Hypothesis on the Dual Origin of the Mammalian Subplate

Montiel, Juan F.; Wang, Wei Zhi; Oeschger, Franziska M.; Hoerder-Suabedissen, Anna; Tung, Wan Ling; García-Moreno, Fernando; Holm, Ida Elizabeth; Villalón, Aldo; Molnár, Zoltán

doi:10.3389/fnana.2011.00025

Cited by 70Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationGenetics and Neurodevelopmental Disorders

Hypothesis on the Dual Origin of the Mammalian Subplate

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Montiel, Juan F., Wang, Wei Zhi, Oeschger, Franziska M., Hoerder-Suabedissen, Anna, Tung, Wan Ling, García-Moreno, Fernando, Holm, Ida Elizabeth, Villalón, Aldo +1 more·2011·Frontiers in Neuroanatomy

DOI 10.3389/fnana.2011.00025PMC PMC3078748

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Abstract

The development of the mammalian neocortex relies heavily on subplate. The proportion of this cell population varies considerably in different mammalian species. Subplate is almost undetectable in marsupials, forms a thin, but distinct layer in mouse and rat, a larger layer in carnivores and big-brained mammals as pig, and a highly developed embryonic structure in human and non-human primates. The evolutionary origin of subplate neurons is the subject of current debate. Some hypothesize that subplate represents the ancestral cortex of sauropsids, while others consider it to be an increasingly complex phylogenetic novelty of the mammalian neocortex. Here we review recent work on expression of several genes that were originally identified in rodent as highly and differentially expressed in subplate. We relate these observations to cellular morphology, birthdating, and hodology in the dorsal cortex/dorsal pallium of several amniote species. Based on this reviewed evidence we argue for a third hypothesis according to which subplate contains both ancestral and newly derived cell populations. We propose that the mammalian subplate originally derived from a phylogenetically ancient structure in the dorsal pallium of stem amniotes, but subsequently expanded with additional cell populations in the synapsid lineage to support an increasingly complex cortical plate development. Further understanding of the detailed molecular taxonomy, somatodendritic morphology, and connectivity of subplate in a comparative context should contribute to the identification of the ancestral and newly evolved populations of subplate neurons.

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Many genes showed similar enrichment in developing mouse and human SP, including KCNAB1 and NR4A2.
“Many genes showed similar enrichment in the developing mouse and human SP, including the known SP markers KCNAB1 and NR4A217,18,44 (Fig. 4b).”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [17]
Species differences in distinct fetal transient zones, including SZ, SP, CP, and SG, have been described.
“Species differences in distinct fetal transient zones, including the SZ2, SP17,18, CP6, and SG9, have also been described.”
From Transcriptional landscape of the prenatal human brain (2014) · cites this paper as [17]

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REVIEW ARTICLE: Neurotransmitters regulate cell migration in the telencephalon
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Dynamic integration of subplate neurons into the cortical barrel field circuitry during postnatal development in the Golli‐tau‐eGFP (GTE) mouse
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Populations of GABAergic neurons and axons in layer I of rat auditory cortex
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Comparative Aspects of Subplate Zone Studied with Gene Expression in Sauropsids and Mammals
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The Early Differentiation of the Neocortex: a Hypothesis on Neocortical Evolution
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Time of Origin and Early Fate of Preplate Cells in the Cerebral Cortex of the Rat
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Olfactory and amygdalar structures of the chicken ventral pallium based on the combinatorial expression patterns of LIM and other developmental regulatory genes
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Functional Thalamocortical Synapse Reorganization from Subplate to Layer IV during Postnatal Development in theReeler-Like Mutant Rat (Shaking Rat Kawasaki)
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Exploring Cortical Subplate Evolution Using Magnetic Resonance Imaging of the Fetal Brain
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Genetic Control of Neuronal Migrations in Human Cortical Development
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Layer VII of rodent cerebral cortex
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Molecular Evidence for a Clade of Turtles
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Prenatal Development of NADPH-diaphorase-Reactive Neurons in Human Frontal Cortex
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Australian marsupials as models for the developing mammalian visual system
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Origin and evolution of the vertebrate telencephalon, with special reference to the mammalian neocortex.
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The Claustrum Is Not Missing from All Monotreme Brains
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Immunocytochemical detection of GABAergic nerve cells in the human temporal cortex using a direct γ-aminobutyric acid antiserum
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Apparent Absence of Claustrum in Monotremes: Implications for Forebrain Evolution in Amniotes
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Feature Article: Comparative Development of the Mammalian Isocortex and the Reptilian Dorsal Ventricular Ridge. Evolutionary Considerations
Aboitiz, F. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.8.783 · Cited by 39 · see citing works
The Course and Termination of Corticothalamic Fibres Arising in the Visual Cortex of the Rat
Lozsádi, D. A., González‐Soriano, J., & Guillery, R. W. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01205.x · Cited by 38 · see citing works
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 · see citing works
Cell proliferation and death: Morphological evidence during corticogenesis in the developing human brain
Simonati, A., Tosati, C., Rosso, T., Piazzola, E., & Rizzuto, N. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19990615)45:6 · Cited by 34 · see citing works
Role of p35/Cdk5 in Preplate Splitting in the Developing Cerebral Cortex
Rakić, S., Davis, C., Molnár, Z., Nikolić, M., & Parnavelas, J. G. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj172 · Cited by 31 · see citing works
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Development and progression of age-related macular degeneration after cataract surgery--in the near future it could become a forensic medicine problem.
Vojniković, B., Čoklo, M., & Bosnar, A. (2008) · PubMed · Cited by 31 · see citing works
Development of the Visual Cortex in a Wallaby – Phylogenetic Implications
Harman, A. M., Eastough, N. J., & Beazley, L. D. (2008) · Brain Behavior and Evolution · doi:10.1159/000113546 · Cited by 29 · see citing works
Absence of selectivity in the loss of neurons from the developing cortical subplate of the rat
Arias, M. S., Baratta, J. L., Yu, J. Z., & Robertson, R. T. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00582-5 · Cited by 27 · see citing works
Ancestry of the Mammalian Preplate and its Derivatives: Evolutionary Relicts or Embryonic Adaptations?
Aboitiz, F., Montiel, J. F., & García, R. R. (2005) · Reviews in the Neurosciences · doi:10.1515/revneuro.2005.16.4.359 · Cited by 27 · see citing works
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Synaptogenesis in Purified Cortical Subplate Neurons
McKellar, C. E., & Shatz, C. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn194 · Cited by 26 · see citing works
Development and Evolution of Thalamocortical Interactions
Moln�r, Z. (2000) · European Journal of Morphology · doi:10.1076/ejom.38.5.313.7363 · Cited by 23 · see citing works
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Cortical connections of the claustrum and subjacent cell groups in the hedgehog tenrec
Künzle, H., & Radtke‐Schuller, S. (2001) · Anatomy and Embryology · doi:10.1007/s004290100175 · Cited by 21 · see citing works
Cortical Target Depletion and Ingrowth of Geniculocortical Axons: Implications for Cortical Specification
Woo, T., & Finlay, B. L. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.457 · Cited by 21 · see citing works
Reelin expression during embryonic development of the pig brain
Nielsen, K. B., Søndergaard, A., Johansen, M., Schauser, K., Vejlsted, M., Nielsen, A. L., Jørgensen, A. L., & Holm, I. E. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-75 · Cited by 18 · see citing works
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Cyto-architecture and neuronal types of the dorsomedial cerebral cortex of the common Indian wall lizard, Hemidactylus flaviviridis.
Srivastava, U., Maurya, R. C., & Chand, P. (2009) · PubMed · Cited by 17 · see citing works
Thalamocortical development: how are we going to get there?
López‐Bendito, G., & Molnár, Z. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1131 · Cited by 17 · see citing works
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Building Bridges to the Cortex
Hanashima, C., Molnár, Z., & Fishell, G. (2006) · Cell · doi:10.1016/j.cell.2006.03.021 · Cited by 14 · see citing works
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Genes Involved in the Formation of the Earliest Cortical Circuits
Molnár, Z., Hoerder‐Suabedissen, A., Wang, W., DeProto, J., Davies, K. E., Lee, S., Jacobs, E. C., Campagnoni, A. T., Paulsen, O., Piñon, M. C., et al. (2008) · Novartis Foundation symposium · doi:10.1002/9780470994030.ch15 · Cited by 10 · see citing works
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1Identification of genes differentially expressed in the embryonic pig cerebral cortex before and after appearance of gyration
Nielsen, K. B., Kruhøffer, M., Holm, I. E., Jørgensen, A. L., & Nielsen, A. L. (2010) · BMC Research Notes · doi:10.1186/1756-0500-3-127 · Cited by 10 · see citing works
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Conserved Developmental Algorithms During Thalamocortical Circuit Formation in Mammals and Reptiles
Molnár, Z. (2000) · Novartis Foundation symposium · doi:10.1002/0470846631.ch11 · Cited by 7 · see citing works
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Development and Evolution of Thalamocortical Interactions
Molnár, Z. (2000) · European Journal of Morphology · doi:10.1076/ejom.38.5.0313 · Cited by 7 · see citing works
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Rapid developmental switch in the mechanisms driving early cortical columnar networks
Dupont, E., Hanganu, I. L., Kilb, W., Hirsch, S. J., & Luhmann, H. J. (2006) · e-Neuroforum · doi:10.1515/nf-2006-0206 · Cited by 3 · see citing works
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Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer’s disease
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Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: Evidence for their selective activation by interleukin-1?
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Yamauchi (2000) · doi:10.1002/1097-4547(20001115)62:4

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Kostović I. Jovanov-Milosević N. (2008). Subplate zone of the human brain: historical perspective and new concepts. Coll. Antropol. 32, 3– 8 18405051
Molnár Z. Cordery P. (1999). Connections between cells of the internal capsule, thalamus, and cerebral cortex in embryonic rat. J. Comp. Neurol. 413, 1– 25 10464367

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 · see citing works
Development, evolution and pathology of neocortical subplate neurons
Hoerder‐Suabedissen, A., & Molnár, Z. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3915 · Cited by 269 · see citing works
Self-citation
Early Diagnosis and Early Intervention in Cerebral Palsy
Hadders‐Algra, M. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00185 · Cited by 208 · see citing works
“The subplate, which became increasingly important during phylogeny (17), plays an important role in the processes of differentiation and cortical organization (8, 18).”
Background
Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity
Sorensen, S. A., Bernard, A., Menon, V., Royall, J. J., Glattfelder, K. J., Desta, T., Hirokawa, K., Mortrud, M., Miller, J. A., Zeng, H., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht243 · Cited by 131 · see citing works
“This layer varies extensively across species (Montiel et al. 2011), and is known to contain a diverse cell population with selective gene expression (HoerderSuabedissen et al. 2009; Oeschger et al. 2012).”
Background
Cerebral cortical development in rodents and primates
Molnár, Z., & Clowry, G. J. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00003-9 · Cited by 130 · see citing works
“The cortical subplate shows important differences between humans and rodents (reviewed by Ayoub and Kostovic, 2009; Kanold and Luhmann, 2010; Montiel et al., 2011; Wang et al., 2010).”
BackgroundSelf-citation
Development of the Corticothalamic Projections
Grant, E., Hoerder‐Suabedissen, A., & Molnár, Z. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00053 · Cited by 120 · see citing works
“Furthermore they share gene-expression patterns as demonstrated by correlation data from Allan Brain Atlas (Figures 3C,D) and comparative expression research (Montiel et al., 2011; Wang et al., 2011).”
MethodSelf-citation
The premature brain: developmental and lesional anatomy
Raybaud, C., Ahmad, T. M., Rastegar, N., Shroff, M. M., & Nassar, M. A. (2013) · Neuroradiology · doi:10.1007/s00234-013-1231-0 · Cited by 111 · see citing works
“Some residual SP neurons persist throughout life as the interstitial neurons of the white matter [20, 22–24].”
Background
The enigmatic fetal subplate compartment forms an early tangential cortical nexus and provides the framework for construction of cortical connectivity
Kostović, I. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101883 · Cited by 102 · see citing works
“taxonomy and somato-dendritic morphology which were also observed in marsupials and even in sauropsids (Montiel et al., 2011; Wang et al., 2011).”
Transcriptomic Perspectives on Neocortical Structure, Development, Evolution, and Disease
Lein, E. S., Belgard, T. G., Hawrylycz, M., & Molnár, Z. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013858 · Cited by 92 · see citing works
Self-citation
Developmental gene expression in the mouse clarifies the organization of the claustrum and related endopiriform nuclei
Watson, C., & Puelles, L. (2017) · The Journal of comparative neurology · doi:10.1002/cne.24034 · Cited by 77 · see citing works
“These close developmental links were emphasized by Moln ar and Butler (2002), and many of the markers that were identified by Hoerder-Suabedissen et al. (2009, 2013) were jointly expressed in the claustrum and dorsal endopiriform nucleus (see review by Montiel et al., 2011).”
Background
The significance of the subplate for evolution and developmental plasticity of the human brain
Judáš, M., Sedmak, G., & Kostović, I. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00423 · Cited by 86 · see citing works
“In addition, in primates, in contrast to rodents, neurons are continuously added to the subplate throughout cortical neurogenesis (Smart et al., 2002; Lukaszewicz et al., 2005; Molnár et al., 2006).”
BackgroundInfluential
In search of common developmental and evolutionary origin of the claustrum and subplate
Bruguier, H., Suarez, R., Manger, P., Hoerder‐Suabedissen, A., Shelton, A. M., Oliver, D. K., Packer, A. M., Ferran, J. L., García‐Moreno, F., Puelles, L., et al. (2020) · Journal of Comparative Neurology · doi:10.1002/cne.24922 · Cited by 84 · see citing works
“…to the subpial part of the mesopallial DVR and includes as well a credible EPd homolog cell population in VPall, under piriform cortex (Molnár & Butler, 2002; Montiel et al., 2011; Norimoto et al., 2020; Puelles, 2017; Puelles et al., 2000, 2016; Wang et al., 2011; Watson & Puelles, 2017).”
BackgroundResultInfluentialSelf-citation
Selective early expression of the orphan nuclear receptor Nr4a2 identifies the claustrum homolog in the avian mesopallium: Impact on sauropsidian/mammalian pallium comparisons
Puelles, L., Ayad, A., Alonso, A., Sandoval, J. E., Martinez-de-la-Torre, M., Medina, L. M., & Ferrán, J. L. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23902 · Cited by 84 · see citing works
“Serendipitiously, we found that Wang et al. (2011) (see also Montiel et al., 2011), in their study of the evolutionary status of subplate cells across turtle, chick, opossum, rat, and mouse brains, used Nurr1 (Nr4a2) immunocytochemistry as a subplate and claustral marker.”
Background
Changing Microcircuits in the Subplate of the Developing Cortex
Viswanathan, S., Bandyopadhyay, S., Kao, J. P. Y., & Kanold, P. O. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4748-11.2012 · Cited by 82 · see citing works
“This is consistent with recent observations that suggest a degree of compartmentalization, which is most apparent in primates and might reflect evolutionarily distinct origins (Montiel et al., 2011; Wang et al., 2011).”
Result
From sauropsids to mammals and back: New approaches to comparative cortical development
Montiel, J. F., Vasistha, N. A., García‐Moreno, F., & Molnár, Z. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23871 · Cited by 74 · see citing works
Self-citation
Comments on the Updated Tetrapartite Pallium Model in the Mouse and Chick, Featuring a Homologous Claustro-Insular Complex
Puelles, L. (2017) · Brain, Behavior and Evolution · doi:10.1159/000479782 · Cited by 65 · see citing works
“…development in mammals of the Cajal-Retzius population in layer 1 and the subplate population in layer 6b, which apparently include or are largely formed by tangentially migrated cells [see Montiel et al., 2011; Wang et al., 2011; Pedraza et al., 2014; Puelles, 2014; Watson and Puelles, 2017].”
Background
hPSC Modeling Reveals that Fate Selection of Cortical Deep Projection Neurons Occurs in the Subplate
Ozair, M. Z., Kirst, C., van den Berg, B. L., Ruzo, A., Rito, T., & Brivanlou, A. H. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.05.024 · Cited by 72 · see citing works
Evolution of Cerebral Cortical Development
Molnár, Z. (2011) · Brain Behavior and Evolution · doi:10.1159/000327325 · Cited by 71 · see citing works
“…low numbers of neurons in an arbitrary unit column relative to mammalian values, and the single cell-dense layer shows similarity to layers I, V and VI of mammals but lacks the upper layers [Kriegstein and Connors, 1986; Shepherd, 1988; Reiner, 1991; Montiel et al., 2011; Wang et al., 2011] ( fig.”
BackgroundSelf-citation
Tangential migration of glutamatergic neurons and cortical patterning during development: Lessons from Cajal‐Retzius cells
Barber, M., & Pierani, A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22363 · Cited by 70 · see citing works
“…et al., 2011a) has led to the theory that the emergence of the subplate may have contributed to the increased complexity of cortical circuitry and function during evolution (Luhmann et al., 2009; Montiel et al., 2011; Wang et al., 2011a; Judas et al., 2013; Hoerder-Suabedissen and Molnar, 2015).”
Background
Cajal–Retzius cells: Update on structural and functional properties of these mystic neurons that bridged the 20th century
Kirischuk, S., Luhmann, H. J., & Kilb, W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.009 · Cited by 67 · see citing works
Evolution of neuronal identity in the cerebral cortex
Tosches, M. A., & Laurent, G. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.04.009 · Cited by 57 · see citing works
The Superior Function of the Subplate in Early Neocortical Development
Luhmann, H. J., Kirischuk, S., & Kilb, W. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00097 · Cited by 65 · see citing works
Postmitotic control of sensory area specification during neocortical development
Alfano, C., Magrinelli, E., Harb, K., Hevner, R. F., & Studer, M. (2014) · Nature Communications · doi:10.1038/ncomms6632 · Cited by 63 · see citing works
Neocortical arealization: Evolution, mechanisms, and open questions
Alfano, C., & Studer, M. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22067 · Cited by 57 · see citing works
“…of TCA to their areal targets in the cerebral cortex during early stages of brain development (as claimed by the \handshake hypothesis") (Ghosh and Shatz, 1993; Allendoerfer and Shatz, 1994; Molnar and Blakemore, 1995; Molnar et al., 2003; Garel and Rubenstein, 2004; Montiel et al., 2011).”
Background
Neural progenitors, patterning and ecology in neocortical origins
Aboitiz, F., & Zamorano, F. J. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00038 · Cited by 38 · see citing works
“Thus, Pax6 is required for the development of some relatively early, layer V phenotypes (like those expressing Er81; Tuoc and Stoykova, 2008), but in later development it facilitates the production of intermediate progenitors in the SVZ, and promotes the differentiation of late born superficial…”
BackgroundInfluential
Subplate Neurons as an Organizer of Mammalian Neocortical Development
Ohtaka‐Maruyama, C. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.00008 · Cited by 37 · see citing works
Early brain activity: Translations between bedside and laboratory
Luhmann, H. J., Kanold, P. O., Molnár, Z., & Vanhatalo, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102268 · Cited by 32 · see citing works
Self-citation
Neuronal subtype specification in establishing mammalian neocortical circuits
Kumamoto, T., & Hanashima, C. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.07.002 · Cited by 31 · see citing works
Lineage-resolved atlas of the developing human cortex
Keefe, M. G., Steyert, M. R., & Nowakowski, T. J. (2025) · Nature · doi:10.1038/s41586-025-09033-8 · Cited by 29 · see citing works
Maternal-fetal unit interactions and eutherian neocortical development and evolution
Montiel, J. F., Kaune, H., & Maliqueo, M. A. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00022 · Cited by 27 · see citing works
Self-citation
Temporal origin of mouse claustrum and development of its cortical projections
Hoerder‐Suabedissen, A., Ocana-Santero, G., Draper, T. H., Scott, S. A., Kimani, J. G., Shelton, A. M., Butt, S. J. B., Molnár, Z., & Packer, A. M. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac318 · Cited by 24 · see citing works
“…(Zingg et al. 2018; Marriott et al. 2021), fibre- and cytoarchitecture (Celio 1990; Druga et al. 1993; Dávila et al. 2005; White et al. 2018), and molecular markers (Montiel et al. 2011; WZ Wang et al. 2011, Q Wang et al. 2017), or a combination of these (Grimstvedt et al. n.d.; Wang et al. 2022).”
BackgroundMethodInfluentialSelf-citation
From tetrapods to primates
Aboitiz, F., & Montiel, J. F. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00001-5 · Cited by 23 · see citing works
Self-citation
ATP released from astrocytes modulates action potential threshold and spontaneous excitatory postsynaptic currents in the neonatal rat prefrontal cortex
Beamer, E. H., Kovács, G., & Sperlágh, B. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.10.006 · Cited by 22 · see citing works
Initiation and developmental dynamics of Wfs1 expression in the context of neural differentiation and ER stress in mouse forebrain
Tekko, T., Lilleväli, K., Luuk, H., Sütt, S., Truu, L., Örd, T., Möls, M., & Vasar, E. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.03.009 · Cited by 22 · see citing works
“…VIb – both contain significant amount of transient cells, constitute a temporary target for corticothalamic or thalamocortical projections, and share common gene expression patterns (Price et al., 1997; Molnár and Cordery, 1999; Jacobs et al., 2007; Montiel et al., 2011; Grant et al., 2012).”
Background
Cortical layer with no known function
Molnár, Z. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13978 · Cited by 23 · see citing works
Self-citation
Function and Evolution of the Reptilian Cerebral Cortex
Naumann, R. K., & Laurent, G. (2016) · Evolution of Nervous Systems · doi:10.1016/b978-0-12-804042-3.00022-1 · Cited by 17 · see citing works
Genetic Elimination of Connective Tissue Growth Factor in the Forebrain Affects Subplate Neurons in the Cortex and Oligodendrocytes in the Underlying White Matter
Yu, I., Chang, H., Chen, K., Lu, Y., Shy, H.-T., Chen, C.-Y., Lee, K., & Lee, L. (2019) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2019.00016 · Cited by 15 · see citing works
“Nurr1 and Cplx3 are well-accepted makers for subplate neurons (Montiel et al., 2011) and these findings suggest that the subplate neuron-derived CTGF”
BackgroundInfluential
A novel, clinically relevant use of a piglet model to study the effects of anesthetics on the developing brain
Whitaker, E. E., Bissonnette, B., Miller, A. D., Koppert, T. L., Tobias, J. D., Pierson, C. R., & Christofi, F. L. (2016) · Clinical and Translational Medicine · doi:10.1186/s40169-015-0079-9 · Cited by 16 · see citing works
“The multilayer cortical sub-plate of the developing pig brain and the expression pattern of reelin, a glycoprotein that influences neuronal migration, are strongly analogous to the developing human brain [10, 19].”
Background
Cortical Columns
Molnár, Z. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397267-5.00137-0 · Cited by 16 · see citing works
Self-citation
Molecular Signatures in Cortical Development
Steyert, M. R., Li, T., Piao, X., & Nowakowski, T. J. (2025) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-091823-014001 · Cited by 15 · see citing works
Distinct Development of the Cerebral Cortex in Platypus and Echidna
Ashwell, K. W. S., & Hardman, C. D. (2011) · Brain Behavior and Evolution · doi:10.1159/000334188 · Cited by 13 · see citing works
“…adult life to perform functions similar to those of the therian claustrum, much as the persisting subplate neurons in deeper levels of the cortex of many eutherian mammals have an intimate relationship with the claustrum [Montiel et al., 2011], but this hypothesis requires further investigation.”
The first cortical circuits: Subplate neurons lead the way and shape cortical organization
Kanold, P. O. (2018) · e-Neuroforum · doi:10.1515/nf-2018-0010 · Cited by 12 · see citing works
“…profiling has enabled the study of subplate evolution, which has already identified subpopulations that are conserved across species, e. g., from birds to mammals, and other populations that seem to be specific to mammalian neocortex (Montiel et al., 2011; Wang et al., 2011; Molnar et al., 2014).”
Background
The distribution, number, and certain neurochemical identities of infracortical white matter neurons in the brains of a southern lesser galago, a black‐capped squirrel monkey, and a crested macaque
Swiegers, J., Bhagwandin, A., Maseko, B. C., Sherwood, C. C., Hård, T., Bertelsen, M. F., Spocter, M. A., Molnár, Z., & Manger, P. R. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25216 · Cited by 11 · see citing works
Self-citation
Continuity and change in neural plasticity through embryonic morphogenesis, fetal activity‐dependent synaptogenesis, and infant memory consolidation
Luu, P., & Tucker, D. M. (2023) · Developmental Psychobiology · doi:10.1002/dev.22439 · Cited by 11 · see citing works
Quantitative analysis of somatosensory cortex development in metatherians and monotremes, with comparison to the laboratory rat
Ashwell, K. W. S. (2014) · Somatosensory & Motor Research · doi:10.3109/08990220.2014.978849 · Cited by 9 · see citing works
“…Sheng et al. 1991; Balslev et al. 1992; Krause and Saunders 1994; Marotte et al. 1997; Molnár et al. 1998; Leamey et al. 2007), and in recent decades molecular analysis has been made of isocortical development in Monodelphis domestica (Cheung et al. 2010; Montiel et al. 2011; Wang et al. 2011).”
Background
Regional scattering of primate subplate
Molnár, Z., & Hoerder‐Suabedissen, A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611194113 · Cited by 10 · see citing works
Self-citation
The layer 6b theory of attention
Zolnik, T. A., Eickholt, B. J., Molnár, Z., & Larkum, M. E. (2026) · Neuron · doi:10.1016/j.neuron.2025.11.024 · Cited by 12 · see citing works
Self-citation
Correlation between the number of interstitial neurons of the white matter and number of neurons within cortical layers: Histological analyses in postnatal macaque
Ahmed, B., Duque, A., RAKIC, P. T., & Molnár, Z. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.25626 · Cited by 7 · see citing works
“However,thenovelandlargelyexpandedpopulationsofsubplateinthe primate might suggest that some of the subplate neurons have novel origin and novel functions in the developing and in the adult primate brain (Montiel et al., 2011).”
BackgroundSelf-citation
Seeking clues in brain development to explain the extraordinary evolution of language in humans
Clowry, G. J. (2014) · Language Sciences · doi:10.1016/j.langsci.2014.06.014 · Cited by 7 · see citing works
Development of reciprocal connections between the dorsal lateral geniculate nucleus and the thalamic reticular nucleus
Campbell, P. W., Govindaiah, G., & Guido, W. (2024) · Neural Development · doi:10.1186/s13064-024-00183-5 · Cited by 6 · see citing works
“Moreover this sectorial arrangement persists even in the absence of retinal innervation (see also [75, 76]), suggesting that the organization of TRN is determined largely by intrinsic guidance cues and seems impervious to alterations in signaling from the periphery [62, 77].”
Background
Expression of Cre Recombinase in Alveolar Epithelial Cells of the AQP2-Cre Transgenic Mini-Pigs
Luo, W., Li, Z., Li, P., Huang, Y., Han, Y., Yao, C., Zhang, Z., Yan, H., Pang, D., Ouyang, H., et al. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000366363 · Cited by 6 · see citing works
Quantitative analysis of somatosensory cortex development in eutherians, with a comparison with metatherians and monotremes
Ashwell, K. W. S. (2015) · Somatosensory & Motor Research · doi:10.3109/08990220.2015.1004046 · Cited by 6 · see citing works
“The sequence of events involved in production of the cerebral cortex and the sources of cortical neurons have been studied extensively in a narrow group of domesticated mammals (mainly mice, rats, cats, monkeys) and humans (Zecevic et al. 2005; Carney et al. 2007; Jones 2009; Montiel et al. 2011).”
Background
The need for research on human brain development
Molnár, Z. (2011) · Brain · doi:10.1093/brain/awr140 · Cited by 6 · see citing works
Self-citation
Function and Evolution of the Reptilian Cerebral Cortex
Naumann, R. K., & Laurent, G. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820584-6.00009-x · Cited by 5 · see citing works
The impact of different modes of neuronal migration on brain evolution
García‐Moreno, F., & Molnár, Z. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00025-0 · Cited by 4 · see citing works
Self-citation
Evolution of the Mammalian Brain with a Focus on the Whale Olfactory Bulb
Kishida, T. (2017) · Diversity and commonality in animals · doi:10.1007/978-4-431-56469-0_14 · Cited by 3 · see citing works
Basal Ganglia and Extrapyramidal System
Strominger, N. L., Demarest, R. J., & Laemle, L. B. (2012) · Humana Press eBooks · doi:10.1007/978-1-61779-779-8_24 · Cited by 2 · see citing works
Cortical evolution 2018: Advantages of animal model species
Martínez‐Cerdeño, V., & Noctor, S. C. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24536 · Cited by 1 · see citing works
“However there are important differences, for instance in the subplate zone (Montiel et al., 2011).”
Background
Cajal–Retzius and subplate cells: transient cortical neurons and circuits with long-term impact
Luhmann, H. J., Kilb, W., & Kirischuk, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-823672-7.00022-3 · Cited by 1 · see citing works
Early Neuronal Differentiation/patterning of the Human Pallium, Modeling by in Vitro Systems, and Disruption in Developmental Disorders
Scuderi, S., Jourdon, A., & Vaccarino, F. M. (2023) · Wiley eBooks · doi:10.1002/9781119860914.ch20 · Cited by 1 · see citing works
Development of feedforward and feedback connections between the dorsal lateral geniculate nucleus and the thalamic reticular nucleusPreprint
Campbell, P. W., Govindaiah, G., & Guido, W. (2024) · Research Square · doi:10.21203/rs.3.rs-4014221/v1 · Cited by 1 · see citing works
From inside-out to outside-in: cortical lamination development in the Reelin-deficient neocortex
Mingo-Moreno, N. (2019) · doi:10.53846/goediss-7335
Formation, organization, and synaptic properties of circuits between thalamic reticular nucleus and dorsal lateral geniculate nucleus.
Campbell, P. W. (2020) · doi:10.18297/etd/3420
Erratum
(2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25222
Faculty Opinions recommendation of Genetic elimination of connective tissue growth factor in the forebrain affects subplate neurons in the cortex and oligodendrocytes in the underlying white matter.
Molnár, Z., Hoerder‐Suabedissen, A., & Hayashi, S. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.735265206.793557828
Self-citation
Evolution and Development of Thalamocortical Relationships
Molnár, Z., Bandiera, S., & Clowry, G. J. (2023) · Oxford University Press eBooks · doi:10.1093/med/9780197676158.003.0058
Self-citation
Additional file 2 of Development of reciprocal connections between the dorsal lateral geniculate nucleus and the thalamic reticular nucleus
Campbell, P. W., Govindaiah, G., & Guido, W. (2024) · Figshare · doi:10.6084/m9.figshare.26061543
Additional file 1 of Development of reciprocal connections between the dorsal lateral geniculate nucleus and the thalamic reticular nucleus
Campbell, P. W., Govindaiah, G., & Guido, W. (2024) · Figshare · doi:10.6084/m9.figshare.26061452
Assembling layer 1 of the neocortex : roles of Cajal-Retzius cells
Genescu, I. (2020) · theses.fr (ABES) · doi:10.70675/3fe1b21cz5c6bz4150z94e6zd77163aba0ad
Microglial maturation across human and mouse as a reference for interpreting large-animal models of perinatal brain injury
Shearer, I. K., Antonson, A. M., Steenwinckel, J. V., Gressèns, P., Tolcos, M., Walker, D., Spencer, S. J., Johnson, R., & Fleiss, B. (2026) · Pediatric Research · doi:10.1038/s41390-026-05355-z

Reviewed by:
Montiel, J. F., Wang, W. Z., Oeschger, F. M., Hoerder‐Suabedissen, A., Tung, W. L., García-moreno, O., Holm, I. E., Villalón, A., Molnár, Z., Kanold, P. O., et al. (2011)
Self-citation
Dual Developmental Origins and Activity-dependent Specification of Mammalian Subplate NeuronsPreprint
Kumamoto, T., Hara, Y., Katayama, R., Aota, I., Achiwa, H., Noguchi, Y., Gotoh-Saito, S., Wada, R., Hasegawa, H., Nakajima, K., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.12.731985
Comparative Aspects of Subplate Zone Studied with Gene Expression in Sauropsids and Mammals
Wang, W. Z., Oeschger, F. M., Montiel, J. F., García-Moreno, F., Hoerder-Suabedissen, A., Krubitzer, L., Ek, C. J., Saunders, N. R., Reim, K., Villalón, A., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq278 · Cited by 76 · see citing works
Self-citation
In search of common developmental and evolutionary origin of the claustrum and subplate
Bruguier, H., Suarez, R., Manger, P., Hoerder‐Suabedissen, A., Shelton, A. M., Oliver, D. K., Packer, A. M., Ferran, J. L., García‐Moreno, F., Puelles, L., et al. (2020) · Journal of Comparative Neurology · doi:10.1002/cne.24922 · Cited by 84 · see citing works
Self-citation
Cerebral Cortex doi:10.1093/cercor/bhq278 Comparative Aspects of Subplate Zone Studied with Gene Expression in Sauropsids and Mammals
Wang, W. Z., Oeschger, F. M., Montiel, J. F., & Hoerder‐Suabedissen, A. (2016)
Self-citation

Authors: Montiel, J. F., Wang, W. Z., Oeschger, F. M., Hoerder-Suabedissen, A., Tung, W. L., García-Moreno, F., Holm, I. E., Villalón, A., & Molnár, Z.
Affiliations: University of Oxford (GB)
Aarhus University (DK)
Universidad Diego Portales (CL)
Corresponding author: Montiel, Juan F.
Molnár, Zoltán
ORCID: Montiel, Juan F.
Molnár, Zoltán
Venue: Frontiers in Neuroanatomy
Publisher: Frontiers Media SA
Published: 2011
Volume: 5
Pages: 25-25
ISSN: 1662-5129 (ISSN-L)
DOI: 10.3389/fnana.2011.00025
PMC: PMC3078748
OpenAlex: W1982422375
Cited by: 70
References: 135
Citations by year: 2026: 2 · 2025: 2 · 2024: 5 · 2023: 3 · 2022: 2 · 2021: 2 · 2020: 8 · 2019: 4 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 5 · 2014: 9 · 2013: 6 · 2012: 6
FWCI: 2.52
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Neuroanatomy (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Americanae (AECID Library) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
Funders: HistoGenetics
Medical Research Council (G00900901)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: neocortex evolution, dorsal pallium, hodology, marsupials, primates

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Hypothesis on the Dual Origin of the Mammalian Subplate

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