborn, Mental Disorders, Dopamine, gamma-Aminobutyric Acid, Humans, Nervous System Diseases, Neural Pathways, Neuronal Plasticity, Serotonin, Prefrontal Cortex
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