The DOI matches its Crossref record; 75 of the 75 references it cites were found in a registry or an index.
The development of the subplate and thalamocortical connections in the human foetal brain
Abstract
The aim of this review is to present clinically relevant data on prenatal development of thalamocortical connections in the human brain. The analysis is based on extensive Zagreb Neuroembryological Collection, including more than 500 prenatal human brains stained with various classical neurohistological, as well as modern histochemical and immunohistochemical methods. The connection of thalamocortical axons during the ‘waiting’ period with transient cortical subplate zone and subsequent synaptic engagement in the cortical plate is the main connectivity event in the late foetus and preterm infant. This connectivity is the structural substrate for the endogeneous subplate and sensory‐driven circuitry generating transient electrical phenomena and may represent a transient network in the developmental history of consciousness. Conclusion: Findings presented in this review should be considered in the management of pain in preterm infants, in searching for the vulnerability of the subplate zone in diagnostic procedures using the in vivo MRI and in revealing the developmental origin of cognitive and mental disorders.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“SP, which contains the earliest-generated neurons, showed enrichment for mature neuronal markers and synaptic transmission, reflecting early thalamic afferent input by midgestation35.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [35]
In the citing paper
“The SP is a largely transient zone beneath the CP that plays an important role in establishment of thalamocortical connectivity (see35 for review).”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [35]
Citations
Cites
(1909) · Cited by 2,575
Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances
Volpe, J. J. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70294-1 · Cited by 2,501
Pain and Its Effects in the Human Neonate and Fetus
Anand, K. J. S., & Hickey, P. R. (1987) · New England Journal of Medicine · doi:10.1056/nejm198711193172105 · Cited by 1,715
Normal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391
Schmahmann, J. D., & Pandya, D. N. (2006) · doi:10.1093/acprof:oso/9780195104233.001.0001 · Cited by 1,157
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912
Self-citationThe development of nociceptive circuits
Fitzgerald, M. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1701 · Cited by 778
Prenatal development of the visual system in rhesus monkey
RAKIC, P. T., Barlow, H. B., & Gaze, R. M. (1977) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1977.0040 · Cited by 739
Resting-state networks in the infant brain
Fransson, P., Skiöld, B., Horsch, S., Nordell, A., Blennow, M., Lagercrantz, H., & Åden, U. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704380104 · Cited by 696
Allendoerfer, K. L., & Shatz, C. J. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.001153 · Cited by 653
Development of the corpus callosum and cavum septi in man
RAKIC, P. T., & Yakovlev, P. I. (1968) · The Journal of Comparative Neurology · doi:10.1002/cne.901320103 · Cited by 640
The development of cerebral connections during the first 20–45 weeks’ gestation
Kostović, I., & Milošević, N. J. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.001 · Cited by 568
Self-citationOntogeny of the human central nervous system: What is happening when?
de Graaf-Peters, V. B., & Hadders-Algra, M. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2005.10.013 · Cited by 559
Exuberance in the development of cortical networks
Innocenti, G. M., & Price, D. J. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1790 · Cited by 512
Pain activates cortical areas in the preterm newborn brain
Bartocci, M., Bergqvist, L. L., Lagercrantz, H., & Anand, K. J. S. (2006) · Pain · doi:10.1016/j.pain.2006.01.015 · Cited by 507
Cortical Pain Responses in Human Infants
Slater, R., Cantarella, A., Gallella, S., Worley, A., Boyd, S. G., Meek, J. H., & Fitzgerald, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0348-06.2006 · Cited by 447
Thalamocortical development: how are we going to get there?
López‐Bendito, G., & Molnár, Z. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1075 · Cited by 447
The subplate and early cortical circuits
Kanold, P. O., & Luhmann, H. J. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153244 · Cited by 440
Lee, S. H., Ralston, H. J., Drey, E. A., Partridge, J. C., & Rosen, M. A. (2005) · JAMA · doi:10.1001/jama.294.8.947 · Cited by 413
Kostović, I. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.5.536 · Cited by 408
Self-citationCounsell, S. J., Allsop, J. M., Harrison, M. C., Larkman, D. J., Kennea, N. L., Kapellou, O., Cowan, F. M., Hajnal, J. V., Edwards, A. D., & Rutherford, M. (2003) · PEDIATRICS · doi:10.1542/peds.112.1.1 · Cited by 397
The development of synapses in cerebral cortex of the human fetus
Molliver, M. E., Kostović, I., & der Loos, H. V. (1973) · Brain Research · doi:10.1016/0006-8993(73)90741-5 · Cited by 385
Self-citationImaging biomarkers of outcome in the developing preterm brain
Ment, L. R., Hirtz, D., & Hüppi, P. S. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70257-1 · Cited by 383
Huang, H., Xue, R., Zhang, J., Ren, T., Richards, L. J., Yarowsky, P., Miller, M. I., & Mori, S. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2769-08.2009 · Cited by 364
Two types of ipsilateral reorganization in congenital hemiparesis: A TMS and fMRI study
Staudt, M. (2002) · Brain · doi:10.1093/brain/awf227 · Cited by 348
Spontaneous correlated activity in developing neural circuits
Feller, M. B. (1999) · Neuron · doi:10.1016/s0896-6273(00)80724-2 · Cited by 342
Rapid Cortical Oscillations and Early Motor Activity in Premature Human Neonate
Milh, M., Kamińska, A., Huon, C., Lapillonne, A., Ben‐Ari, Y., & Khazipov, R. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl069 · Cited by 322
Development of neonatal EEG activity: From phenomenology to physiology
Vanhatalo, S., & Kaila, K. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.008 · Cited by 316
Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study
Mrzljak, L., Uylings, H. B. M., Kostović, I., & van Eden, C. G. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160408 · Cited by 316
Self-citationPenn, A. A., & Shatz, C. J. (1999) · Pediatric Research · doi:10.1203/00006450-199904010-00001 · Cited by 294
Petanjek, Z., Judas, M., Kostovic, I., & Uylings, H. B. M. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm124 · Cited by 273
Self-citationKostovic, I., & Rakic, P. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00025.1984 · Cited by 270
Self-citationForms and measures of adult and developing human corpus callosum: Is there sexual dimorphism?
Clarke, S., Kraftsik, R., der Loos, H. V., & Innocenti, G. M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902800205 · Cited by 264
The Emergence of Human Consciousness: From Fetal to Neonatal Life
Lagercrantz, H., & Changeux, J.-P. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e3181973b0d · Cited by 261
Kostovic, I., & Goldman‐Rakic, P. S. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902190405 · Cited by 260
Self-citationOlson, L., Bor�us, L. O., & Seiger, �. (1973) · Anatomy and Embryology · doi:10.1007/bf00519968 · Cited by 255
The development of cortical connections
Price, D. J., Kennedy, H., Dehay, C., Zhou, L., Mercier, M., Jossin, Y., Goffinet, A. M., Tissir, F., Blakey, D., & Molnár, Z. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04620.x · Cited by 223
In utero tractography of fetal white matter development
Kasprian, G. J., Brugger, P. C., Weber, M., Krššák, M., Krampl, E., Herold, C., & Prayer, D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.026 · Cited by 218
Kostović, I., & Judáš, M. (2002) · The Anatomical Record · doi:10.1002/ar.10069 · Cited by 215
Self-citationBourgeois, J., Jastreboff, P. J., & RAKIC, P. T. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.11.4297 · Cited by 215
Judáš, M., Radoš, M., Milošević, N. J., Hrabač, P., Štern-Padovan, R., & Kostović, I. (2005) · PubMed Central · Cited by 190
Self-citationPutative neural substrate of normal and abnormal general movements
Hadders‐Algra, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.009 · Cited by 185
Neuronal damage accompanies perinatal white-matter damage
Leviton, A., & Gressèns, P. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.009 · Cited by 175
From selective vulnerability to connectivity: insights from newborn brain imaging
Miller, S. P., & Ferriero, D. M. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.010 · Cited by 172
Functional Synaptic Projections onto Subplate Neurons in Neonatal Rat Somatosensory Cortex
Hanganu, I. L., Kilb, W., & Luhmann, H. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07165.2002 · Cited by 159
Perinatal Subplate Neuron Injury: Implications for Cortical Development and Plasticity
McQuillen, P. S., & Ferriero, D. M. (2005) · Brain Pathology · doi:10.1111/j.1750-3639.2005.tb00528.x · Cited by 155
Kostović, I. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90077-1 · Cited by 153
Self-citationKostović, I., & Judáš, M. (2006) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162206000831 · Cited by 150
Self-citationMaas, L., Mukherjee, P., Carballido-Gamio, J., Veeraraghavan, S., Miller, S. P., Partridge, S., Henry, R. G., Barkovich, A., & Vigneron, D. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.02.035 · Cited by 148
Ontogenesis of goal-directed behavior: anatomo-functional considerations
Kostović, I., Judaš, M., Petanjek, Z., & Šimić, G. (1995) · International Journal of Psychophysiology · doi:10.1016/0167-8760(94)00081-o · Cited by 139
Self-citationHerrmann, K., Antonini, A., & Shatz, C. J. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00565.x · Cited by 136
Counsell, S. J., Dyet, L. E., Larkman, D. J., Nunes, R. G., Boardman, J. P., Allsop, J. M., Fitzpatrick, J. A., Srinivasan, L., Cowan, F. M., Hajnal, J. V., et al. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.036 · Cited by 134
Kostović, I. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62682-5 · Cited by 127
Self-citationSubplate Neurons-Missing Link in Brain Injury of the Premature Infant?
Volpe, J. J. (1996) · PEDIATRICS · doi:10.1542/peds.97.1.112 · Cited by 122
Monoaminergic influence on testosterone-activated copulatory behavior in the castrated male rat.
Malmnäs, C. O. (1973) · PubMed · Cited by 122
Kostović, I., & JUDAS, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.018 · Cited by 119
Self-citationOn the early development of the isocortex in fetal sheep.
Ke, A. (1967) · PubMed · Cited by 111
Moore, A. R., Filipovic, R., Mo, Z., Rasband, M. N., Zečević, N., & Antic, S. D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn206 · Cited by 103
Ultrasound studies of human fetal behaviour
Prechtl, H. F. R. (1985) · Early Human Development · doi:10.1016/0378-3782(85)90173-2 · Cited by 101
Functional Excitatory Microcircuits in Neonatal Cortex Connect Thalamus and Layer 4
Zhao, C., Kao, J. P. Y., & Kanold, P. O. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4471-09.2009 · Cited by 101
The corticostriatal junction: A crucial region for forebrain development and evolution
Molnár, Z., & Butler, A. B. (2002) · BioEssays · doi:10.1002/bies.10100 · Cited by 93
Hanganu, I. L., Okabe, A., Leßmann, V., & Luhmann, H. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn061 · Cited by 92
Development of the Human Fetal Auditory Cortex: Growth of Afferent Fibres
Krmpotić‐Nemanić, J., Kostović, I., Kelović, Z., Nemanić, Đ., & Mrzljak, L. (1983) · Cells Tissues Organs · doi:10.1159/000145727 · Cited by 89
Self-citationMeinecke, D. L., & RAKIC, P. T. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903170107 · Cited by 86
Neonatal SEP – Back to bedside with basic science
Vanhatalo, S., & Lauronen, L. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.009 · Cited by 83
The newborn brain. Neuroscience and clinical applications
Lagercrantz, H. (2002) · Archives de Pédiatrie · doi:10.1016/s0929-693x(01)00955-1 · Cited by 77
On the Early Development of the Isocortex in Fetal Sheep
Åarströum, K.-E. (1967) · Progress in brain research · doi:10.1016/s0079-6123(08)61418-1 · Cited by 70
Magnetic resonance imaging—Insights into brain injury and outcomes in premature infants
Mathur, A., & Inder, T. E. (2009) · Journal of Communication Disorders · doi:10.1016/j.jcomdis.2009.03.007 · Cited by 67
An Ontogenetic Study of Evoked Somesthetic Cortical Responses in the Sheep
Molliver, M. E. (1967) · Progress in brain research · doi:10.1016/s0079-6123(08)61420-x · Cited by 53
Guinard, D., Usson, Y., Guillermet, C., & Saxod, R. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980817)398:1 · Cited by 41
New Horizons for the Subplate Zone and Its Pioneering Neurons
Ayoub, A. E., & Kostović, I. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp025 · Cited by 37
Self-citationDevelopment of somatosensory cortical functions. An electrophysiological study in prenatal sheep.
Persson, H. E. (1973) · PubMed · Cited by 33
The emergence of the mind—a borderline of human viability?
Lagercrantz, H. (2007) · Acta Paediatrica · doi:10.1111/j.1651-2227.2007.00232.x · Cited by 27
Anderson, G., & Price, D. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02069.x · Cited by 18
Neurotransmitters and neuromodulators
Herlenius, E., & Lagercrantz, H. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511711848.009 · Cited by 10
Research works printed but not linked: 1
- Kostović I, 1974, A new interpretation of the laminar development of cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus, Anat Rec, 178, 395
Cited by
Sorted by citations
Transcriptional landscape of the prenatal human brain
Miller, J. A., Ding, S.-L., Sunkin, S. M., Smith, K. A., Ng, L., Szafer, A., Ebbert, A., Riley, Z. L., Royall, J. J., Aiona, K., et al. (2014) · Nature · doi:10.1038/nature13185 · Cited by 1,325
Trujillo, C. A., Gao, R., Negraes, P. D., Gu, J., Buchanan, J., Preissl, S., Wang, A., Wu, W., Haddad, G. G., Chaim, I. A., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.08.002 · Cited by 974
Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.044 · Cited by 851
Neuron Number and Size in Prefrontal Cortex of Children With Autism
Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., Barnes, C. C., & Pierce, K. (2011) · JAMA · doi:10.1001/jama.2011.1638 · Cited by 779
Procedural pain and brain development in premature newborns
Brummelte, S., GRUNAU, R. E., Chau, V., Poskitt, K. J., Brant, R., Vinall, J., Gover, A., Synnes, A. R., & Miller, S. P. (2012) · Annals of Neurology · doi:10.1002/ana.22267 · Cited by 735
Metadata
- Authors
- Kostović, I., & Judaš, M.
- Affiliations
- University of Zagreb (HR)
- ORCID
- Kostović, Ivica
- Venue
- Acta Paediatrica
- Publisher
- Wiley
- Published
- 2010-07
- Volume
- 99
- Issue
- 8
- Pages
- 1119-1127
- ISSN
- 0365-1436 (ISSN-L)
- 0803-5253
- 1651-2227
- OpenAlex
- W1755908671
- Cited by
- 462
- References
- 75
- Citations by year
- 2026: 22 · 2025: 26 · 2024: 28 · 2023: 24 · 2022: 26 · 2021: 19 · 2020: 68 · 2019: 30 · 2018: 24 · 2017: 25 · 2016: 31 · 2015: 33 · 2014: 36 · 2013: 29 · 2012: 15
- FWCI
- 1.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Acta Paediatrica (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- subplate, thalamocortical connections, fetal brain development, cortical plate, preterm infants, pain management, consciousness development
- MeSH terms
- Afferent Pathways, Axons, Cerebral Cortex, Humans, Infant, Newborn, Infant, Premature, Neural Pathways, Staining and Labeling, Thalamus, Fetal Development
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 ›
Are you an author, or do you see a problem with this page? Request a review
