Perturbed Developmental Serotonin Signaling Affects Prefrontal Catecholaminergic Innervation and Cortical Integrity
Open accessAbstract
Proper development of the medial prefrontal cortex (mPFC), crucial for correct cognitive functioning, requires projections from, among others, the serotonergic (5-HT) and catecholaminergic systems, but it is unclear how these systems influence each other during development. Here, we describe the parallel development of the 5-HT and catecholaminergic prefrontal projection systems in rat and demonstrate a close engagement of both systems in the proximity of Cajal-Retzius cells. We further show that in the absence of the 5-HT transporter (5-HTT), not only the developing 5-HT but also the catecholaminergic system, including their projections towards the mPFC, are affected. In addition, the layer identity of the mPFC neurons and reelin-positive interneuron number and integration are altered in the absence of the 5-HTT. Together, our data demonstrate a functional interplay between the developing mPFC 5-HT and catecholaminergic systems, and call for a holistic approach in studying neurotransmitter systems-specific developmental consequences for adult behavior, to eventually allow the design of better treatment strategies for neuropsychiatric disorders.
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Serotonin exerts a significant trophic and modulatory function in neurodevelopmental processes such as proliferation, migration, and differentiation in cortical areas, including the PFC.
“It has become widely accepted that serotonin exerts a significant trophic and modulatory function in neurodevelopmental processes such as proliferation, migration and differentiation in cortical areas, including the PFC [119, 123, 125–129].”
From Development of prefrontal cortex (2022) · cites this paper as [123]
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Cites
The developmental role of serotonin: news from mouse molecular genetics
Gaspar, P., Cases, O., & Maroteaux, L. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1256 · Cited by 1,297 · see citing works
The spectrum of behaviors influenced by serotonin
Lucki, I. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00139-5 · Cited by 1,154 · see citing works
Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system
Lammel, S., Hetzel, A., Häckel, O., Jones, I., Liss, B., & Roeper, J. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.022 · Cited by 976 · see citing works
Cloning and expression of a functional serotonin transporter from rat brain
Blakely, R., Berson, H. E., Fremeau, R. T., Caron, M. G., Peek, M. M., Prince, H. K., & Bradley, C. C. (1991) · Nature · doi:10.1038/354066a0 · Cited by 831 · see citing works
Stress weakens prefrontal networks: molecular insults to higher cognition
Arnsten, A. F. T. (2015) · Nature Neuroscience · doi:10.1038/nn.4087 · Cited by 752 · see citing works
A transient placental source of serotonin for the fetal forebrain
Bonnin, A., Goeden, N., Chen, K., Wilson, M. L., King, J., Shih, J. C., Blakely, R. D., Deneris, E. S., & Levitt, P. (2011) · Nature · doi:10.1038/nature09972 · Cited by 608 · see citing works
Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., & Rudy, B. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1869-10.2010 · Cited by 600 · see citing works
The developmental origins of anxiety
Gross, C. T., & Hen, R. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1429 · Cited by 563 · 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
Azmitia, E. C. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00614-1 · Cited by 497 · see citing works
Bagri, A., Marín, O., Plump, A., Mak, J., Pleasure, S., Rubenstein, J., & Tessier-Lavigne, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00561-5 · Cited by 467 · see citing works
A whole-brain atlas of inputs to serotonergic neurons of the dorsal and median raphe nuclei
Pollak Dorocic, I., Fürth, D., Xuan, Y., Johansson, Y., Pozzi, L., Silberberg, G., Carlén, M., & Meletis, K. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.002 · Cited by 451 · see citing works
Development of the serotonergic system in the rat embryo: An immunocytochemical study
Wallace, J. A., & Lauder, J. M. (1983) · Brain Research Bulletin · doi:10.1016/0361-9230(83)90144-2 · Cited by 402 · see citing works
Akil, M., Pierri, J. N., Whitehead, R. E., Edgar, C. L., Mohila, C., Sampson, A. R., & Lewis, D. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.10.1580 · Cited by 393 · see citing works
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 · see citing works
Hervé, D., Pickel, V. M., JOH, T. H., & Beaudet, A. (1987) · Brain Research · doi:10.1016/0006-8993(87)91588-5 · Cited by 372 · see citing works
Dissecting the diversity of midbrain dopamine neurons
Roeper, J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.003 · Cited by 372 · see citing works
The organization of two new cortical interneuronal circuits
Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., & Zhu, J. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3305 · Cited by 338 · see citing works
Schizophrenia: a tale of two critical periods for prefrontal cortical development
Selemon, L. D., & Zecevic, N. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.115 · Cited by 336 · see citing works
Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex
Jossin, Y., & Cooper, J. A. (2011) · Nature Neuroscience · doi:10.1038/nn.2816 · Cited by 332 · see citing works
Franco, S. J., Martínez‐Garay, I., Gil, C., Harkins-Perry, S. R., & Müller, U. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.003 · Cited by 329 · see citing works
The roles of dopamine and serotonin, and of their receptors, in regulating sleep and waking
Monti, J. M., & Jantos, H. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00929-1 · Cited by 303 · see citing works
Muzerelle, A., Scotto-Lomassese, S., Bernard, J. F., Soiza-Reilly, M., & Gaspar, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-014-0924-4 · Cited by 303 · see citing works
Díaz-Mataix, L., Scorza, M. C., Bortolozzi, A. A., Tóth, M., Celada, P., & Artigas, F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2999-05.2005 · Cited by 288 · 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
Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis
Buznikov, G. A., Lambert, H. W., & Lauder, J. M. (2001) · Cell and Tissue Research · doi:10.1007/s004410100408 · Cited by 274 · see citing works
Fabre, V., Beaufour, C., Evrard, A., Bilan, A. R., Hanoun, N., Lesch, K., Murphy, D. L., Lanfumey, L., Hamon, M., & Martres, M. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00126.x · Cited by 274 · see citing works
Lmx1b is essential for the development of serotonergic neurons
Ding, Y.-Q., Marklund, U., Yuan, W., Yin, J., Wegman, L., Ericson, J., Deneris, E., Johnson, R. L., & Chen, Z.-F. (2003) · Nature Neuroscience · doi:10.1038/nn1104 · Cited by 262 · see citing works
Calizo, L. H., Akanwa, A., Ma, X., Pan, Y.-Z., Lemos, J. C., Craige, C., Heemstra, L. A., & Beck, S. G. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.008 · Cited by 252 · see citing works
Serotonin modulates the response of embryonic thalamocortical axons to netrin-1
Bonnin, A., Torii, M., Wang, L., RAKIC, P. T., & Levitt, P. R. (2007) · Nature Neuroscience · doi:10.1038/nn1896 · Cited by 249 · see citing works
Redefining the serotonergic system by genetic lineage
Jensen, P., Farago, A. F., Awatramani, R. B., Scott, M. M., Deneris, E. S., & Dymecki, S. M. (2008) · Nature Neuroscience · doi:10.1038/nn2050 · Cited by 244 · see citing works
The activation of 5‐HT2A receptors in prefrontal cortex enhances dopaminergic activity
Bortolozzi, A. A., Díaz-Mataix, L., Scorza, M. C., Celada, P., & Artigas, F. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03485.x · Cited by 224 · see citing works
Developmental origins of brain disorders: roles for dopamine
Money, K. M., & Stanwood, G. D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00260 · Cited by 221 · see citing works
Li, Q., Wichems, C. H., Heils, A., Lesch, K., & Murphy, D. L. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-07888.2000 · Cited by 218 · see citing works
Smits, B. M. G., Mudde, J., van de Belt, J., Verheul, M., Olivier, J., Homberg, J. R., Guryev, V., Cools, A. R., Ellenbroek, B. A., Plasterk, R. H. A., et al. (2006) · Pharmacogenetics and Genomics · doi:10.1097/01.fpc.0000184960.82903.8f · Cited by 197 · see citing works
Self-citationBeyond working memory: the role of persistent activity in decision making
Curtis, C. E., & Lee, D. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.03.006 · Cited by 191 · see citing works
Projections and interconnections of genetically defined serotonin neurons in mice
Bang, S. J., Jensen, P., Dymecki, S. M., & Commons, K. G. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07936.x · Cited by 181 · see citing works
<i>Lmx1b, Pet-1</i>, and<i>Nkx2.2</i>Coordinately Specify Serotonergic Neurotransmitter Phenotype
Cheng, L., Chen, C.-L., Luo, P., Tan, M., Qiu, M., Johnson, R., & Ma, Q. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09961.2003 · Cited by 177 · see citing works
The Role of Serotonin in Early Cortical Development
Vitalis, T., & Parnavelas, J. G. (2003) · Developmental Neuroscience · doi:10.1159/000072272 · Cited by 171 · see citing works
Dopamine-serotonin interactions in attention-deficit hyperactivity disorder (ADHD).
Oades, R. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00926-6 · Cited by 169 · see citing works
Fenstermaker, A. G., Prasad, A. A., Bechara, A., Adolfs, Y., Tissir, F., Goffinet, A. M., Zou, Y., & Pasterkamp, R. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4508-10.2010 · Cited by 162 · see citing works
DIMATTEO, V., Pierucci, M., Esposito, E., Crescimanno, G., Benigno, A., & Giovanni, G. D. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00921-7 · Cited by 161 · see citing works
Role for Reelin in stabilizing cortical architecture
Frotscher, M. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.06.001 · Cited by 157 · see citing works
The ability of the mesocortical dopamine system to operate in distinct temporal modes
Lapish, C. C., Kroener, S., Durstewitz, D., Lavı́n, A., & Seamans, J. K. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0527-8 · Cited by 153 · see citing works
Schubert, D., Martens, G. J. M., & Kolk, S. M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.147 · Cited by 149 · see citing works
Self-citationNarboux-Nême, N., Pavone, L. M., Avallone, L., Zhuang, X., & Gaspar, P. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.08.020 · Cited by 148 · cited 2× · see citing works
“Narboux-Nème and colleagues [60] elegantly showed a transient 5-HTTexpression within layers II, V, and VI of the mPFC at E15.”
Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development
Janušonis, S., Glunčić, V., & RAKIC, P. T. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4651-03.2004 · Cited by 146 · see citing works
Crandall, J. E., McCarthy, D. M., Araki, K. Y., Sims, J. R., Ren, J.-Q., & Bhide, P. G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5124-06.2007 · Cited by 134 · see citing works
Sekine, K., Honda, T., Kawauchi, T., Kubo, K., & Nakajima, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0650-11.2011 · Cited by 131 · see citing works
Wozny, C., & Williams, S. R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq257 · Cited by 129 · see citing works
Atlas of the Prenatal Mouse Brain
(1992) · Elsevier eBooks · doi:10.1016/c2009-0-02642-7 · Cited by 118 · see citing works
Kolk, S. M., Gunput, R.-A. F., Tran, T. S., van den Heuvel, D. M. A., Prasad, A. A., Hellemons, A. J. C. G. M., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P. H., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2521-09.2009 · Cited by 114 · see citing works
Self-citationExpression of serotonin transporter protein in developing rat brain
Zhou, F. C., Sari, Y., & Zhang, J. K. (2000) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00152-2 · Cited by 111 · see citing works
Radnikow, G., Feldmeyer, D., & Lübke, J. H. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-06908.2002 · Cited by 104 · see citing works
Homberg, J. R., de Boer, S. F., Raasø, H. S., Olivier, J. D. A., Verheul, M., Ronken, E., Cools, A. R., Ellenbroek, B. A., Schoffelmeer, A. N. M., Vanderschuren, L. J. M. J., et al. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1212-x · Cited by 103 · see citing works
Self-citationGAP-43 Is Critical for Normal Development of the Serotonergic Innervation in Forebrain
Donovan, S. L., Mamounas, L. A., Andrews, A. M., Blue, M. E., & McCasland, J. S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03543.2002 · Cited by 100 · see citing works
Fernandez, S. P., Cauli, B., Cabezas, C., Muzerelle, A., Poncer, J.-C., & Gaspar, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-015-1142-4 · Cited by 100 · see citing works
Development of raphe serotonin neurons from specification to guidance
Kiyasova, V., & Gaspar, P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07910.x · Cited by 98 · see citing works
The role of dopamine and serotonin in suicidal behaviour and aggression
Ryding, E., LINDSTROM, M., & Träskman‐Bendz, L. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00915-1 · Cited by 96 · see citing works
Serotonin–dopamine interaction: an overview
ESPOSITO, E., DIMATTEO, V, & DIGIOVANNI, G. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00901-1 · Cited by 88 · see citing works
Fate of Cajal-Retzius neurons in the postnatal mouse neocortex
Chowdhury, T. G. (2010) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.010.2010 · Cited by 86 · see citing works
Qu, Y., Villacreses, N. E., Murphy, D. L., & Rapoport, S. I. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2231-5 · Cited by 85 · see citing works
Microdomains for Dopamine Volume Neurotransmission in Primate Prefrontal Cortex
Paspalas, C. D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0195-04.2004 · Cited by 85 · see citing works
Spencer, G. E., Klumperman, J., & Syed, N. I. (1998) · PubMed · Cited by 81 · see citing works
Alterations of dopamine and serotonin transmission in schizophrenia
Remington, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00906-0 · Cited by 81 · see citing works
Altamura, C., Dell'Acqua, M., Moessner, R., Murphy, D., Lesch, K., & Persico, A. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl051 · Cited by 79 · see citing works
Niederkofler, V., Asher, T. E., & Dymecki, S. M. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00021 · Cited by 75 · see citing works
Catecholamine/Serotonin Interactions
Hensler, J. G., Artigas, F., Bortolozzi, A., Daws, L. C., De Deurwaerdère, P., Milan, L., Navailles, S., & Koek, W. (2013) · Advances in Pharmacology · doi:10.1016/b978-0-12-411512-5.00009-9 · Cited by 73 · see citing works
Making and breaking serotonin neurons and autism
Scott, M. M., & Deneris, E. S. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.012 · Cited by 71 · see citing works
Origin of the dopaminergic innervation of the rat dorsal raphe nucleus
Peyron, C., Luppi, P., Kitahama, K., Fort, P., Hermann, D. M., & Jouvet, M. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00019 · Cited by 67 · see citing works
Kirischuk, S., Luhmann, H. J., & Kilb, W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.009 · Cited by 67 · see citing works
Molecular genetics of the early development of hindbrain serotonergic neurons
Cordes, S. P. (2005) · Clinical Genetics · doi:10.1111/j.1399-0004.2005.00534.x · Cited by 66 · see citing works
Chen, X., Ye, R., Gargus, J. J., Blakely, R., Dobrenis, K., & Sze, J. Y. (2015) · Cell Reports · doi:10.1016/j.celrep.2014.12.033 · Cited by 65 · see citing works
Prenatal development of the serotonin transporter in mouse brain
Brüning, G., Liangos, O., & Baumgarten, H. G. (1997) · Cell and Tissue Research · doi:10.1007/s004410050868 · Cited by 63 · see citing works
Stanwood, G. D., Parlaman, J. P., & Levitt, P. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20548 · Cited by 62 · see citing works
DEALMEIDA, J., Palacios, J. M., & Mengod, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00905-9 · Cited by 61 · see citing works
Function and developmental origin of a mesocortical inhibitory circuit
Kabanova, A., Pabst, M., Lorkowski, M., Braganza, O., Boehlen, A., Nikbakht, N., Pothmann, L., Vaswani, A. R., Musgrove, R., Di Monte, D. A., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4020 · Cited by 61 · see citing works
Insights into the complex influence of 5‐HT signaling on thalamocortical axonal system development
van Kleef, E. S. B., Gaspar, P., & Bonnin, A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.8096.x · Cited by 61 · see citing works
Bhide, P. G. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.01.006 · Cited by 60 · see citing works
Fox, M. A., Stein, A. R., French, H. T., & Murphy, D. L. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00578.x · Cited by 57 · see citing works
Establishing diversity in the dopaminergic system
Bodea, G. O., & Blaess, S. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.09.016 · Cited by 56 · see citing works
Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00143 · Cited by 53 · see citing works
Self-citationLü, H., Lim, B. K., & Poo, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1984-09.2009 · Cited by 52 · see citing works
Neuronal Polarity in the Embryonic Mammalian Cerebral Cortex
Kon, E., Cossard, A., & Jossin, Y. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00163 · Cited by 52 · see citing works
Arnsten, A. F. T., & Wang, M. (2016) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010715-103617 · Cited by 50 · see citing works
Ledonné, F., Orduz, D., Mercier, J., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.11.074 · Cited by 49 · see citing works
Naqui, S. Z. H., Harris, B. S., Thomaidou, D., & Parnavelas, J. G. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00003-6 · Cited by 47 · see citing works
Trowbridge, S., Narboux‐Nême, N., & Gaspar, P. (2011) · The Anatomical Record · doi:10.1002/ar.21248 · Cited by 45 · see citing works
DIGIOVANNI, G., DIMATTEO, V, & ESPOSITO, E. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00931-x · Cited by 44 · cited 2× · see citing works
“In the adult brain, there is a clear interaction between the 5-HT and catecholaminergic projections towards the PFC, especially in the light of their engaged involvement in higher-order cognitive functioning [12, 15, 51].”
BackgroundKalsbeek, A., De Bruin, J. P. C., Feenstra, M. G. P., & Uylings, H. B. M. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62684-9 · Cited by 43 · see citing works
A unique subpopulation of Tbr1-expressing deep layer neurons in the developing cerebral cortex
Kolk, S. M., Whitman, M. C., Yun, M. E., Shete, P. B., & Donoghue, M. J. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.08.017 · Cited by 43 · see citing works
Self-citationAraragi, N., Mlinar, B., Baccini, G., Gutknecht, L., Lesch, K., & Corradetti, R. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00097 · Cited by 38 · see citing works
A Comparison of the Subsecond Dynamics of Neurotransmission of Dopamine and Serotonin
Jennings, K. A. (2013) · ACS Chemical Neuroscience · doi:10.1021/cn4000605 · Cited by 34 · see citing works
Quantitation of 5HT3 receptors in forebrain of serotonin transporter deficient mice
M�ssner, R., Schmitt, A. G., Hennig, T., Benninghoff, J., Gerlach, M., Riederer, P. F., Deckert, J., & Lesch, K. (2004) · Journal of Neural Transmission · doi:10.1007/s00702-003-0074-y · Cited by 31 · see citing works
A unique subpopulation of Tbr1-expressing deep layer neurons in the developing cerebral cortex
Kolk, S. M., Whitman, M. C., Yun, M. E., Shete, P. B., & Donoghue, M. J. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.08.022 · Cited by 29 · see citing works
Self-citationEditorial perspective of the Research Topic “Deciphering serotonin's role in neurodevelopment”
Homberg, J. R., Kolk, S. M., & Schubert, D. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00212 · Cited by 26 · see citing works
Self-citationJennings, K. A., Licht, C. L., Bruce, A., Lesch, K., Knudsen, G. M., & Sharp, T. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001258 · Cited by 25 · see citing works
Kroeze, Y., Oti, M., van Beusekom, E., Cooijmans, R. H. M., van Bokhoven, H., Kolk, S. M., Homberg, J. R., & Zhou, H. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhw407 · Cited by 21 · see citing works
Self-citationTeng, T., Gaillard, A., Muzerelle, A., & Gaspar, P. (2017) · eNeuro · doi:10.1523/eneuro.0327-16.2017 · Cited by 18 · see citing works
Serotonergic Heterotypic Sprouting in the Unilaterally Dopamine-Depleted Mouse Neostriatum
Yamazoe, I., Takeuchi, Y., Matsushita, H., et al. (2001) · Developmental Neuroscience · doi:10.1159/000048698 · Cited by 13 · see citing works
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- [59]Jacobowitz DM, Abott LC(1998) Chemoarchitectonic atlas of the developing mouse brain. CRC Press, Boca Raton. https://scholar.google.com/scholar_lookup? author=DM+Jacobowitz&author=LC+Abott&title=Chemoarchitectonic+atlas+of+the+developing+mouse+brain&publication_year=1998
Cited by
Sorted by citations
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
Self-citationGestational Factors throughout Fetal Neurodevelopment: The Serotonin Link
Hanswijk, S. I., Spoelder, M., Shan, L., Verheij, M. M. M., Muilwijk, O. G., Li, W., Liu, C., Kolk, S. M., & Homberg, J. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165850 · Cited by 86 · see citing works
Self-citationvan de Wijer, L., Garcia, L. P., Hanswijk, S. I., Rando, J., Middelman, A., ter Heine, R., Mast, Q. D., Martens, G. J. M., van der Ven, A. J. A. M., Kolk, S. M., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0420-y · Cited by 13 · see citing works
Self-citationGarcia, L. P., Van de Wijer, L., Hanswijk, S. I., Rando, J., Witteveen, J. S., Middelman, A., ter Heine, R., de Mast, Q., Martens, G. J. M., van der Ven, A. J. A. M., et al. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114050 · Cited by 6 · see citing works
Self-citation
- Authors
- Garcia, L. P., Witteveen, J. S., Middelman, A., van Hulten, J. A., Martens, G. J. M., Homberg, J. R., & Kolk, S. M.
- Affiliations
- Radboud University Nijmegen (NL)
- Corresponding author
- Kolk, Sharon M.
- Venue
- Molecular Neurobiology
- Published
- 2018-06-09
- Volume
- 56
- Issue
- 2
- Pages
- 1405-1420
- ISSN
- 0893-7648 (ISSN-L)
- 1559-1182
- PMC
- PMC6400880
- OpenAlex
- W2806865194
- Cited by
- 28
- References
- 101
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 5 · 2023: 1 · 2022: 2 · 2021: 7 · 2020: 4 · 2019: 1
- FWCI
- 1.11
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular Neurobiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BEX11914/13-0)
- Era-Net NEURON (RESPOND)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- serotonin signaling, catecholaminergic system, medial prefrontal cortex, 5-HT transporter, Cajal-Retzius cells, cortical integration, neuropsychiatric disorders
- MeSH terms
- Reelin Protein, Animals, Male, Neurons, Raphe Nuclei, Serotonin, Signal Transduction, Rats, Wistar, Prefrontal Cortex, Neurotransmitter Agents
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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