High serotonin levels during brain development alter the structural input-output connectivity of neural networks in the rat somatosensory layer IV
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Homeostatic regulation of serotonin (5-HT) concentration is critical for "normal" topographical organization and development of thalamocortical (TC) afferent circuits. Down-regulation of the serotonin transporter (SERT) and the consequent impaired reuptake of 5-HT at the synapse, results in a reduced terminal branching of developing TC afferents within the primary somatosensory cortex (S1). Despite the presence of multiple genetic models, the effect of high extracellular 5-HT levels on the structure and function of developing intracortical neural networks is far from being understood. Here, using juvenile SERT knockout (SERT(-/-)) rats we investigated, in vitro, the effect of increased 5-HT levels on the structural organization of (i) the TC projections of the ventroposteromedial thalamic nucleus toward S1, (ii) the general barrel-field pattern, and (iii) the electrophysiological and morphological properties of the excitatory cell population in layer IV of S1 [spiny stellate (SpSt) and pyramidal cells]. Our results confirmed previous findings that high levels of 5-HT during development lead to a reduction of the topographical precision of TCA projections toward the barrel cortex. Also, the barrel pattern was altered but not abolished in SERT(-/-) rats. In layer IV, both excitatory SpSt and pyramidal cells showed a significantly reduced intracolumnar organization of their axonal projections. In addition, the layer IV SpSt cells gave rise to a prominent projection toward the infragranular layer Vb. Our findings point to a structural and functional reorganization of TCAs, as well as early stage intracortical microcircuitry, following the disruption of 5-HT reuptake during critical developmental periods. The increased projection pattern of the layer IV neurons suggests that the intracortical network changes are not limited to the main entry layer IV but may also affect the subsequent stages of the canonical circuits of the barrel cortex.
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Serotonin plays important neurotrophic roles during early development, and elevations of 5-HT during critical time periods can alter cognition and sensory processing.
“Serotonin plays important neurotrophic roles during early development, and elevations of 5-HT during critical time periods can alter cognition and sensory processing [109].”
From The Gut Microbiota and Dysbiosis in Autism Spectrum Disorders (2018) · cites this paper as [109]
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Hughes, H. K., Rose, D., & Ashwood, P. (2018) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-018-0887-6 · Cited by 225 · see citing works
The serotonin-BDNF duo: developmental implications for the vulnerability to psychopathology
Homberg, J. R., Molteni, R., Calabrese, F., & Riva, M. A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.03.012 · Cited by 177 · see citing works
Self-citationHomberg, J. R., Schubert, D., Asan, E., & Aron, E. N. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.029 · Cited by 121 · see citing works
Self-citationLayer I Interneurons Sharpen Sensory Maps during Neonatal Development
Che, A., Babij, R., Iannone, A. F., Fetcho, R. N., Ferrer, M., Liston, C., Fishell, G., & De Marco García, N. V. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.002 · Cited by 91 · see citing works
The neurodevelopmental effects of serotonin: A behavioural perspective
Kepser, L.-J., & Homberg, J. R. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.022 · Cited by 103 · see citing works
Self-citationRefining the Role of 5-HT in Postnatal Development of Brain Circuits
Teissier, A., Soiza‐Reilly, M., & Gaspar, P. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00139 · Cited by 101 · see citing works
Modelling and Analysis of Electrical Potentials Recorded in Microelectrode Arrays (MEAs)
Ness, T. V., Chintaluri, C., Potworowski, J., Łęski, S., Głąbska, H., Wojcik, D. K., & Einevoll, G. T. (2015) · Neuroinformatics · doi:10.1007/s12021-015-9265-6 · Cited by 83 · see citing works
Homberg, J. R., Kyzar, E. J., Nguyen, M., Norton, W., Pittman, J. T., Poudel, M. K., Gaikwad, S., Nakamura, S., Koshiba, M., Yamanouchi, H., et al. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.013 · Cited by 83 · see citing works
Self-citationWang, B., Iyengar, R. V., Li-Harms, X., Joo, J. H., Wright, C., Lavado, A., HORNER, L. H., Yang, M., Guan, J., Frase, S., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1386820 · Cited by 75 · see citing works
Delayed growth, motor function and learning in preterm pigs during early postnatal life
Andersen, A. D., Sangild, P. T., Munch, S. L., van der Beek, E. M., Renes, I. B., Ginneken, C. J. V., Greisen, G. O., & Thymann, T. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00349.2015 · Cited by 72 · see citing works
Development of Serotonergic Fibers in the Post-Natal Mouse Brain
Maddaloni, G., Bertero, A., Pratelli, M., Barsotti, N., Boonstra, A., Giorgi, A. U. D., Migliarini, S., & Pasqualetti, M. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00202 · Cited by 71 · see citing works
Multisensory cortical processing and dysfunction across the neuropsychiatric spectrum
Hornix, B., Havekes, R., & Kas, M. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.02.010 · Cited by 60 · 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-citationZhang, Z., Rasmussen, L., Saraswati, M., Koehler, R., Robertson, C., & Kannan, S. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2017.5450 · Cited by 49 · see citing works
Miceli, S., Kasri, N. N., Joosten, J., Huang, C., Kepser, L.-J., Proville, R. D., Selten, M. M., van Eijs, F., Azarfar, A., Homberg, J. R., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx016 · Cited by 38 · see citing works
Self-citationKroeze, Y., Peeters, D., Boulle, F., van den Hove, D. V. D., van Bokhoven, H., Zhou, H., & Homberg, J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.145 · Cited by 36 · see citing works
Self-citationAkhmetshina, D., Zakharov, A., Vinokurova, D. A., Nasretdinov, A., Valeeva, G. R., & Khazipov, R. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.03.011 · Cited by 31 · see citing works
The roles of CC2D1A and HTR1A gene expressions in autism spectrum disorders
Şener, E. F., Uytun, M. Ç., Bayram, K. K., Zararsız, G., Öztop, D. B., Canatan, H., & Özkul, Y. (2016) · Metabolic Brain Disease · doi:10.1007/s11011-016-9795-0 · Cited by 28 · see citing works
Kroeze, Y., Peeters, D., Boulle, F., van den Hove, D. V. D., van Bokhoven, H., Zhou, H., & Homberg, J. (2015) · Translational Psychiatry · doi:10.1038/tp.2016.60 · Cited by 11 · 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-citationSener, E. F., Taheri, S., Sahin, M. C., Bayramov, K. K., Marasli, M. K., Zararsiz, G., Mehmetbeyoglu, E., Oztop, D. B., Canpolat, M., Canatan, H., et al. (2019) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1213-0 · Cited by 23 · see citing works
Kingston, R., Amin, D., Misra, S., Gross, J. M., & Kuwajima, T. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009885 · Cited by 19 · see citing works
Van, V. D. P., Krause, E. T., & Phi‐van, L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00284 · Cited by 17 · see citing works
van der Knaap, N. J. F., Wiedermann, D., Schubert, D., Hoehn, M., & Homberg, J. R. (2021) · Scientific Reports · doi:10.1038/s41598-021-81327-z · Cited by 15 · see citing works
Self-citationHomberg, J. R., Brivio, P., Greven, C. U., & Calabrese, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105605 · Cited by 14 · see citing works
Self-citationPerinatal SSRI exposure impacts innate fear circuit activation and behavior in mice and humans
Zanni, G., van Dijk, M. T., Cagliostro, M. K. C., Sepúlveda, P., Pini, N., Rose, A. L., Kesin, A. L., Lugo-Candelas, C. I., Gonçalves, P. D., MacKay, A. S., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-58785-4 · Cited by 13 · see citing works
Huang, X., Kuang, S., Applegate, T. J., Lin, T.-L., & Cheng, H. W. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.08.011 · Cited by 12 · see citing works
Chaji, D., Venkatesh, V., Shirao, T., Day, D. J., & Ellenbroek, B. (2021) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01764-9 · Cited by 7 · see citing works
Lee, M., Chen, Y., Wu, S., Huang, C., Dewey, M. E., & Chen, V. C. (2024) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-024-02460-4 · Cited by 9 · see citing works
The development of the serotonergic and dopaminergic systems during chicken mid-late embryogenesis
Huang, X., Kuang, S., Applegate, T. J., Lin, T.-L., & Cheng, H. W. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110472 · Cited by 9 · see citing works
Freitag, F. B., Ahemaiti, A., Weman, H. M., Ambroz, K., & Lagerström, M. C. (2021) · Scientific Reports · doi:10.1038/s41598-021-82649-8 · Cited by 10 · see citing works
van der Knaap, N. J. F., Marroun, H. E., Klumpers, F., Mous, S. E., Jaddoe, V. W. V., Albert Hofman, D., Homberg, J. R., White, T. J. H., Tiemeier, H. W., & Fernández, G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0505-14.2014 · Cited by 9 · see citing works
Self-citationWhitaker‐Azmitia, P. M. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-444-64125-0.00023-2 · Cited by 9 · see citing works
The chemokine Cxcl14 regulates interneuron differentiation in layer I of the somatosensory cortex
Iannone, A. F., Akgül, G., Zhang, R., Wacks, S., Hussein, N., Macias, C. G., Donatelle, A., Bauriedel, J. M. J., Wright, C., Abramov, D., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114531 · Cited by 9 · see citing works
Age- and estrous-dependent effects of psilocybin in rats
Zylko, A. L., Rakoczy, R. J., Roberts, B. F., Wilson, M., Powell, A., Page, A., Heitkamp, M., Feist, D., Jones, J. A., & McMurray, M. S. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110619 · Cited by 10 · see citing works
Endocannabinoid-dependent formation of columnar axonal projection in the mouse cerebral cortex
Itami, C., Uesaka, N., Huang, J.-Y., Lu, H., Sakimura, K., Kano, M., & Kimura, F. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122700119 · Cited by 8 · see citing works
Impact of Monoaminergic Neuromodulators on the Development of Sensorimotor Circuits
Schubert, D., Kasri, N. N., Celikel, T., & Homberg, J. R. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2975-7_11 · Cited by 8 · see citing works
Self-citationSerotonergic development of active sensingPreprint
Azarfar, A., Zhang, Y., Alishbayli, A., Schubert, D., Homberg, J. R., & Celikel, T. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/762534 · Cited by 8 · see citing works
Self-citationNeurodevelopment and the gut microbiome
Oliphant, K., & Lu, J. N. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820602-7.00006-4 · Cited by 4 · see citing works
The Role of Serotonin in Brain Development: From Molecular Pathways to Neurodevelopmental Risk
Chan, W. K., Rasmusson, S., Shiadeh, S. M. J., Wilhelmsson, R., Johansson, M. E., Elfving, B., Müller, H. K., Mallard, C. E., & Ardalan, M. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01746-2 · Cited by 2 · see citing works
Gestational Chlorpyrifos Exposure Imparts Lasting Alterations to the Rat Somatosensory Cortex
Koenig, J. A., Haga, C. W., Cramer, N., & Keller, A. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0363-25.2025 · Cited by 2 · see citing works
Gallo, M. T. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.10.026 · Cited by 1 · see citing works
Partners in plasticity: serotonergic glial interactions in brain circuit remodeling
Miller, V. K., & Broadie, K. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1782246 · Cited by 1 · see citing works
Prado-Rivera, M. A., Jagersma, J. D., & Olivier, J. D. A. (2025) · Current topics in behavioral neurosciences · doi:10.1007/7854_2025_602
Koenig, J. A., Cramer, N., Kessler, K., Olusakin, J., Lobo, M. K., & Keller, A. (2025) · eNeuro · doi:10.1523/eneuro.0195-25.2025
Dynamic analysis of epileptic seizures induced by excitatory circuits in the corticothalamic network
Zeng, J., Zheng, Y., Ma, L., Zhong, S., & Chen, Y. (2026) · Nonlinear Dynamics · doi:10.1007/s11071-026-13078-3
Samina, M. C. F., Stanciu, M., Merkelijn, T., Garcia, L. P., Hanswijk, S. I., Witteveen, J. S., Alenina, N. V., Bäder, M., Homberg, J. R., & Kolk, S. M. (2026) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6c00382
Self-citation
- Authors
- Miceli, S., Negwer, M., van Eijs, F., Kalkhoven, C., van Lierop, I., Homberg, J., & Schubert, D.
- Affiliations
- Radboud University Nijmegen (NL)
- Corresponding author
- Miceli, Stéphanie
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 7
- Pages
- 88-88
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC3675331
- OpenAlex
- W2148476512
- Cited by
- 49
- References
- 98
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 3 · 2022: 1 · 2021: 5 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 4 · 2016: 7 · 2015: 3 · 2014: 3 · 2013: 2
- FWCI
- 2.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Digital Library (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- serotonin, serotonin transporter, thalamocortical afferents, primary somatosensory cortex, layer 4, barrel cortex, topographic map, spiny stellate cells, pyramidal neurons, cortical development, neural network reorganization
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